2020, Scott, Essential Ornithology, Second Edition

OUP CORRECTED PROOF – FINAL, 27/08/20, SPi
Essential Ornithology
Essential Ornithology
Second Edition
Graham Scott
Director, Teaching Excellence Academy, University of Hull, UK
1
1
Great Clarendon Street, Oxford, OX2 6DP,
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DOI: 10.1093/oso/9780198804741.001.0001
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For Lisa and Adam who have been very, very patient (again),
for my parents, Mary and Bill who indulged my passion for birds,
and for Will who keeps me birding!
Preface
As was the case with the first edition of Essential I remain aware that in places I could have included
Ornithology this book is intended to be an introduc- more depth, and that in places I could have provided
tion to what I consider to be the essentials of orni- a broader treatment, but my aim was once again to
thology; those areas of the broader biology of birds produce a relatively short useful text and so I was
that are, in my view, the minimum that a student of unable to follow through every avenue of thought—
ornithology should know. In writing the second no matter how much I should have liked to!
edition I have attempted to take on board feedback Instead, by covering a breadth of material and by
that I have had from students (my own included) restricting myself to case studies that should be
and from teachers who I am pleased to say have accessible to all, I hope that I have provided the
found Essential Ornithology to be a useful resource. reader with a ‘way in’ to academic ornithology.
Essential Ornithology. Second Edition. Graham Scott, Oxford University Press (2020). © Graham Scott (2020).
DOI: 10.1093/oso/9780198804741.001.0001
Acknowledgements
A book such as this one may have a single assisted in the publication progress. At the risk of
author—but it would be impossible to write with- missing any one of them, they are: Lisa Scott, Will
out access to all of the published works produced Scott, Bill Scott, Phil Wheeler, Margaret Boyd,
by active researchers/writers in ornithology; I am James Spencer, Robin Arundale, Peter Dunn, Ian
indebted to them all. Similarly, I owe a debt of Robinson, Ian Grier, Les Hatton, Shirley Millar,
thanks to friends and colleagues who have pro- Andy Gosler, Stanislav Pribil, Sjirk Geets, Kyle
vided their views on sections of the text; provided Elliott, José Tella, Simone Tenório, and the very
most of the pictures that are included in it, and patient Ian Sherman.
DOI: 10.1093/oso/9780198804741.001.0001
Contents
1 Evolution of birds 1
1.1 Birds are dinosaurs 1
1.2 Archaeopteryx 3
1.3 The evolution of modern birds 6
1.4 The phylogeny of birds 7
1.4.1 Morphological phylogeny 7
1.4.2 Character conservation and convergence 7
1.4.3 Biomolecular phylogeny 8
1.5 Adaptive radiation and speciation 10
1.5.1 Darwin’s finches 10
1.5.2 Genes and evolution 13
1.5.3 Hybrids 13
Summary 17
Appendix 1 Familiar names of the members of the Orders
and Families of modern birds 17
2 Feathers and flight 21

2.1 Feathers 21
2.1.1 Feather types 21
2.1.2 Contour feathers 22
2.1.3 Down feathers and semiplumes 22
2.2 Feather tracts 24
2.3 Feather colour 26
2.4 Feather damage 26
2.5 Feather maintenance 28
2.6 Moult 28
2.6.1 Moult strategies 30
2.7 Flight 33
2.7.1 Gliding and soaring 34
2.7.2 Flapping flight 36
2.7.3 Respiration and flight energetics 38
2.7.4 Flying high 39
2.7.5 Flight speeds 41
2.8 The evolution of flight and flightlessness 45
Summary 47
xi
xii CONTENTS
3 Movement: migration and navigation 48

3.1 The ecology of migration 51
3.2 Genes and migration 52
3.3 Physiology and migration 57
3.3.1 Seasonality and coordination of migration 57
3.3.2 Hormones and the control of migration 58
3.3.3 Fuelling migration 59
3.3.4 Long haul flights 62
3.4 The weather and migration 63
3.5 Navigation 65
3.5.1 Navigational cues 68
Summary 72
4 Eggs, nests, and chicks 73

4.1 Sex and the gonads of birds 73
4.2 The egg 75
4.3 Clutch size 77
4.4 Egg shell colouration and patterning 81
4.4.1 Camouflage 81
4.4.2 Egg mimicry 82
4.4.3 Egg recognition 82
4.4.4 Signals of quality 84
4.4.5 Pigments and shell quality 84
4.5 Nests 85
4.6 Incubation 87
4.7 Hatching 91
4.8 Chicks 91
Summary 93
5 Reproduction 94
5.1 Males and females are different 94
5.2 Mating systems 97
5.3 Courtship and mate choice 99
5.3.1 Resource provision 99
5.3.2 Ornaments and displays 101
5.3.3 Sharing a mate 101
5.4 Song 105
5.4.1 Song learning 106
5.4.2 Functions of song 107
5.4.3 Synchronized singing 110
5.5 Raising a family 113
5.5.1 Begging 113
5.5.2 Imprinting and independence 118
Summary 119
CONTENTS xiii
6 Foraging and avoiding predators 120

6.1 Finding food and capturing prey 120
6.1.1 Sharing information 122
6.1.2 Foraging flocks 123
6.1.3 Do herbivores cooperate? 125
6.2 Optimal foraging 125
6.2.1 Feeding territories 126
6.3 Risk and foraging 130
6.4 Predator avoidance 131
6.4.1 Camouflage 131
6.4.2 Predator distraction displays 132
6.4.3 Tonic immobility 133
6.4.4 Alarm calls 134
6.4.5 Mobbing 136
6.4.6 Flocks and colonies 136
Summary 139
7 Populations, communities, and conservation 140

7.1 Populations 140
7.1.1 Life history strategies influence population growth 140
7.1.2 Population change 142
7.2 Communities 144
7.2.1 Communities are dynamic 145
7.2.2 Niche divergence 147
7.2.3 Niche shifts, ecological release, and competition 148
7.3 Extinction and conservation 150
7.3.1 Conservation can be a success 151
7.3.2 The task that faces us as ornithologists 153
Summary 154
Index 155
C H A PT ER 1
Evolution of birds
‘Creation is never over. It had a beginning but it has no ending.’

Immanuel Kant, A General Natural
History of the Heavens (1755)
I often ask my students, ‘what is a bird?’, it’s a ques- to flight and will be discussed in more detail in
tion that I was asked when I was a student and then chapter 2. Here in chapter 1, I want to consider not
as now the most common answer is ‘a flying verte- so much what birds are, but rather to explore their
brate’. Well of course this is only partly right. Birds, evolutionary history.
like fish, amphibians, reptiles, and mammals do And the answer to my opening question? Well I
have vertebrae (and the other defining characteris- vividly recall my own incredulity as a student when
tics of that group) and are therefore vertebrates— my smiling tutor declared ‘Birds are the last of the
but not all birds fly, nor are all flying vertebrates dinosaurs!’
birds (what about bats?). In practice it can be sur-
prisingly difficult to define a bird, although we all
know what one is. A feathered vertebrate may do Chapter overview
the job because the only extant vertebrates to have
feathers are the birds. Feathers however can no 1.1 Birds are dinosaurs
longer be claimed to belong uniquely to the birds 1.2 Archaeopteryx
following the discovery of fossilized specimens of a 1.3 The evolution of modern birds
number of feathered dinosaurs such as Ornithomimus 1.4 The phylogeny of birds
and Sinosauropteryx. Many of the other defining fea- 1.5 Adaptive radiation and speciation
tures of birds are in fact shared with one or more
vertebrate groups and so only set birds apart when
1.1 Birds are dinosaurs
considered in concert. Like most reptiles they lay
eggs and their young develop outside of the body Although the first suggestions that birds might be
of the parent. Like crocodilians and mammals related to reptiles were made when Archaeopteryx
they have a four-chambered heart. Like mammals was first described in the 1860s, it wasn’t until late in
they are warm blooded and have a high metabolic the twentieth century that the idea that birds evolved
rate, which in turn requires that they feed regularly. from dinosaurs began to be generally accepted.
Uniquely among vertebrates they lack teeth and There were initially two main theories to explain the
have a beak. They have bones that are pneumatized evolutionary origins of birds. Both agreed that birds
(they have air-filled cavities) and are therefore light arose from reptiles, as of course did mammals. But
compared with the solid bones of other vertebrates, whereas the mammals were thought to have their
their clavicles are fused to form a furcula or wish- origins in the synapsid reptiles, the birds were
bone, and they have a deeply keeled sternum for thought to have evolved from the diapsid reptiles.
the attachment of large flight muscles. These and The numerous species of lizard and snake living
many other features particular to birds are related today are diapsids, but to uncover the evolutionary
DOI: 10.1093/oso/9780198804741.003.0001
2 ESSENTIAL ORNITHOLOGY
roots of birds we need to look back to the now extinct

Concept
archosaurs, perhaps the most successful of the
Synapsids vs diapsids
diapsid groups historically—giving rise as it did to
Reptiles are classified into one of two types depending
the thecodonts, the pterosaurs, and most notably to
upon the morphology of the skull, or more precisely
the dinosaurs. From the fossil record it has become upon the arrangement of fenestrae (windows) in the
increasingly apparent that birds evolved from dino- skull. Synapsid reptiles have a single fenestration behind
saurs over a period of some 100 million years, grad- the eye socket, whereas the skulls of diapsids have two,
ually developing the features of modern birds one above the other. As a result diapsids have a lighter
(Figure 1.1). It is also apparent that their closest and generally more ‘open’ skull. They also tend to have
dinosaur relatives are the small, fast, feathered, and a lighter skeleton and more slender body—they are
perhaps relatively intelligent (by virtue of large more bird-like.
brain size) dromaesaurs such as Velociraptor.
Confuciusornithiformes
Hesperornithiformes
Dromaeosauridae
Oviraptorosauria
Enantiornithes
Archaeopteryx
Tyrannosaurus
omithischians
Troodontidae
Amphibians
Neornithes
Ichthyomis
Sauropods
Jeholomis
crocodiles
Mammals
Sapeornis
Lizards
Vorona
Cz
66
Cretaceous
145 130 120 100
Ornithurae
Ornithuromorpha
Ornithorthoraces
Pygostylia
Avialae/Aves (Birds) Keeled

174 163
sternum
Jurassic
Paraves Pygostyle
Wings
(fused tail)
Maniraptora
201
Theropoda/Coelurosauria Vaned feathers

Triassic
Furcula (wishbone)
237
Saurischia
Dinosauria Simple filamentous feathers
250
Archosauria
Diapsida
Amniota
Tetrapoda
Hinge-like ankle
Figure 1.1 A summary phylogeny of birds. This genealogical tree shows the relationship between the birds, their dinosaur ancestors, and the
wider vertebrate tree. The thick line between the Cretaceous and the Cenozoic (CZ) represents the asteroid impact-induced mass extinction event
and the arrows above that line show which lineages survived that event. From the figure it can be seen that the anatomical features of birds
evolved over a period of around 100 million years. Adapted from Brusatte, S.L., O’Connor, J.K., and Jarvis, E.D. (2015) The Origin and Diversification
of Birds. Current Biology 25(19), R888-R898. With permission from Elsevier.
EVOLUTION OF BIRDS 3
announced from the same region—that of an almost

Flight path: evolution of feathers and flight,
complete feathered skeleton (called the London speci-
pages 26 and 45.
men it resides in London at the Natural History
Museum, Figure 1.2 is the more complete Berlin speci-
1.2 Archaeopteryx
men). A bird—but not just a bird, a bird with reptilian
In 1860, just one year after the publication of Charles or dinosaur features—exactly the putative ‘missing
Darwin’s world-changing book On the Origin of link’ that Darwin had predicted in his book. This
Species, a fossil was discovered in the Solnhofen fossil was destined to become one of the most famil-
lithographic limestone of southern Germany that iar and at the same time most fiercely debated in
caused a sensation. The fossil was that of a single history. It is important to note that although I have
secondary flight feather and it was the first conclu- used the word ‘bird’ to describe Archaeopteryx, I have
sive evidence of the existence of prehistoric birds. done so in the sense that it is a member of the group
Within weeks, in 1861, a second fossil was Aves, a group that is represented in the extant fauna
Figure 1.2 Archaeopteryx

Archaeoptery lithographica, the Berlin
specimen. © Markéta Machovà, from
Pixabay.
by the Neornithes, the members of which are the facilitated the limb flapping essential for flight. So
modern birds. perhaps it did fly in the true sense of the word.
From the handful of Archaeopteryx fossils that It does seem to have been at home on the ground
have been discovered we now know that it was and has relatively long/strong running legs—perhaps
feathered in a way consistent with flight and that it it was a wader, or darted through scrub like a
had a broadly bird like skeleton (Figure 1.3). However, modern Roadrunner Geococcyx sp. Significantly it
because it lacked the well developed sternal keel of had an arrangement of toes similar to that of mod-
the modern birds we cannot be sure that it was ern perching birds, three of them pointing forwards
capable of powered flight and so it may have been and one pointing backwards. This backwards-
more of an accomplished glider. But then again it pointing toe, which is properly termed the hallux, is
did have a reduced pelvis (like modern flying not found in any of the known non-avian dinosaurs.
birds), an enlarged furcula (wishbone) and corac- It had well developed forelimbs and in fact these
oid, and a broad sternum, all of which would have may have been more important in locomotion than
3
4
5
(B)
(A)
Figure 1.3 The skeleton of Archaeopteryx (A) in comparison with that of a modern domestic pigeon (B). Note the expansion of the modern brain
case (1), the fusion of the modern hand bones (the wing) (2), the fusion of the pelvic bones and reduction of the tail to form the modern pygostyle
(3 and 4), the development of the sternum in the modern birds (to facilitate the attachment of large flight muscles (5), and the strengthening of
the modern rib cage (6). From Colbert, E.H. (1955) Evolution of vertebrates. John Wiley and Sons Inc., New York.
the legs, being longer, stronger, and equipped with reconstructions of the conditions at the time that the
claws. Perhaps it swam like a young Hoatzin fossil bearing sediments were laid down suggest
Opisthacomus hoazin. It had fingers suited to climb- a habitat of scrubby islands in shallow lagoons.
ing and it had claws typical in curvature of modern A predatory habit is further supported by the sug-
perching birds (Figure 1.4). We know this because gestion that this was a large-eyed animal with a
of the work of Derek Yalden and Alan Feduccia who degree of binocular vision and a larger brain capacity
have obtained curvature measurements of the claws than contemporary animals (although not yet on a
of a large number of species of living bird and shown par with modern birds).
that they form three natural groupings: ground dwell- Although Archaeopteryx does have a significant
ers like the pheasants with relatively straight claws, role to play in the story of the evolution of birds, it
tree climbers like the woodpeckers with strongly is not in itself the ancestor of the birds we see today.
curved claws, and perching birds like the finches It seems more likely that it represents a dead-end
with intermediate claw curvature. The mean claw branch on the bird evolutionary tree; one that died
curvature value of the available Archaeopteryx speci- out before the end of the Jurassic period (145.5 million
mens together with the presence of the backwards- years ago (mya)).
pointing hallux makes it highly likely that this was
a bird capable of perching.
Classification and the nomenclature of birds,
Key reference
an example
Yalden, D.W. (1985) Forelimb function in The House Sparrow:
Archaeopteryx. In The Beginnings of Birds. Hecht, M.,
Ostrom, J., Viohl, G., and Wellnhofer, P. (eds) Freunde Class Aves
des Jura-museum, Eichstätt. Subclass Neornithines
Superorder Neognathae
The teeth of Archaeopteryx suggest a carnivorous Order Passeriformes
Family Passeridae
diet and it may be that the clawed hands were used
Genus Passer
to catch and grasp large invertebrates or small verte-
Species domesticus
brates. Perhaps it ate fish—after all, palaeoecological
200
180
160
140
Claw (Curvature)
120
100 Climbers
80
Perchers Figure 1.4 The variation in claw curvature in 30 species of
60 modern bird, grouped according to life-style characteristics. The
40 mean curvature of the claws of fossilized Archaeopteryx foot
claws are plotted as a solid line (amongst the perchers), those of
20 Ground
the hand/wing are plotted as a solid line amongst the climbers.
0 From Feduccia, A. (1993) Evidence from claw geometry indicating
0 10 20 30 arboreal habits of Archaeopteryx. Science 259, 790–3. Reprinted
Species with permission from AAAS.
1.3 The evolution of modern birds were flightless). There are of course no toothed mod-
ern birds (hence the expression ‘as rare as hens’
Since the discovery of Archaeopteryx, new fossil finds teeth’). The Icthyornithiformes and Hesperornithiformes
have considerably enhanced our understanding of occur in the fossil record right up to the end of the
the evolution of the modern birds from their dino- Cretaceous but none are found in the next geological
saur ancestors. It is also becoming increasingly evi- time period, the Triassic. This is because 66 mya at
dent that many of the key features of birds evolved the Cretaceous/Triassic (K/T) boundary an asteroid
initially in the dinosaur ancestors and as Figure 1.1 collided with the earth and triggered the mass
indicates, the transition from dinosaur to bird was extinction event that wiped out some 75 per cent of
a gradual one, taking place over millions of years. life on the planet, including the dinosaurs and the
In the 1990s the fossilized remains of a significant avian ancestors of the modern birds.
number of feathered dinosaurs were discovered in
the Liaoning province of northeast China (a collec-
Key references
tion of fossils referred to as the Jehol biota). They
Feduccia, A. (2014) Avian extinction at the end of the
included primitive birds similar at some levels to
Cretaceous: Assessing the magnitude and subsequent
Archaeopteryx and specimens that possessed the fea- explosive radiation. Cretaceous Research 50, 1–15.
tures of more modern birds, indicating that the bird Jarvis, E.D., Mirarab, S., Aberer, A.J., et al. (2014)
lineage had diversified considerable by the early Whole-genome analyses resolve early branches in the
Cretaceous (145–100 mya). tree of life of modern birds. Science 346(6251),
The fossils included species like Sinosauropteryx 1320–31.
prima a small (1 m long), bipedal dinosaur (125 mya) Jetz, W., Thomas, G.H., Joy, J.B., et al. (2012) The global
that was partially covered with bristle-like struc- diversity of birds in space and time. Nature 491, 444–8.
tures that are thought to be simple filamentous
feathers. Another of the Liaoning fossils, Microraptor There is strong fossil evidence that this event
gui (120 mya) had plumulaceous feathers on its head resulted in the extinction of the majority of the bird
and body and long asymmetrical pennaceous feathers lineages that had evolved through the Cretaceous
on its tail and on both its fore and hind limbs (yes it period. Alan Feduccia has described the fossil
had four wings!), these feathers closely resemble record at the K/T boundary as being scrappy and as
those of modern birds. Microraptor could certainly a result it is currently difficult to be absolutely cer-
glide and, because it had feathers like those of mod- tain, on the basis of paleontological evidence, which
ern birds, it may have been able to exert some con- types of birds had survived the mass extinction,
trol over its flight. But because it lacked the skeletal and which therefore diversified prior to it. But there
structures required for the attachment of large breast is some fossil evidence to support the idea that the
muscles and had a long flexible tail (not good for in- true modern birds evolved towards the end of the
flight control) it may not have been capable of true Cretaceous and that the survivors of the mass
powered flight. The tail bones of modern birds are extinction were shorebirds or water birds. Erich
fused during embryological development to form Jarvis and his colleagues have used molecular tech-
the pygostyle (perhaps familiar to you as the bony niques to shed further light on this period of the
part of the ‘parsons nose’ of a chicken). The pygo- evolution of birds. Through a whole genome com-
style provides a solid support for the tail feathers, parison of the extant orders of birds, they have
enabling them to be moved during flight so that the determined that the modern birds did diverge from
bird can maintain flight path control. The earliest their ancestors during the late Cretaceous. Their
examples of pygostyle-like structures are found in analyses date the divergence of the two major groups
fossils from the early Cretaceous period, like those of modern birds; the Palaeognathae (Tinamous and
of Confuciusornis a primitive bird that also possessed Ostriches) and the Neognathae (all other modern
a toothless beak. Interestingly Confuciusornis is a birds) to the late Cretaceous (around 100 mya).
contemporary of the fish-eating and tooth-beaked The Neognathae subsequently diverged to form
Icthyornithiformes (gull-like flying birds) and the Galloanseres (the waterfowl) and the Neoaves
Hesperornithiformes (diver-like birds, some of which around 90 mya. Then, during the K/T transition
(around 66 mya), there was a period of rapid (10–15 world’s avifauna. Passerines also occupy a bewilder-
million years) evolutionary radiation as species ing array of ecological niches and exhibit an amazing
evolved to take advantage of the diversity of eco- range of morphologies. However we can be confi-
logical niches left empty as a result of the asteroid dent that they form what is known as a monophy-
impact and all of the modern sub-groups became letic group, i.e. all of the current passerine species
established. Moreover, phylogenetic analyses car- have evolved from a single common ancestor.
ried out by Walter Jetz and his colleagues have We know this because all passerine birds share
shown that during the last 50 million years there features in common that are unique to the passerine
has been a significant increase in the rate of species’ order. For example, most birds have a preen gland
diversification particularly among the Passeriformes (or uropygial gland) low on their back, just above the
(songbirds) and the Anseriformes (waterfowl). base of the tail. This gland produces an oily secretion
that is used by birds to maintain the physical quality
Concept of their feathers and to regulate bacterial and fungal
Dating evolutionary change
communities that grow on them. In the case of aquatic
Palaeontologists are able to date fossil remains through birds the preen gland is particularly large and its
their association with sediment deposits of known
secretions are important in feather water-proofing.
age—i.e. they use a geological clock. Molecular
Preen glands vary in their structure but all passerines
biologists on the other hand are able to calibrate
share a unique preen gland morphology. The pas-
rates of gene mutation within organisms through
evolutionary time—i.e. they use a molecular clock. serines also all share a unique sperm morphology.
The spermatozoa of the birds of most orders are
straight whereas those of the passerines are helical
1.4 The phylogeny of birds in structure and move forwards via a spinning
action. The passerine preen gland and sperm type
1.4.1 Morphological phylogeny are therefore conserved characters; i.e. they have
There is at present no single accepted phylogeny of evolved once in the early passerine ancestor and
the modern birds, that is to say we do not yet have a been retained throughout the passerine radiation.
definitive statement of the evolutionary relationships Generally those characters that remain fixed in
of different groupings of birds. Traditionally taxon- the face of ecological adaptation, so called conserva-
omists have attempted to uncover evolutionary relative characters, are the most useful in classification.
tionships through the comparison of morphological Where characters do respond readily to ecological
characters. Figure 1.3 provides an example of this selection pressures convergence in evolution may lead
kind of comparison, the bones highlighted are basic to confusion in apparent relationships. For example,
characters shared by both Archaeopteryx and the mod- all passerine birds have a foot that is adapted for
ern domestic pigeon. If we were to add to this com- perching, having three forward and one backward
parison the skeleton of a Passenger Pigeon Ectopistes pointing toes. This toe arrangement is termed aniso-
migratorius we would be able to use the closer simi- dactyly and is illustrated in Figure 1.5.
larities between the two pigeons than between either Anisodactyly is a conserved character that can
and Archaeopteryx to infer that the pigeons were the be used to confirm membership of the passerine
more closely related pair in an evolutionary sense. order (because it is only exhibited by birds that also
exhibit all of the other uniquely passerine features).
It has evolved once in the passerine ancestor and
1.4.2 Character conservation and convergence has been retained thereafter. Figure 1.5 also illustrates
However, it is not always the case that apparent an alternative toe arrangement—zygodactyly. The
similarity of shared characters equates to close evo- zygodactyl foot does not indicate membership of a
lutionary ties. The order Passeriformae comprises single order. In fact close examination of the precise
more than 5,000 species or more than half of all arrangement of bones of the foot suggests that zygo-
extant bird species. As such they can reasonably be dactyly is an example of character convergence; i.e. it
described as being the dominant component of the has evolved on a number of independent occasions
Anisodactyl
3
2 4
1
Blue Jay (Cyanocitta cristata)
Zygodactyl
2 3
1 4
Grey-faced Woodpecker (Picis canus)
Figure 1.5 Examples of the toe arrangements of two modern birds: the anisodactyl Blue Jay Cyanocitta cristata, a perching bird (A); and the
zygodactyl Grey-faced Woodpecker Picis canus, a climbing bird (B). These are just two of 15 different avian toe arrangements. Adapted from
Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
in a range of unrelated species and orders including

Mitochondria, the powerhouses of our cells, also
the Osprey Pandion haliaetus, the woodpeckers
each contain a small circle of DNA. This mtDNA we
(Picidae), the owls (Strigidae), and some swifts inherit only from our mothers.
(Apodidae). When genes are inherited they may change, either as
Not all of the characters used in taxonomy are a result of the recombination of nuclear DNA from two
skeletal/anatomical however and comparisons of parental sources, or as a result of mutations, accidental
plumage, behaviour, vocalizations, and even copying errors in either nuclear DNA or mtDNA.
ectoparasites have all been used in attempts to elu-
cidate avian evolutionary relationships. But per-
Key references
haps the most exciting development in efforts to
Sibley, C.G. and Ahlquist, J.E. (1990) Phylogeny and
unravel the avian phylogenetic tree in recent times classification of birds. Yale University Press, New Haven.
is the use of biomolecular information—informa- Jarvis, E.D., Mirarab, A., Aberer, A.J., et al. (2014) Whole
tion about genes and their chemical products. genome analyses resolve early branches in the tree of
life of modern birds. Science 346(6215), 1320–31.
Concept Prum, R.O., Berv, J.S., Field, D.J., et al. (2015) A
DNA deoxyribonucleic acid comprehensive phylogeny of birds (Aves) using targeted
The nuclei of our cells contain chromosomes; paired next-generation sequencing. Nature 526, 569–73.
strands of DNA arranged in the iconic double helix with
which we are all no doubt familiar.
Sequences of the basic units of these strands act 1.4.3 Biomolecular phylogeny
as templates for the production of proteins—these
In 1990 Sibley and Ahlquist published a phylogeny
templates are our genes. We inherit one strand of each
of avian families based on the process of DNA-DNA
of our chromosomes from our father and one from our
mother.
hybridization. In simple terms they directly compared
the chemical structure of the DNA of different bird
species. Their work pioneered the use of biochemical have been numerous attempts to elucidate the rela-
characters in avian phylogeny, but their results did tionships of the extant bird taxa and almost 300
not produce a definitive avian tree and were limited putative trees had been published during the 30
because of the small units of DNA used and there- years prior to my writing this. Attempts to arrive at
fore the limited number of characters involved in a definitive phylogeny are dogged by data availabil-
tree construction. Subsequent workers in the field ity and trees vary depending upon the method and
have used improved molecular techniques to gain a data used to construct them. However, Sushma
better level of discrimination between taxa, particu- Reddy and her colleagues have carried out an analysis
larly but not exclusively, at the species level, comparing a number of recently proposed phyloge-
through the comparison of mitochondrial DNA and nies and the methodologies used in their construc-
nuclear gene sequences. I began this section by stat- tion and have proposed the consensus tree that I
ing that there is no single accepted phylogeny of have included as Figure 1.6. But this is an exciting
birds and that remains the case. Since the publica- and rapidly moving field and I would recommend
tion of the first molecular phylogeny of birds there that any student with an interest in this area regularly
Ostrich Struthioniformes
Tinamous Tinamiformes
Waterfowl Anseriformes
Landfowl Galliformes
Flamingos Phoenicopteriformes
Grebes Podicipediformes
Doves Columbiformes
Sandgrouse Pterocliformes
Mesites Mesitornithiformes
Shorebirds Charadriiformes
Cranes, Rails Gruiformes
Hoatzin Opisthocomiformes
Nightjars & allies Caprimulgiformes
Swifts Caprimulgiformes
Hummingbirds Caprimulgiformes
Turacos Musophagiformes
Bustards Otidiformes
Cuckoos Cuculiformes
Tropicbirds Phaethontiformes
Sunbittern Eurypygiformes
Loons Gaviiformes
Pelicans & allies Pelecaniformes
Tubenoses Procellariiformes
Penguins Sphenisciformes
New World vultures Accipitriformes
Eagles, Hawks Accipitriformes
Owls Strigiformes
Mousebirds Coliiformes
Cuckoo-roller Leptosomiformes
Trogons Trogoniformes Figure 1.6 A phylogeny of birds. Adapted from
Hornbills & allies Bucerotiformes Reddy, S., Kimball, R.T., Pandey, A., et al. (2017) Why
Bee-eaters& allies Coraciiformes do phylogenetic data sets yield conflicting trees? Data
Woodpeckers & allies Piciformes type influences the avian tree of life more than taxon
Seriemas Cariamiformes sampling. Systematic Biology 66(5), 857–79, by
Falcons Falconiformes permission of Oxford University Press. The tree is a
Parrots Psittaciformes consensus of their own Early Bird II tree and trees
Passerines Psittaciformes previously proposed by Erich Jarvis and Richard Prum.
consult the excellent websites https://tree.open occupy their own feeding niche. As such their bills
treeoflife.org and the Encyclopedia of Life http:// and associated mode of feeding can be described as
www.eol.org for updates. evolutionary adaptations which enhance their indi-
vidual survival by reducing the interspecific com-
petition that they experience.
1.5 Adaptive radiation and speciation
The observed diversity in bill morphology is one
One of the first things that a bird watcher notices is visible outcome of a process of adaptive radiation—
that there is an amazing diversity of form even we can presume that at one time the ancestral
within groups of closely related bird species. Living, Charidriiform bill was pretty uniform, but that
as I do, on the coast, the bills of the wading birds are through evolutionary time and in parallel with the
my favourite example of this phenomenon. I regu- evolution of all of the various wader species, it has
larly see as many as a dozen species feeding along evolved as a result of natural selection.
the same area of shore, all of them members of the
same order the Charidriiformes, but ranging in bill
morphology from the tiny, straight bill of the Little 1.5.1 Darwin’s finches
Ringed Plover Charidrius dubius used to delicately This is the same phenomenon that has given rise to
pick isopods from the strand line, to the long de- perhaps the most iconic of examples of adaptive
curved bill of the Eurasian Curlew Numenius arquata radiation, that of the finches of the Galapagos and
used to probe deep into wet sand to drag out large Cocos Islands. There are 15 species of so-called
polychaetes, to the heavy hammering bill of the Galapagos finch, 14 of them are endemic to the
Eurasian Oystercatcher Haematopus ostralegus ideal Galapagos Islands and one is only found on the
for smashing open the shells of bivalve molluscs Cocos Islands. Galapagos, or Darwin’s finches as
(Figure 1.7). they are also often called (Charles Darwin did col-
lect the first specimens of these species, but they
Flight path: foraging behaviour and the concept of
niche, page 147. were not quite as pivotal in the development of his
ideas as is often assumed to be the case) have been
This diversity of bill shape allows the birds to coexist presumed to have evolved from an ancestral spe-
without competing too closely for food—they each cies that accidentally colonized these isolated
Eurasian Little
Eurasian Bar-tailed Oyster- Common Red Gray Ringed Ruddy
Curlew Godwit catcher Redshank Knot Plover Plover Turnstone
4 cm
Figure 1.7 Because their bill morphology varies, species of wading shore birds are able to forage alongside one another with minimal
competition. From Gill, F.B. (2007) Ornithology. 3rd edn Freeman, New York (after Goss-Custard, J.D. (1975) Beach feast. Birds
September/October 23–6).
islands from the South American mainland close to The early colonists probably arrived on just one of
1,000 km away. Through the comparison of nuclear the islands and found an environment devoid of
DNA and mtDNA sequences of the Galapagos competition but rich in potential resources. They
finches and a range of putative mainland relatives, are presumed to have formed a self-sustaining
Sato and colleagues have recently deduced that the population from which groups of individuals went
closest living mainland relative of the Galapagos on to eventually colonize the other islands in the
finches is the Dull-coloured Grassquit Tiaris obscura, group. Living on these isolated islands, each popu-
a species which inhabits humid forest edges, farm- lation of birds may have become a specialist in the
land, and scrub throughout Venezuela, Colombia, exploitation of a particular resource and through the
western Ecuador, and western and southern Peru, process of natural selection their populations will have
habitats not dissimilar to those encountered in the diverged from one another in terms of ecology, behav-
islands by the colonists. T. obscura is not the direct iour, and crucially, genetics. Through time these iso-
ancestor of the Galapagos finches, but it is likely lated populations of birds may have diverged from
that they shared a common ancestor. one another to such a level that, if two populations
were to re-colonize the same island and coexist, they
Key reference would remain isolated from one another in the
Sato, A., Tichy, H., O’hUigin, C., et al. (2001) On the sense that they would have evolved to become sep-
Origin of Darwin’s Finches. Molecular Biology and arate species.
Evolution 18(3), 299–311. The coexistence of two or more finch species on a
single island would probably have increased the
rate of divergence as birds increased their levels of
Concept behavioural/ecological isolation from one another
Species
as they became increasingly specialized to avoid
The species is the unit we use to measure biological interspecific competition. Box 1.1 provides more
diversity. Typically species are defined as populations of
information about natural selection and the results
potentially interbreeding individuals that are reproductively
of a natural experiment that demonstrates evolu-
isolated from one another (Biological Species Concept).
tion in action.
Box 1.1 Evolution in action: natural selection and the morphology of finch bills
I am sure that if you take the time to think about the charac- placed them at an advantage relative to others of their kind.
teristics of populations you will note the following: Through time, the differential survival of these individuals
• Not all individuals are the same. That is to say there is should result in a shift in the makeup of the population such
considerable variation within a species. that animals without the advantage become increasingly
• Offspring resemble their parents. This is because heritable rare (or perhaps disappear) and those possessing it become
variations are passed from parents to their offspring more common (Figure 1.8). He proposed a scenario under
through their genes. which beneficial traits were selected for and detrimental
• Reproductive over-production is common. Many more traits were selected against.
individuals are produced than can ever survive to mature We now understand that selection can be strongly direc-
and reproduce. tional in the way that I have just described, leading to the
increasing dominance of a trait or to its eradication, or it can act
These basic observations, a prodigious amount of patient in a disruptive way resulting in the evolution of two populations
work, and probably a touch of genius, allowed Charles that have very different but successful phenotypes. Selection
Darwin to construct his theory of evolution by natural selec- can also act in a stabilizing way to maintain the status quo.
tion. Long before the importance of genes was appreciated he
realized that some heritable property of certain individuals continued
Box 1.1 Continued
A B A
12.0
10.0
Seed abundance (g/m2)

8.0
6.0
C
4.0
2.0
Figure 1.8 The effect of directional (A), stabilizing (B), and 1400
disruptive (C) selection upon a hypothetical population. In each
case an arrow indicates the direction of the selection taking place,
Population size
the solid line describes the pre-selection population, and the 1000
broken line the post-selection population(s). From Scott,
G.W. (2005) Essential Animal Behavior. Blackwell Science,
Cambridge. 800
So can we see evolution by natural selection actually hap- 200

pening? Well thanks to the work of Peter Grant, Peter Boag,
and their colleagues we can. They have carried out a very C
detailed study of the population of the Medium Ground Finch 1.0 Males
Geospiza fortis on the tiny island of Daphne Major, one of the
0.8
Galapagos Islands. Since the mid 1970s these researchers
Principal component 1
have ringed and measured almost all of the G. fortis on the 0.6
All birds
island, they have recorded year on year survivorship and have 0.4
regularly trapped birds to take measurements from them.
0.2
These measurements include mass, wing length, tarsus
length, and bill length and depth. During the early years of 0.0
their study Daphne Major received regular seasonal rainfall –0.2 Females
(around 130 mm per year) and the finch populations did well.
–0.4
But in 1977 the island suffered an intense drought with just J S N J MM J S N J MM J S N J MM J S N J
24 mm of rain falling during the wet season. The impact upon 1975 1976 1977 1978
the birds was dramatic. They made no breeding attempts,
many birds delayed their moult, or failed to moult at all, and Figure 1.9 Under drought conditions in 1977/78 seed
significant levels of mortality were recorded (an 85 per cent production on the Galapagos islands fell (A). Without food the
finch population crashed (B) but some birds did survive. The
decline in the population in just one season).
principal component plotted in graph C is a mathematical measure
The drought did not just affect the birds on the island.
of the morphology of the finch population. As the drought
Many plants failed to set seed leading to a food shortage for progresses morphology clearly changes. In fact by 1978 only larger
the finches and most of the finch mortality could be attrib- birds with larger beaks remain in the population. Adapted from
uted either directly or indirectly to starvation. However some Boag, P.T. and Grant, P.R. (1981) Intense natural selection in a
birds did survive. They tended to be the bigger birds in the population of Darwin’s finches (Geospizinae) in the Galapagos.
population with bigger beaks (Figure 1.9). Science 214, 82–825. Reprinted with permission from AAAS.
In effect what has happened here is a burst of intense direc-

1976–77
tional selection. Initially the population exhibited size vari- WT
ation—smaller birds with smaller beaks and bigger birds with WG
TAR
bigger beaks. When the seed crop failed the available seeds BL
were used up quickly, and initially it seems that smaller seeds BD
were consumed preferentially. When seeds became scarce the BW
bigger birds changed their feeding behaviour to exploit the big-
ger seeds, but the smaller birds did not have the beak morph-
1984–85 WT
ology needed to crack these seeds and starved. Thus some of
WG
the observed variation in beak size was lost from the popula- TAR
tion which became dominated by bigger birds. But surely that BL
wasn’t the first drought to have occurred so why were there BD
small birds in the population? By continuing to study the finch BW
population of Daphne Major these dedicated researchers seem 0
to have the answer. Although natural selection favours large Smaller Direction of Selection Larger
size in response to drought, small size is favoured in response
to particularly wet years (when there are many more smaller Figure 1.10 Oscillating selection for finch size in response to
seeds than larger seeds) and during the first year of a bird’s life climate. During dryer periods (such as the mid 1970s) selection
(possibly for metabolic reasons). It would seem therefore that favours bigger birds. However, following wet periods (such as the
in effect, size in G. fortis is an example of oscillating selection, El Niño of 1982/83) smaller size is favoured. Biometrics listed
include: WT, weight; WG, wing length; TAR, tarsus length; BL, bill
repeated bursts of opposing directional selection in response to
length; BD, bill depth; and, BW, bill width. Adapted from Gibbs,
extremes of climate and associated fluctuations in food supply
L.H. and Grant, P.R. (1987) Oscillating selection on Darwin’s
(Figure 1.10). This work demonstrates two important things: it finches. Nature 327, 511–513.
shows us that we can see evolution in action and it shows us
that very long term studies are important.
1.5.2 Genes and evolution illa, a European songbird, and those associated with
morphological change in populations that are
Advances in genome level analysis are providing
becoming isolated as a result of differential migra-
exciting insights into the genes that are directly
tion, may provide further insights into the genetic
involved in the changes that take place during the
changes taking place during speciation events. This
evolutionary process. For example it has recently
is a topic that will be returned to in chapter 3.
been demonstrated that variations in the gene ALX1,
a gene known to be involved in the development of Flight path: evolution and bird migration, page 52.
the cranium and facial features of humans, is linked to
beak morphology in the Galapagos finches (although
Key references
an exact role has yet to be determined). An interact-
Abzhanov, A., Protas, M., Grant, B.R., et al. (2004)
ing effect of two other genes CaM and BMP4 and
Bmp4 and morphological variation of beaks in
their products has also been demonstrated to be Darwin’s Finches. Science 305, 1462–5.
important. Calmodulin (CaM) is a calcium-binding Lamichaney, S., Berglund, J., Almén, M.S., et al.
protein, and bone morphometric protein (BMP4) is (2015) Evolution of Darwin’s finches and their beaks
involved in bone and cartilage development. Variation revealed by genome sequencing. Nature 518, 371–5.
in the expression of these genes and the actions of
their protein products have been shown to be involved
1.5.3 Hybrids
in the differential growth of finch beaks (Figure 1.11).
These genes might therefore be important in the When the behavioural and genetic isolation between
speciation of these finches. Similarly the identifica- two species is incomplete it may be possible for
tion of the genes involved in the evolution of new hybridization to occur. In some cases these hybrids
migratory strategies in the Blackcap Sylvia atricap- might be sterile and so make no genetic contribution
(A) (B)
Depth
Upper
D beak
Mixed diet of
seeds and insects
R C Sharp-beaked finch
Low CaM; Low BMP4:
short beak low beak dept/width
V Wi
dth
Length C
/f rui
t l a r r ush
Crusing seeds
era g e in
ui s
flow
/fr tu
se g h
rs cac
us ed ar
t
ct s d/
g ca
we g
flo obin
bin
Pro
Pr
Low BMP4: Low-mod. BMP4: Mod. BMP4: Early/high BMP4:
low beak depth/width mod. beak depth/width mod. beak depth/width high beak depth/width
High CaM; High CaM; Low CaM; Low CaM;
elongated beak elongated beak short beak short beak
Cactus finch Large cactus finch Medium ground Large ground finch
finch
Figure 1.11 The morphology of a beak can vary along three axes: depth, width, and length (A) BMP- and CaM-dependent signalling regulates
growth along these axes resulting in a broad range of beak shapes. (B) The figure illustrates the way in which CaM/BMP variation has resulted in
the development of a range of beak morphologies. Adapted from Abzhanov, A., Kuo, W.P., Hartmann, C., et al. (2006) The calmodulin pathway and
evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–67.
to the next generation themselves, as such they between the two types (black with varying amounts
are an evolutionary dead end and should probably of grey).
be regarded as no more than a curiosity. But One fascinating example of transient hybridiza-
occasionally these hybrids are fertile and may tion is that of the Blue-winged and Golden-winged
reproduce either amongst themselves, or with one warblers Vermivora pinus and V. chrysoptera of
or other of their parent species. There are two North America. Ornithologists 200 years ago would
main outcomes possible as a result of this phe- have known the Blue-winged Warbler as a south-
nomenon. In some cases hybrid zones are formed ern species, and the Golden-winged warbler as a
when the stable ranges of two geographically species found in the north, but today the ranges of
adjacent species overlap. In other cases transient the two species overlap and that of the Blue-winged
hybridization, or genetic swamping, occurs as the Warbler is increasing whilst the Golden-winged
range of one species expands and previously iso- Warbler is becoming increasingly scarce. This shift in
lated species are brought into contact with one the range of the Blue-winged Warbler is a response
another. to an increase in their preferred secondary scrub
The classic example of the stable hybrid zone is habitat and is largely a result of human clearances
that of the black and grey Hooded Crow Corvus cor- of forested areas. Increased scrub cover also bene-
nix of northern and eastern Europe and the all black fited Golden-winged Warblers initially but where
Carrion Crow Corvus corone of southern Europe. the two species do overlap, Golden-wings eventu-
Along the narrow (2,100 km long but only 50–120 ally disappear. This disappearance takes about 50
km wide) contact zone between the populations of years so it isn’t simply the case that the Blue-wings
these two crows they freely interbreed and their see off the competition immediately. In fact the two
hybrids exhibit a plumage that is intermediate species do coexist initially but where they do, two
new ‘species’ also appear. These are hybrids. One, type hybrid. As this process of hybridization and
Brewster’s Warbler Vermivora chrysoptera x pinus, or backcrossing continues, Golden-winged Warblers
V. ‘leucobronchialis’, is a bird with the body plumage become increasingly rare. Eventually Blue-winged
of a Golden-winged Warbler and the face pattern of Warblers dominate the community, Golden-winged
a Blue-winged Warbler. The other is Lawrence’s Warblers have all but gone and hybrid types are
Warbler Vermivora pinus x chrysoptera or V. ‘lawren- rarely seen. However, as a result of the backcross-
cei’ which has a Golden-wing face pattern and ing of hybrids, the genes of the Golden-winged
Blue-wing body (Figure 1.12). Warblers may persist in the Blue-winged Warbler
The pattern of the hybrids’ appearance is predict- population with the result that an occasional aber-
able whenever the two parent species come into rant form may appear. This process of genetic take-
contact. Initially there are good numbers of Golden- over is referred to as ‘swamping’. Where a species is
wings in a population, but as numbers of immigrant introduced to habitat outside of its natural range
Blue-wings increase the numbers of Brewster’s type hybridization can become a major issue. Box 1.2
hybrids also increases. These hybrids are fertile and provides a real example of the threat of hybridiza-
backcross with both of the parent species resulting tion and of the difficult decisions and actions that
in intermediate types and in the rarer Lawrence’s environmental managers sometimes have to take.
Lawrence’s Warbler
(Vermivora pinus x chrysoptera,
or V. ‘lawrencei’ )
Brewster’s Warbler
(Vermivora chrysoptera x pinus,
or V. ‘leucobronchialis’ )
Blue-winged Warbler
(Vermivora pinus)
Golden-winged Warbler
(Vermivora chrysoptera)
Figure 1.12 The Blue-winged Warbler/Golden-winged Warbler hybrid types. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian
Structure and Function. Yale University Press, New Haven.
Box 1.2 Hybridization and duck conservation
The White-headed Duck Oxyura leucocephala is an eastern from museum specimens collected between 1900 and 1935,
European and central Asian species with a small isolated and was therefore able to establish their contemporary and
population in Spain. Populations are fragmented and under historical relatedness. Her results showed that the genetic
increasing pressure due to loss of habitat. This coupled with distinction between the two species is shrinking, presumably
the fact that populations are small and declining makes this as a result of continuing hybridization and genetic swamp-
species globally endangered (the Spanish population fell to ing. In the conclusion to her paper, Mank makes the some-
just 22 birds in 1977, and the main central Asian population what sombre statement that ‘The implications of our findings
fell from 100,000 in the 1930s to 10,000 in 2000). In for the conservation of the black duck are grim. Without
Europe the species faces another threat—genetic swamping preventing hybridization, conservation of pristine black duck
through hybridization with an alien invader! habitat will be ineffective in preserving the species’. So can
The alien in question is the Ruddy Duck Oxyura jamicensis hybridization be prevented in such a situation?
a close relative of the White-headed Duck but one that In the case of the White-headed Duck situation it may
would naturally be isolated from it by the Atlantic Ocean. In not be too late. There are various articles of legislation
their native range (North and South America) Ruddy Duck that are used by the international community to bring
are a successful species with an increasing population (of pressure upon nation states to take action for conservation.
more than half a million birds). They are an attractive duck In this case the relevant agreement is the Bonn Convention:
and have been popular additions to wildfowl collections for the Convention on the Conservation of Migratory Species.
many years. In Britain in the 1950s or early 1960s, Ruddy Within the convention there is an agreement, The African-
Duck from such collections were accidentally released and a Eurasian Migratory Water bird Agreement (AEWA) designed
feral population quickly established itself such that the to provide a legal framework for the conservation and
population grew from a handful of original birds to some management of 172 species of bird that are ecologically
6,000 individuals in 50 years. dependent upon wetland habitats. There are 116 signatory
If the British Ruddy Duck population had stayed in Britain nations to the AEWA in Europe, Africa, north-east Arctic
it may not have posed much of a problem, but as the popu- Canada, Greenland, Asia Minor, the Middle East, Kazakhstan,
lation grew increasing numbers of Ruddy Duck, presumed to Turkmenistan, and Uzbekistan. The list includes a number of
originate from Britain, were reported from a number of states which have White-headed Duck populations. Amongst
European countries. It was first recorded in Spain in the other conservation measures the AEWA encourages states
1980s and in 1991 the first hybrids between invading Ruddy to assess the impact that alien species might have in the
Duck and Spanish White-headed Duck were quickly reported. context of wetlands. Article III of the agreement requires sig-
The hybrids were fertile and second generation hybridization natories to prohibit the deliberate introduction of non-native
was observed. In this situation there is obviously the possi- water birds into the wild and to take all reasonable meas-
bility that the genome of the Ruddy Duck would swamp that ures to prevent their accidental release. This is very positive,
of the White-headed Duck in Spain and another valuable but these steps will not solve the Ruddy Duck problem—the
population would disappear. And if the Ruddy Duck were to birds are already out there. However, the AEWA also requires
spread across Europe and invade central Asia, the White- that signatories ‘ensure that when non-native species or
headed Duck might disappear as a distinct species. hybrids thereof have already been introduced into their ter-
Extinction by genetic swamping might seem far-fetched, ritory, those species or their hybrids do not pose a potential
but Judith Mank and others have demonstrated that in the hazard to the population listed’. So here is the legal require-
case of at least one other duck species this might be just ment for the control of the Ruddy Duck in Europe. If that was
what is happening. Mank and colleagues have compared insufficient in itself, the Council of Europe have published a
the genomes of American Black Duck Anas rubripes and specific action plan for the conservation of White-headed
European Mallard Anas platyrhynchos. Mallard were intro- Duck and the Bern Convention has put forward a strategy
duced to the Americas probably by early settlers and they did for the eradication of the Ruddy Duck throughout the
very well there. They are closely related to Black Duck and so Western-Palaearctic region. Ruddy Duck control measures
it is not very surprising that Mank and her colleagues found are now in place and birds have been culled throughout
genetic similarities between them. But as well as making a Europe. Eradication efforts in Spain and the UK have been
comparison of today’s populations she also took material particularly successful; Ruddy Duck and hybrids are now a
rarity in Spain and the UK population is almost extinct. At a References and further reading
European level the population of Ruddy Duck in 2013 had
Mank, J.E., Carlson, J.E., and Brittingham, M.C. (2004) A century of
been reduced to just 7 per cent of that in 2000. The picture hybridization: Decreasing genetic distance between American
does vary country by country, but the long term goal of black ducks and mallards. Conservation Genetics 5, 395–403.
the complete removal of Ruddy Duck from the European Rehfisch, M.M., Blair, M.J., McKay, H., and Musgrove, A.J. (2004) The
continent does seem to be achievable. We can be optimistic impact and status of introduced waterbirds in Africa, Asia Minor,
that this particular threat to the White-Headed Duck can be Europe and the Middle East. Acta Zoologica Sinica 52, 572–5.
overcome, but of course the future security of the species Robertson, P.A., Adriaens, T., Caizergues, A., et al. (2015) Towards
will depend upon other conservation actions to protect the European eradication of the North American ruddy duck.
specific habitats and populations. Biological Invasions 17, 9–12.
Summary
Anseriformes
Birds are specialist vertebrates thought to have Ahnhimidae Screamers
Anseranatidae Magpie goose
evolved from theropod dinosaurs. The evolutionary
Anatidae Ducks, geese, and swans
relationships of modern birds species are not yet
Podicipediformes
fully understood, but advances in phylogeny and Podicipedidae Grebes
new molecular techniques are bringing them within Phoenicopteriformes
our grasp. Like all organisms, birds continue to adapt Phoenicopteridae Flamingoes
and evolve in the face of environmental pressure. Phaethontiformes
Phaethontidae Tropicbirds
Eurypygiformes
Appendix 1
Euripygidae Sunbittern
Rhynochetidae Kagu
Familiar names of the members of the Orders
and Families of modern birds Mesitornithiformes
Mesitornithidae Mesites
The list follows Joseph del Hoyo and Nigel Columbiformes
Collar’s Illustrated Checklist of the Birds of the World Columbidae Pigeons and doves
volume 1 (2014, Non-Passerines) and volume 2 (2016, Pterocidiformes
Passerines), Lynx Edicions, Barcelona. As I high- Pteroclididae Sandgrouse
lighted earlier in this chapter, the phylogeny of Caprimulgiformes
birds is a fast-moving field and so this list should Steatornithidae Oilbirds
not be considered to be a definitive. Podargidae Frogmouths
Nyctibiidae Potoos
Caprimulgidae Nightjars or goatsuckers
Struthioniformes Aegothelidae Owlet-nightjars
Struthionidae Ostrich Apodidae Swifts
Rheidae Rheas Trochilidae Hummingbirds
Tinamidae Tinamous
Opisthocomiformes
Casuariidae Cassowaries and emu
Opisthocomidae Hoatzin
Apterygidae Kiwis
Cuculiformes
Galliformes
Cuculidae Cuckoos, roadrunners, and anis
Megapodiidae Megapodes
Cracidae Curassows, guans, and chachalas Gruiformes
Numididae Guineafowl Hellornithidae Finfoots
Odontophoridae New world quail Rallidae Rails, gallinules, and coots
Phasianidae Pheasants, partridges, grouse turkeys, old Psophiidae Trumpeters
world quail Aramidae Limpkin
Gruidae Cranes Accipitriformes

Otidiformes Sagittariidae Secretary-bird
Otididae Bustards Pandionidae Osprey
Musophagiformes Accipitridae Hawks, eagles, kites, old world vultures
Musophagidae Turacos Coliiformes
Gaviiformes Coliidae Mousebirds
Gaviidae Divers or loons Leptosomiformes
Sphenisciformes Leptosomatidae Cuckoo-roller
Spheniscidae Penguins Trogoniformes
Procellariiformes Trogonidae Trogons
Oceanitidae Southern storm-petrels Bucerotiformes
Hydrobatidae Northern storm-petrels Bucerotidae Hornbills
Diomedidae Albatrosses Upupidae Hoopoes
Procelariidae Shearwaters and petrels Phoeniculidae Woodhoopoes
Ciconiiformes Coraciiformes
Ciconiidae Storks Meropidae Bee-eaters
Coraciidae Rollers
Pelecaniformes
Brachypteraciidae Ground-rollers
Threskiornithidae Ibises and spoonbills
Todidae Todies
Ardeidae Herons, egrets, and bitterns
Momotidae Motmots
Scopidae Hamerkop
Alcedinidae Kingfishers
Balaenicipitidae Shoebill
Pelicanidae Pelicans Piciformes
Galbulidae Jacamars
Suliformes
Bucconidae Puffbirds
Fregatidae Frigatebirds
Ramphastidae Toucans
Sulidae Boobies and gannets
Capitonidae New world barbets
Phalacrocoracidae Cormorants
Semnornithidae Prong-billed barbets
Anhingidae Anhingas
Megalaimidae Asian barbets
Charadriiformes Lybiidae African barbets
Burhinidae Thick-knees Indicatoridae Honeyguides
Chionididae Sheathbill Picidae Woodpeckers and allies
Pluvianellidae Magellanic plovers
Cariamiformes
Pluvianidae Egyptian plovers Cariamidae Seriemas
Haematopodidae Oystercatchers
Ibidorhynchidae Ibisbill Falconiformes
Recurvirostridae Avocets and stilts Falconidae Falcons and caracaras
Charadriidae Plovers Psittaciformes
Pedionomidae Plains-wanderer Strigopidae New Zealand parrots
Thinocoridae Seedsnipe Cacatuidae Cockatoos
Rostratulidae Painted-snipe Psittacidae Parrots
Jacanidae Jacanas
Passeriformes
Scolopacidae Sandpipers
Acanthisittidae New Zealand wrens
Turnicidae Button-quails
Pittidae Pittas
Dromadidae Crab-plover Philepittidae Asites
Glareolidae Coursers and pratincoles Eurylamidae Typical broadbills
Laridae Gulls, terns, and skimmers Sapayoidae Sapayoa
Stercorariidae Skuas Calyptomenidae African and green broadbills
Alcidae Auks Thamnophilidae Typical ant birds
Strigiformes Conopophagidae Gnateaters
Tytonidae Barn owls Melanopareiidae Crescentchests
Strigidae Typical owls Grallariidae Antpittas
Rhynocryptidae Tapaculos
Cathartiformes
Formicariidae Ground-antbirds
Cathartidae New world vultures
Furnariidae Ovenbirds Paridae Tits and chickadees

Pipridae Manakins Remizidae Penduline-tits
Cotingidae Cotingas Alaudidae Larks
Tityridae Tityras and allies Panuridae Bearded reedling
Tyrannidae Tyrant-flycatchers Nicatoridae Nicators
Menuridae Lyrebirds Macrosphenidae Crombecs and allies
Atrichornithidae Scrub-birds Cisticolidae Cisticolas and allies
Ptilonorhynchidae Bowerbirds Acrocephalidae Reed-warblers
Climacteridae Australasian treecreepers Pnoepygidae Cupwings
Maluridae Fairywrens Locustellidae Grasshopper-warblers and Grassbirds
Dasyornithidae Bristlebirds Donacobiidae Donacobius
Meliphagidae Honeyeaters Bernieridae Tetrakas
Pardalotidae Pardalotes Hirundinidae Swallows and martins
Acanthizidae Thornbills Pycnonotidae Bulbuls
Orthonychidae Logrunners Phylloscopidae Leaf-warblers
Pomatostomidae Australian babblers Scotocercidae Bush-warblers
Mohouidae Mohouas Aegithalidae Long-tailed tits
Eulacestomidae Ploughbill Sylviidae Old world warblers and parrotbills
Neosittidae Sittellas Zosteropidae White-eyes
Oriolidae Old world orioles Timaliidae Scimitar-babblers and allies
Paramythiidae Painted berrypeckers Pellormeidae Ground babblers
Oreoicidae Australo-Papuan bellbirds Leiotrichidae Laughing thrushes and allies
Cinclosomatidae Quail-thrushes and jewel-babblers Certhiidae Treecreepers
Falcunculidae Shrike-tits Sittidae Nuthatches
Pachycephalidae Whistlers Polioptilidae Gnatcatchers
Psophodidae Whipbirds and wedgebills
Troglodytidae Wrens
Vireonidae Vireos
Cinclidae Dippers
Campephagidae Cuckoo-shrikes
Buphagidae Oxpeckers
Rhagologidae Berryhunter
Sturnidae Starlings
Artamidae Woodswallows and butcherbirds
Mimidae Mockingbirds and thrashers
Machaerirhynchidae Boatbills
Vangidae Vangas and allies Turdidae Thrushes
Platysteiridae Batises and wattle-eyes Muscicapidae Old world flycatchers
Aegithinidae Ioras Regulidae Kinglets and firecrests
Pityriasidae Bristlehead Dulidae Palmchat
Malaconotidae Bush-shrikes Hypocoliidae Hypocolius
Rhipiduridae Fantails Hylocitreidae Hylocitreas
Dicruridae Drongos Bombycillidae Waxwings
Ifritidae Ifrit Ptiliogonidae Silky-flycatchers
Monarchidae Monarch-flycatchers Elachuridae Elachura
Platylophidae Crested jay Promeropidae Sugarbirds
Laniidae Shrikes Modulatricidae Spot-throat and allies
Corvidae Crows and jays Irenidae Fairy-bluebirds
Melampittidae Melampittas Chloropseidae Leafbirds
Corcoracidae Australian mudnesters Dicaeidae Flowerpeckers
Paradisaeidae Birds-of-paradise Nectariniidae Sunbirds
Callaeidae New Zealand wattlebirds Prunellidae Accentors
Notiomystidae Stitchbird Peucedramidae Olive warbler
Melanocharitidae Berrypeckers and longbills Urocynchramidae Przevalski’s Rosefinch
Cnemophilidae Satinbirds Ploceidae Weavers
Picathartidae Picathartes Estrildidae Waxbills
Eupetidae Rail-babbler Viduidae Whydahs and indigobirds
Chaetopidae Rockjumpers Passeridae Old world sparrows
Petroicidae Australasian robins Motacillidae Wagtails and pipits
Hyliotidae Hyliotas
Fringillidae Finches
Stenostiridae Fairy flycatcher and allies
Calcariidae Longspurs
Rhodinocichlidae Thrush-tanager Phaenicophilidae Hispaniolan tanagers

Emberizidae Old world buntings Spindalidae Spindalises
Passerellidae New world sparrows Nesospingidae Puerto Rican tanagers
Zeledoniidae Wren thrush Calyptophilidae Chat-tanagers
Teretistridae Cuban warblers Mitrospingidae Mitrospingid tanagers
Icteridae New world blackbirds Cardinalidae Cardinals
Parulidae New world warblers Thraupidae Tanagers
C H A PT ER 2
Feathers and flight
‘Birds are pilot and aircraft in one.’

John Videler (2006)
‘No bird soars too high if he soars on his own wings.’

William Blake, (1793)
Although not unique to birds, the power of flight Tyrannosaurs rex. The significance of this will be
and feathers are probably their distinguishing fea- returned to towards the end of this chapter. There is
ture in the eyes of most people. In this chapter I no doubt that feather types have evolved to make
want to take some time to consider the feathers that flying more efficient, but their original function
make flight possible, their growth, their mainten- must have been very different. Among modern
ance, and their replacement through moult. I will birds, feathers are essential in flight, for waterproof-
also describe the anatomical adaptations of birds to ing, and insulation. They often have a role in com-
flight, and the process of flight itself. munication, for courtship or competition, and in
predator avoidance through camouflage. In some
cases they even have a tactile function, an example
Chapter overview
being the feather-derived bristles around the
mouths of some insectivores and some nocturnal
2.1 Feathers
birds.
2.2 Feather tracts
2.3 Feather colour Flight path: evolution of birds from dinosaurs,
2.4 Feather damage page 6.
2.5 Feather maintenance
2.6 Moult
2.1.1 Feather types
2.7 Flight
2.8 The evolution of flight and flightlessness I am sure that you have in your mind a picture of
the typical feather (perhaps something like the quill
of the medieval scribe?). But if you took some time
2.1 Feathers
to think about all of the feather types that you have
Feathers were once thought to be one of, if not the, ever experienced, their variety might start to bewil-
defining character of birds. But recent discoveries of der you; ranging as it does from the simple bristles
fossil dinosaur feathers, indistinguishable from around the beak of some flycatchers, to the magnifi-
those of modern birds, prove that this is not the cently ornate tail plumes of male Indian Peafowl
case. It has also been a commonly held belief that Pavo cristatus, to the fluffy down that fills your
feathers evolved in association with the evolution jacket and keeps you warm when birding in cold
of flight, but this too can be discounted. Feathers weather. Thankfully for the purpose of this book we
of the modern type have been found on fossils of can reduce this bewildering array to essentially two
non-flying dinosaurs, including the ancestors of basic types: contour feathers and downs.
DOI: 10.1093/oso/9780198804741.003.0002
2.1.2 Contour feathers to use their tails as a support when clinging to the
trunk of a tree.
The contour feathers are all of those feathers that
One particular class of contour feather, the filo-
form the outline of the bird. They therefore include
plumes, do have a somewhat atypical structure.
the tail feathers (rectrices), the feathers of the wing
They have a rachis that is almost naked, having
(remiges), those covering the body of the bird,
only a small tuft of plumulaceous barbs at its tip.
and the highly modified bristles that are often
These feathers protrude through the plumage and
found around the head of the bird and may bear a
are thought to be important in providing the bird
superficial resemblance to mammalian hairs. The
with sensory information (via motion sensing cells
arrangement and extent of these various feather
at their base) concerning wind movements and
types is illustrated in Figure 2.1, and a range of
feather alignment.
typical feather types and structures are illustrated
in Figure 2.2.
The typical contour feather has at its base a bare
2.1.3 Down feathers and semiplumes
quill, or calamus, this is the part of the feather that
sits inside the feather follicle and is attached to the Down feathers and semiplumes (which can be
body of the bird. The calamus extends into the often classed as an intermediate between a contour
long and tapering central shaft of the feather that is feather and a down feather) do have a calamus,
more properly termed the rachis. In the case of most rachis, and vane anatomy similar to that of the con-
contour feathers (but not the bristles) the rachis tour feathers but their rachis is usually short and
supports two vanes, the blades of the feather. The the vanes are entirely plumulaceous. As a result
vanes are actually composed of two opposite rows they often resemble more of a tuft than a typical
of barbs, projections of the rachis which in their feather. These are the feathers that cover nestlings,
turn support two parallel rows of smaller projec- providing them with excellent insulation, and in
tions or barbules. some situations with a degree of protection against
The barbules themselves are sculptured to allow cannibalism. For example in some colonial situations
them to lock together like Velcro, giving the vane its newly hatched (wet) gull chicks are often swal-
sheet-like quality, Specifically those barbules which lowed whole by neighbouring adults—but when
project from the barb and point forwards towards they have dried out, their stiff feathers make them
the tip of the feather (distal barbules) have a comb difficult to swallow and cannibalism rates decline.
like arrangement of hooked barbicels which lock In adult birds, down feathers and semiplumes are
into ridges on the adjacent backwards pointing usually found beneath the contour feathers where
barbules (proximal barbules). Most feathers have a they continue to perform an insulatory role and
basal area of the vane (i.e. the area closest to the in species of waterbirds they contribute towards
calamus) the barbs of which lack barbicels, result- buoyancy. Interestingly, species that experience
ing in a more open structure that can only really be environmental temperature fluctuations in their
described as ‘fluffy’. A vane or vane area with this annual cycle, such as the Redpoll Carduelis flammea
open structure is properly referred to as being of the northern forests, often have a greater number
plumulaceous, and the alternative locked sheet of down feathers immediately after completing
structure is referred to as being a pennaceous vane. their moult in the autumn to provide extra insula-
The pennaceous vane structure is what gives feathers tion during the colder months. Presumably these
their strength. Thus the outer plumage acts as a feathers are lost as a result of wear and tear, or are
light but relatively impenetrable armour against shed to reduce insulation as the warmer spring and
wind, water, and abrasion; and, the overlapping summer proceed.
vanes of the open wing form the solid aerofoil One particular class of down feather, the powder-
required for flight. The strength of the rachis of the down feathers, grow continuously but constantly
tail feathers of tree climbing species like the wood- break at their tip resulting in the production of the
peckers and treecreepers is such that they are able powder of feather wax particles that give them their
F E AT H E R S A N D F L I G H T 23
Crest Crown
General Topography
Blue Jay (Cyanocitta cristata) Lore
Forehead
Supercilium Upper Mandible
Primaries and Secondaries Auriculars

are collectively called ‘Remiges’ Lower Mandible
Back Nape
Secondaries Chin
Malar
Primaries
Scapulars Throat or Jugulum
Upper Tail
Coverts
Breast
Upper Wing Coverts
Side
Rectrices of the Tail Undertail coverts Flank
Alula Belly
or Crissum
Crural feathers
Crest Tarsus
Crown
Hallux
Forehead Scapulars (hind toe)
Lore
Nape
Rictal Bristles
Back Tertials
Gape Upper Tail
Rump
Throat Scapulars Coverts
Marginal
Coverts 11
10
Middle Secondary 9
Coverts Gr. Secondary Coverts 8
Alula 7
6
5
Greater 4
3
Primary 1 2 Secondaries
Coverts 1
Note how the numbering of the
2 remiges proceeds from this point. Rectrices
3
Primaries
4
5
6
10 7
8
9
Figure 2.1 The general topography of a bird. The species illustrated is the Blue Jay Cyanocitta cristata. From Proctor N.S. and Lynch, P.J. (1993)
Manual of Ornithology: Avian Structure and Function. Yale University Press, New Haven.
Pheasant contour
feather
Anterior vane
Aftershaft
Rachis (shaft)
Calamus (quill)
Rachis
Distal
Cortex barbule
Diagrammatic
Barb
view of Vane
Structure Proximal barbule
Posterior vane Longitudinal

groove Ventral ridge
Barbs
Vaned flight
Superior umbilicus
feather (remex) Drawings are not to scale
Calamus (quill)
Inferior umbilicus
Down feather
Calamus (quill)
Figure 2.2 Feather structure. Adapted from Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale
University Press, New Haven.
name. It is presumed that this powder has a role in 2.2 Feather tracts
the maintenance of feather waterproofing.
Based upon observations of a living bird about its
Flight path: Poorer quality juvenile feathers can be a daily business it could be assumed that the body of
cost worth paying if predation risk is high, page 92. a bird is evenly covered with feathers. After all with
(A) (B)
Inter-ramal tract
Capital tracts
Malar tract
Spinal tract, cervical region Submalar tract

Scapular apterium
Ventral cervical tract
Humeral tract
7
5 31
Primaries 1
3
Eutaxic wing 5
7
Secondaries
9
Spina tract, dorsal
Ventral sternal tract
Upper tail coverts
Ventral abdominal tract
Spinal tract, pelvic
Anal circlet
Uropygial gland
Upper tail coverts Tail 6
Rectrices of the tail 3
1
Undertail coverts
Figure 2.3 The dorsal (A) and ventral (B) feather tracts of a typical passerine bird. Adapted from Proctor, N.S. and Lynch, P.J. (1993) Manual of
Ornithology. Yale University Press, New Haven.
the exception of the typically bare legs, and the

areas adjacent to the beak and eyes, no skin is usu-
ally visible. But it would be wrong to assume that
this superficial impression of feather-covered skin
equates to an even distribution of feathers across
the skin in the same way that hair follicles are
evenly distributed across a human scalp for example.
A similarly even distribution of feather follicles
does occur very rarely (examples include the pen-
guins (Spheniscidae) and the Ostrich Struthio came-
lus) but in almost all birds, feather follicles are
restricted to well defined areas of skin—the feather
tracts or pterylae which are separated from one
another by areas of naked skin, the apteria. Figure 2.4 This adult European Greenfinch Carduelis chloris is
Figure 2.3 illustrates the feather tracts of a general- moulting. Lines of new contour feathers just emerging from their
sheaths clearly show the position of the ventral sternal feather tract
ized passerine, while those of a Greenfinch Cardeulis
(© Peter Dunn).
chloris can be seen in Figure 2.4.
Along the feather tracts individual feathers grow
from specialized groups of skin cells arranged as a feather bud) and an upwards growth of the tubular
feather follicle. These follicles begin as placodes, proto-feather as cells at its base proliferate. The der-
thickenings of the epidermis and dermis (skin) mal pulp in the centre of the feather bud provides
which develop to take on a typical ‘goose-bump’ the nutrients required for feather growth and the
morphology by a simultaneous evagination of the pigments that will give it its characteristic colour.
skin around the feather germ (sometimes called a As the feather germ lengthens, layers of cells
forming the tubular feather differentiate, the outer Other colours—browns, blacks, yellows, and
cells becoming the protective sheath of the growing reds for example, are the result of pigments that
feather, while the inner cells establish the barb are laid down within the growing feather. Black,
ridges that will form the barbs of the developed grey, and browns are the result of melanins (spe-
feather. Finally the feather bursts from the sheath cifically eumelanin and pheomelanin); pigments
and unfurls into its final form. The particular prop- that are synthesized by birds as a result of the oxi-
erties of each feather type, the stiffness of a primary dation of the amino acid tyrosine. Darker feathers
flight feather or the softness of a down feather for have more melanin than lighter ones. Most white
example, depend upon the different combinations birds have black, melanin-rich, wing tips, this is
of proteins they are made from (predominantly because melanin pigments are associated with
corneous beta-proteins together with keratins and the deposition of extra keratin which strengthens
histadine-rich proteins). Genomic analysis has the feathers. Without this additional strength the
revealed that in the domestic chick more than 130 wing tips would quickly abrade and flight effi-
genes are involved in the production of these proteins ciency would be compromised. Reds, red-browns,
and that the properties of different feathers are a result and the green colour of Turacous (Musophagidae)
of the activity of different genes. For example, whilst are derived from porphyrins (specifically turacovera-
the beta-proteins of the softer contour feathers are the din (green), uroporphyrin (red), and coproporphyrin
product of 13 FCbetaPs genes found on chromosome III (red-brown)). Porphyrins too are synthesized by
25, those of the stiffer flight feathers are the product of birds. In this case they are a product of the break-
a different set of 13 FCbetaPs genes found on chromo- down of haemoglobin by the liver. Birds are unable
some 2. These genes are active during initial feather to synthesize the pigments that result in yellows
growth and then reactivated periodically to support and bright reds (principally leutins and carotenoids),
the growth of new feathers during the moult. instead they obtain them through their diet directly
from the environment. As we will see in chapter 5
Key references yellows and reds often feature significantly in the
Alibardi, L. (2017) Review: cornification, morphogenesis courtship plumage of birds, perhaps because they
and evolution of feathers. Protoplasma 254, 1259–81. are a signal of male quality.
Prum, R.O. (1999) Development and evolutionary
origin of feathers. Journal of Experimental Zoology Flight path: Feather colour, male quality, and sexual
285, 291–306. selection, page 101.
2.4 Feather damage

2.3 Feather colour Although the growing feather does have a blood
Birds have a reputation as being amongst the most supply, and the feather itself can be moved by
colourful of vertebrates and much of this reputation muscles that attach to it below the skin, feathers
they owe to the incredible range of colours of their are inert/dead structures and they cannot be
feathers. Some colours—white, greens, and blues repaired. Feathers may be damaged when birds
for example, are the result of the way that structural fight or during encounters with predators or prey,
features of the feather reflect light. For example the and they abrade when they rub against one
interaction of reflective pigment granules, complex another or against objects in the environment (try
layering patterns in the keratin of the feather, and pushing your hand through a briar or bramble
the angle of the observer relative to the bird are patch and imagine the abrasion that birds nesting
responsible for the iridescence of hummingbirds in there must suffer!). Figure 2.5 shows the
(Trochillidae) and starlings (Sturnidae). Recent fos- extreme wear on the tail feathers of Whitethroat
sil discoveries have demonstrated that this type of Sylvia communis, this bird was captured before it
structural iridescence was a feature of the feathers underwent post-breeding moult and after a sum-
of the four-winged Microraptor gui and other dino- mer of skulking in thorny vegetation. Feathers are
saur ancestors of the modern birds. degraded as a result of photochemical reactions
when the ultraviolet component of sunlight alters

the physical structure of the keratin that they are
composed of. They are also under attack by an
array of bacteria, fungi, and ectoparasites such as
mites and lice. There are however some situations
when feather wear can be an advantage, as shown
in Box 2.1.
In the face of such relentless pressure why aren’t
all birds as bald as the proverbial coot! Well of
course feathers are absolutely essential to bird sur-
vival and so birds engage in regular feather main-
tenance activities to minimize the impact of damage
and wear when it occurs. They also periodically
Figure 2.5 The tail feathers of the Whitethroat Sylvia communis shed and replace all of their feathers in a process
exhibit extreme wear. (© Peter Dunn). known as moult.
Box 2.1 Taking advantage of feather wear
Although feather wear can generally be regarded as a bad experienced (and did some background reading rather than
thing—necessitating as it does the periodic replacement of guessing) I discovered that I was wrong. Adult birds of this spe-
feathers—there are birds of a range of species that turn cies complete a full post-breeding moult in the UK before they
wear to their advantage. migrate and then return the following spring with the same
When I catch male Common Redstarts Phoenicurus phoeni- feathers intact. So how do they become brighter? Well if you
curus for ringing (banding) in the UK during their southwards were able to examine closely the facial feathers of the autumn
autumn migration I am always struck by how dull they are. An bird you would see that they are indeed glossy black—but not
adult male Redstart during the breeding season is a joy to at their tips—here they each have a pale fringe (hence the
behold, it is an explosion of colour with its red tail, bright orange/ beige frosting). These fringes are less durable than the black
red breast, glossy black face and bib, and powder blue crown parts of the feather ‘behind’ them—possibly because they con-
and nape. But in autumn they look, well—dull. Muted versions tain less of the pigment melanin—and they wear away over the
of their breeding colours are apparent but overlying them they course of the winter. Because this wear takes place over all of
have a rather dull beige tinge that is often described by birders as the body they do in effect become brighter as the breeding sea-
a frosting. Figure 2.6 shows this difference in plumage. son arrives. So come spring they are in prime condition and,
I confess that I did initially presume that this was a non- without the need to undergo a time- and energy-consuming
breeding plumage that would be lost during a winter moult in moult, they are able to get on with the serious business of
their sub-Saharan African winter grounds. But as I became more impressing their mates (and bird watchers like me).
(A) (B)
Figure 2.6 In spring male Common Redstarts Phoenicurus phoenicurus have a glossy black throat, grey crown, and rusty red breast (A;
© Ian Grier). This bird was trapped and ringed in Cyprus in spring when presumably it was migrating northwards into Europe. On the other
hand the male bird shown in B (© Peter Dunn) was trapped in the UK during its southwards autumn migration and exhibits the dull fringing
typical of freshly moulted birds.
2.5 Feather maintenance ectoparasites, those such as the mites and lice
that feed directly on feathers, and also the ticks,
The keratin that feathers are made from is one of fleas, and Hippoboscid flies that feed on the birds
the strongest and most durable of biological sub- themselves.
stances. This is an advantage on one hand, having Similarly, bathing in sand or water, scratching
resilient feathers is a good thing, but from another (with bill or feet), and having a good shake out
perspective it can be a problem. When a feather is can also be useful in feather realignment but are
wrongly aligned, as can happen very easily, it will probably most important in the physical removal
rub against those around it and might cause increased of parasites and foreign bodies. Sunning (when
abrasion. So, one of the most basic of feather main- birds prostrate themselves with their feathers out-
tenance activities undertaken by birds is regular stretched or stand with their wings open in the full
preening. During preening birds smooth their sun) probably also aids in ectoparasite reduction.
feathers back into place by passing them through However, the most intriguing of feather maintenance
their beak. This has the double effect of restoring behaviours are without doubt anting and smoking.
them to their correct position and ‘zipping’ back In the case of the latter I have often watched with
together any barbicles and barbules that have amusement as Jackdaws Corvus monedula stand
become detached (a process rather like smoothing on the lip of a chimney pot and extend first one
together the parts of a Velcro fastening). The effect wing and then another into the rising smoke from
of preening is often enhanced because prior to the fire below. Presumably the smoke rids the bird
feather smoothing, birds rub onto their beaks the of parasites and perhaps an unpalatable smoky
secretions of their preen gland. The preen gland residue coats the feathers deterring the activity of
(or uropygial gland) is situated low on the back feather-eating mites? During anting, birds position
just above the base of the tail (see Figure 2.3A). themselves on top of a swarm and allow the insects
It produces an oily secretion that is used by to crawl through their feathers and over their bod-
birds to maintain the physical quality of their ies, presumably the ants pick off parasites. In some
feathers and to regulate bacterial and fungal com- cases birds actively select particular ants and rub
munities that grow on them. In the case of aquatic them onto their feathers, it is assumed that in this
birds the preen gland is particularly large and its case the bird is taking advantage of chemicals pro-
secretions are important in feather waterproof- duced by the ants that perhaps serve as a parasite
ing. Figure 2.7 shows a roosting bird busily preen- deterrent.
ing to dislodge and remove dirt particles and
2.6 Moult
Moult occurs when a new feather begins to develop
in the follicle and simply pushes out the old feather
above it. The production of new feathers is expen-
sive in terms of raw materials and the consequences
of a lack of resources during feather growth can
often be seen in the feathers of passerines that have
recently fledged and are still in juvenile plumage.
Close examination of the retrices or tail feathers of
such birds often reveals fault-bars, easily visible
lines running across the vanes of all of the feathers
and aligned across the width of the tail (see for
example Figure 2.8). These are structural weak-
Figure 2.7 Roosting birds such as this Dunlin Calidris alpina spend
nesses caused as a result of a period of resource
a considerable proportion of their time carefully preening their shortage (perhaps that section of the feather grew
feathers (© Ian Grier). on a particularly wet day when the parent bird was
Figure 2.9 An example of wing moult in the European Starling

Sturnus vulgaris. This bird was trapped for ringing in the late summer
and is moulting out of its brown juvenile plumage into its glossy adult
Figure 2.8 A series of faults are evident in the tail feathers of this plumage. Using the numbering conventions explained in Figure 2.1,
Chaffinch Fringilla coelebs. Because they line up across the tail we can the wing feathers are dropped and replaced sequentially starting with
deduce that this is a juvenile bird, and all of these feathers were primary 1 (in the centre of the wing). In this case three new (darker)
grown at the same rate in the nest. However the faults are absent feathers are visible (primaries 1, 2, and 3, one feather (primary 4) is
from the three outer feathers on the right side of the tail, suggesting missing and primaries 5–9 (older brown feathers) can clearly be seen.
that they have been replaced (© Peter Dunn). The small, 10th primary is not visible. Secondary moult has not yet
started (© Graham Scott).
unable to provide sufficient food to the growing
nestling). The width of the bars is a measure of the
production and to maintain aerodynamic efficiency
duration of the resource shortage and they line up
(see Figure 2.9). So moult may also be costly because
because as a nestling all of the feathers of the tail
it prevents or impairs normal feather function. A
are grown at the same time. Possibly, because they
bird with gaps in its tail and wing is less able to fly
do grow their plumage in such a short time period,
efficiently and so may be less able to forage or to
the feathers of most juvenile birds are of poorer
avoid predators. This is possibly why moulting
quality than those of adults and so a post-juvenile
birds tend to skulk and be less active, or undergo
moult involving all or most of the plumage is com-
migrations to specific moulting grounds.
mon. This often involves a change in plumage col-
ouration as birds progress from a more cryptic Flight path: Flocking is an effective anti predator
appearance and/or one that may protect them strategy, page 137.
from the competitive attentions of their elders to
the patterns typical of adults of their species. Young Extreme examples of this are the annual moults of
European Robins Erithacus rubecula do not gain the some species of ducks, swans, and geese many of
red breast feathers characteristic of their species which form large, flightless flocks on or close to
until they have dispersed away from their natal ter- their breeding grounds. These birds are flightless
ritory. This is an advantage because adult Robins for a period of some weeks between the end of the
are strongly motivated to attack anything that is breeding season and the onset of migration (often
red in colour. adults resume flight to coincide with the onset of
Fault bars are also occasionally evident in the tail flight in their attendant young). By flocking it is
feathers of birds which have undergone a moult likely that these birds reduce the predation risks
into their adult plumage, but these bars will usually that they face. In the case of some species of sea
only be seen in one or two feathers and they will not duck such as Steller’s Eider Polysticta stelleri,
line up across the width of the tail. This is because post-breeding flocks are established in estuaries
an adult bird moults its tail feathers in sequence, and on the open sea often with hundreds of thou-
often (but not in all cases) from the centre outwards sands of flightless birds congregating to complete
in pairs. Adult birds almost certainly moult this their moult. Some species have developed behav-
way to both spread the raw material costs of feather iour to minimize the impact of moult, see Box 2.2.
Box 2.2 Minimizing the impact of moult
The wing of a bird acts as an aerofoil providing both lift and 17.2
thrust during flight. To maintain flight efficiency it has been control
Standardized body mass (g)

assumed that birds optimize their body mass to wing area 17 control
ratio. A great number of experiments have been carried out to 16.8
demonstrate that birds can/cannot fly following wing mani-
pulations such as the removal of feathers, feather cutting, 16.6
and even surgical separation of the propatagium (the flap of
skin along the bones of the wing to which the feathers are 16.4
attached). The results of such mutilations have shown for taped
16.2
example that pigeons are able to fly in a wind-free laboratory taped
environment with as little as 50 per cent of their wing area 16
intact. But such studies do not tell us much about the real Capture Recapture Recapture
20–21 August 3–4 September 10–12 September
impact of natural wing area reductions, for example during
moult. It has been suggested that moulting birds would suf- Figure 2.10 Birds with experimentally reduced flight efficiency
fer reduced flight performance to the extent that they might compensate by adjusting their body mass. From Senar, J.C.,
be less able to forage or to escape from predators. We might Domènch, J., and Uribe, F. (2001) Great Tits (Parus major) reduce
therefore have expected natural selection to have resulted in body mass in response to wing area reduction: a field experiment.
a solution to this problem. Joan Senar and colleagues have Behavioural Ecology 13(6), 725–7. Reprinted by permission of
carried out a remarkably elegant experiment to show just Oxford University Press.
how Great Tits Parus major maintain flight efficiency during a
simulated moult, and their experiment was all the more
remarkable because they carried it out in the field and the birds were captured for a third time. They were re-
because they did not mutilate their birds in any way. weighed, all tapes were removed and they were all released.
The researchers captured a sample of wild Great Tits and Following the usual strategy for this species, as autumn
divided them into two groups, A and B. Group A birds had approaches group B birds increased in mass following
primary feathers 5, 6, and 7 (those in the middle of the outer their initial capture, but the taped (group A) birds did not
wing) taped together to simulate an 8 per cent reduction in (Figure 2.10). After the second capture, group A birds (no
wing area (a reduction typical during the moult of this spe- longer taped) did increase their mass to that typical of
cies). Group B birds were not taped. All of the birds were autumn birds, but look at what happened to the newly taped
weighed and then released. Two weeks later the birds were group B birds. Their mass has fallen. These results are evidence
recaptured and re-weighed. Group A birds then had their that birds strategically alter their body mass in response to a
tapes removed whilst group B birds were taped (primaries 5, change in wing area to maintain an optimum wing area to
6, and 7 again), prior to release. After a further two weeks mass ratio.
again; and montane/high latitude birds such as the

2.6.1 Moult strategies
Ptarmigan Lagopus mutus moult into and out of a
As has already been mentioned moult is essential to whiter winter plumage for camouflage.
birds, enabling as it does the replacement of worn The particular moult strategy employed by any
and damaged plumage. In some species however it given species is likely to have evolved as an adap-
serves a further purpose in that it allows birds to tive response to a range of conflicting pressures such
change their appearance to suit their needs at a as the availability of resources, the time available
given stage of their life cycle. For example male before a necessary migration, the need to allocate
birds of a number of species (as diverse as ducks and available resources to reproduction etc. Some spe-
buntings) annually moult all or some of their feathers cies, particularly those at high latitudes, take advan-
to enable them to shift from a non-breeding/eclipse tage of a superabundance of resources and increased
plumage to a breeding/nuptial plumage and back day length to breed and moult simultaneously.
For example, Ivory Gulls Pagophila eburna begin to be completed more quickly than those of larger
their moult prior to egg laying and Alaskan popula- birds and in the cases of some large bird species,
tions of Glaucous Gulls Larus hyperboreus moult one moult cycle may overlap with the next and so
whilst incubating. In the tropics lengthy periods of moult will overlap with the whole of the annual
parental care, perhaps a result of high competition cycle (although it may only be active moult during
for patchily distributed resources, often result in the some periods of the year, being suspended at others).
onset of adult moult overlapping the end of the Some species time their moult around migration,
breeding season. The moults of smaller birds tend see Box 2.3.
Box 2.3 Moult strategies of the old world warblers
Many of the species of old world warbler migrate annually is a typical shorter distance migrant and one which under-
between northern European breeding grounds and African goes a moult before it begins the autumn migration. The
wintering areas. The timing of the moult and particular closely related Greenish Warbler Phylloscopus trochiloides
sequence and extent of feather replacement varies from spe- however begins its moult before migrating, but completes it
cies to species, but all of them have to fit the need to moult once it has reached its winter territory. Notice here that I
around the need to migrate. referred to a winter territory rather than a winter area—this
Among the Sylvia warblers those species that are rela- was quite deliberate. Remember that the first birds to arrive
tively sedentary tend to spend longer on their post-breeding secure the best territories. Greenish Warbler establish and
moult than do those which undertake long migrations. So for defend a winter territory and so presumably are in just as
example non-migratory populations of the Blackcap Sylvia much of a hurry in the autumn as they and the other spe-
atricapilla take around 80 days to complete the same moult cies I have mentioned are in the spring. Finally another
that birds of the migratory population of the United Kingdom Phylloscopus, the Willow Warbler Phylloscopus trochilus
undertake in just half of that time. Most Sylvia warblers com- moults not once but twice each year. Willow warblers
plete their moult on or close to their breeding grounds, but undergo a rapid and complete moult prior to both the
those with longer migrations may start a moult pre-migration, autumn and spring migration. Members of this species
interrupt it, and then complete it at a suitable staging post undergo particularly long migrations, breeding further north
en route. The birds of those populations which do have a and wintering further south than Chiffchaff for example. It is
particularly long migration, such as the Garden Warbler likely that they moult twice because their flight feathers are
Sylvia borin which breeds in northern and eastern Europe simply not sufficiently robust to make the trip twice.
and winters in Africa some 30ºS of the equator, delay their In order to understand the impact of migration upon the
moult until they reach their winter grounds. This is possibly moult strategies of the old world warblers and other old
because the distances travelled are so great that Garden world species Yosef Kiat and Nir Sapir have collected a data
Warblers arrive late and are forced to leave their breeding set involving the measurement of individuals of 134 pas-
grounds very early in the migration season and simply do not serine bird species resident in, or migrating through Israel.
have the time to complete a moult once they have finished Some of these species have relatively short migratory move-
breeding. Once on their winter grounds, birds are probably ments whilst others are long distance migrants. Furthermore
able to complete a moult at a more leisurely pace (not hav- the adult birds who typically undertake a complete annual
ing to fit in a breeding event) and as a consequence are able post-breeding pre-migration moult have a slightly different
to begin the northwards return journey with a set of fresh strategy to juveniles who undertake a partial post-fledging
primaries. It has been suggested that this is in itself signifi- moult that typically involves the replacement of body but
cant because the spring migration tends to be a bit of rush not flight feathers and complete their moult in their winter
to arrive in time to secure the best breeding territories and in quarters. Their idea was that birds of both age classes
such a race primaries in good condition are likely to confer should be expected to vary the timing and/or extent of their
an advantage. moult in a way that was related to the length of their migra-
A similar trend is observed in the moult/migration strategies tory journey and hence to the time available to them to fit a
of the species of another genus of old world warbler, the
Phylloscopus warblers. The Chiffchaff Phylloscopus collybita continued
Box 2.3 Continued
moult into their annual cycle. Their results (Figure 2.11) con- this are important because they help us to understand the
firmed that adults of species with shorter migratory jour- age-specific responses of species to pressures that vary
neys took longer over their moult than those with longer across an annual cycle.
journeys. Similarly they found that juveniles with shorter
journeys were likely to moult more of their body feathers References
prior to migration than birds with longer journeys (who Shirihai, H., Gargallo, G., and Helbig, A.J. (2001) Sylvia
complete their moult in their winter quarters). Juveniles Warblers. Helm, London.
moulting more feathers extended their moult over a longer Ginn, H.B. and Melville, D.S. (1983) Moult in Birds. The
period than those moulting fewer. The results of studies like British Trust for Ornithology, Tring.
(A) (B)
1.0
160
140 Post-juvenile moult extent (proportion) 0.8

Post-breeding moult duration (days)
120
0.6
100
0.4
80
60
0.2
40
0.0
0–2500 2500–5000 >5000 0–2500 2500–5000 >5000

Migration distance (km) Migration distance (km)
Figure 2.11 Adult birds migrating less far take longer over their post-breeding moult (A), and juvenile birds moult less of their feathers
before migration when they have longer migrations to undertake (B). Adapted from Kiat, Y. and Sapir, N. (2017) Age-dependent modulation
of songbird summer feather moult by temporal and functional constraints. The American Naturalist 189(2), 184–95.
2.7 Flight wings. They make these manoeuvres by altering

their wing shape, that is to say by morphing them.
I am confident that there is not a single reader of Lentik and co-workers have carried out wind tunnel
this book who, when watching birds fly, has not experiments on the paired wings of dead swifts (the
asked the question ‘how do they do that?’ To remain birds died during rehabilitation and were not sacri-
airborne and fly a bird relies upon two forces: lift ficed for the experiments). They morphed the wings
and thrust, which must be sufficient to counteract into a variety of shapes based upon observations of
two opposing forces: gravity and drag. Figure 2.13A flying birds and found that fully extended wings
illustrates the opposing directions of these forces in (long and thin and at 90° to the body) generate max-
a hypothetical situation. Gravity acts upon the mass imal lift, but are suited to lower speeds and slow,
of a bird pulling it downwards towards the earth. shallow turns. Wings swept back (to 45º relative to
To remain aloft therefore, it must generate sufficient the body) generate less lift, but minimize drag and so
lift. Drag forces (the friction forces which result as increase glide speed and enable a bird to turn sharply
the bird moves through the air) will push it back- at speed. So by morphing between these wing shapes
wards. To counter this a bird must produce suffi- (and using intermediates between them) swifts
cient thrust either directly through powered flight are able to control their glide. Key adaptations for
or more subtly by the manipulation of the lift/drag powered flight are set out in Box 2.4.
relationship. Swifts Apus apus spend almost their
entire life on the wing, coming to earth only to breed.
They even sleep on the wing, climbing to high alti- Key reference
Lentik, D., Müller, U.K., Stamhuis, E.J., et al. (2007)
tudes and flap-gliding through the night. As aerial
How swifts control their glide performance with
hunters of insects, speed and agility in the air are
morphing wings. Nature 446, 1082–5.
essential to them and I have to admit that watching Videler, J. (2005) Avian Flight. Oxford University Press,
screaming parties of young swifts gathering prior to Oxford.
their autumn migration is one of the thrills of my
birding year. During these bouts of aerobatics, and So wings, and specifically the morphology of wings,
when watching hunting swifts, I am amazed by their are the key to flight characteristics and to achieve
ability to gather speed and to perform seemingly the various modes of flight that I am about to dis-
impossible direction changes without flapping their cuss there are four basic wing types (see Figure 2.12).
(A) Dynamic soaring wing (C) High aspect ratio wing
(B) Elliptical wing (D) High lift ratio wing
Figure 2.12 Dynamic soaring wings (A) are long and narrow enabling birds such as Albatrosses, Petrels, and Shearwaters to glide at speed.
Elliptical wings (B) are broad and rounded; they are typical of birds requiring short bursts of speed and high manoeuvrability such as woodland
species and birds that are the prey of other birds. High aspect ratio wings (C) provide for speed and agility and are commonly found in aerial
hunters such as swallows and hawks. High lift ratio wings (D) are broad and fingered, they enable birds such as Storks and Vultures to soar but
have limited manoeuvrability. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002) Vertebrate Life. 6th edn Prentice Hall, New Jersey.
both lift and thrust are generated and there is a net

Box 2.4 Adaptations for flight movement of the bird forwards. Tilting the wing
upwards will of course increase drag and slow the
Birds have a number of key adaptations which enable bird. Note that lift is generally produced by the inner
them to undertake powered flight efficiently. They will be wing, as air moves over the surfaces of the second-
discussed in more detail throughout this book but the aries, whereas thrust is produced by the primaries
main ones are summarized here: of the outer wing (Figure 2.13E). The primaries are
1. Wings, fore limbs that are modified as aerofoils. asymmetrical and each of them acts as an aerofoil in
2. A skeleton that is strong and rigid, but that is very its own right—generating lift additional to that
light. This is achieved because bird bones are less solid produced by the wing itself. As the wing beats, the
than those of mammals or reptiles. They are filled with primaries twist such that on the down stroke they
a honeycomb of air spaces and strengthened by internal close to form a solid wing, but on the up stroke they
struts. open, reducing wind resistance.
3. The coracoid bone, which acts as a support for the
shoulder.
4. An enlarged sternum with a deep keel for the attach- 2.7.1 Gliding and soaring
ment of the large muscles associated with powered
flight. Under the right conditions birds are able to utilize
5. Large and powerful flight muscles. The pectoralis and the forces of lift and thrust generated by out-
supracoracoideus provide the power for flight. stretched wings to travel considerable distances
6. A highly efficient respiratory system. with minimal energy expenditure. They achieve
7. Considerable modification of the bones of the fore- this by gliding or soaring rather than by using ener-
limb. Fused hand bones, in some cases locking joints getically expensive flapping flight. Vultures, Storks
and in others wrist joints that rotate almost fully. and other large birds are well known for their abil-
8. The furcula or wishbone, which acts as a spring during ity to achieve altitude by hitching a ride on a rising
the wing-beat cycle. column of heated air. From the tops of these ther-
mals they are able to soar for long periods to find
food or to undertake stages of a migratory flight. By
I am not a physicist and do not propose to discuss soaring from the top of one thermal to the bottom of
in detail the aerodynamics of bird wings or the another repeatedly they can travel considerable dis-
aerodynamic theory of bird flight, but for those tances without the need to flap their wings. The
readers who do want to explore these areas I can most accomplished of the gliders are probably the
recommend Avian Flight, the excellent monograph Albatrosses and Giant Petrels of the southern
by John Videler, upon which the following sections oceans. With their very long, slender wings they too
of this chapter draw heavily. are able to travel large distances, and at considerable
As a wing pushes through the air it produces an speed, with almost no need to flap. To further
area of high pressure in front of it. As the air ‘splits’ increase energy conservation they possess a modi-
and moves quickly backwards across the upper and fied wing joint morphology that allows them to lock
less quickly across the lower surface of the open wing in position their fully stretched wings. Without this,
before being deflected downwards behind it, further other species exert muscle energy to achieve the
pressure differentials develop. The net effect is that same end. Unlike vultures, who use thermals to
air moves from the lower pressure areas towards the achieve lift, these seabirds ride the pressure differ-
higher pressure areas and the forces of lift and thrust entials that result when winds close to the ocean
result. The balance of these two forces depends upon surface move at a slower speed (due to friction)
the angle of the wing relative to the oncoming air than do the winds above them. This is termed
stream (Figure 2.13A). When, as in Figure 2.13B this dynamic soaring and relies upon there being a con-
angle of attack (as it is termed) is low, little thrust is stant wind, a perfect strategy then for the seabirds
generated but lift is produced. If the leading edge of of the roaring forties. Recent research involving the
the wing is tilted forwards (Figure 2.13C and 2.13D) monitoring of the fine scale flying behaviour of
Total lift
(A)
Thrust
Total drag
Most of lift R
R
(B) (C) Rest of lift
Thrust Drag
Flow of Drag
air across
inner wing ss
ro
ac
air
of p
w
o ti
Fl ing
W
M
(E) Outer wings

(Primary feathers)
Inner wings
(D) (Secondary feathers)
Movement of bird
Movement Vertical movement
air Vertical movement
of wing-tip wing tip
e to Inner wing
relative tiv
rela
to bird p
g ti
of win
ment
ove
m
ual
Act
Figure 2.13 The forces acting upon, and generated by, a generalized flying bird. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002)
Vertebrate Life. 6th edn Prentice Hall, New Jersey.
Manx Shearwaters Puffinus puffinus with GPS trackers Smaller birds generally lack the wing area to adopt
has revealed that birds adjust their flapping/soaring gliding as a main mode of flight. But they are able to
behaviour to maximize their efficiency as the wind reduce energy expenditure to some degree by punc-
changes. Rory Gibb and his colleagues found that tuating their flapping flight with short glides or
tracked birds were more likely to soar in tailwinds bounds. Typically their flight path is sinusoidal,
and crosswinds above 8 m per second, but at lower gaining height during a burst of flapping and then
speeds they were more likely to flap. falling towards the end of the short glide. But the
savings gained by milliseconds of gliding are con-
Key reference siderable. As an example, in a study of the bound-
Gibb, R., Shoji, A., Fayet, A.L., et al. (2017) Remotely ing flight of the Zebra Finch Taeniopygia guttata
sensed wind speed predicts soaring behaviour in a (Figure 2.14) Tobalske and co-workers have shown
wide-ranging pelagic seabird. Journal of the Royal So-
that birds were able to reduce their flapping (and
ciety Interface 14, 20170262.
presumably therefore their energy expenditure)
excursion (mm)
40
Wingtip
0
–40
40
Altitude (mm) Flapping
20
0 Bounding
–20
0 50 100 150 200 250 300 350
Time (ms)
Figure 2.14 The flapping and bounding flight of the Zebra Finch. By flapping, the bird achieves height (altitude) and momentum so that during
a non-flapping bound it can conserve energy. Wing tip excursion is a descriptive for flapping activity. Adapted with permission from Tobalske, B.W.,
Peacock, W.L., and Dial, K.P. (1999) Kinematics of flapping flight in the zebra finch over a wide range of speeds. Journal of Experimental Biology
202(13), 1725–39.
by between 22 per cent and 45 per cent depending generate no forwards thrust (or at least no more
upon their speed of travel. thrust that is required to counter the drag that they
are experiencing). For the vast majority this is very
difficult and cannot be sustained for anything more
2.7.2 Flapping flight than short periods prior to landing, or striking at
The power for flight comes from the flapping of the food. But there is one group, the Hummingbirds
wings. During a single beat cycle of the wing, in that have perfected hovering to the point that they
some cases a period of just milliseconds, the wing are able to hold their position in mid air for pro-
form and therefore its aerodynamic properties longed periods. They can also fly forwards, back-
changes a number of times. The inner wing (the sec- wards, and even sideways. This is possible because
ondaries) simply moves up and down during the the wing of a Hummingbird has an anatomy unlike
cycle and as it does so it acts in the same way as a that of any other bird (except their close relatives
fixed wing during gliding in that it generates most the Swifts). The Hummingbird inner wing is rela-
of the lift experienced by the bird. As was men- tively very short and is held in a fixed ‘v’ position
tioned previously, the primary feathers twist dur- close to the body. The outer wing (with 10 long pri-
ing the beat, ‘closing’ the wing surface on the maries) forms the main surface and accounts for more
down stroke and opening it to reduce wind resist- than 80 per cent of the total wing (compared to c. 40
ance at it moves upwards. At the same time the per cent in the Buzzard Buteo buteo for example).
wrist joint (between the inner wing and the outer The Hummingbird main flight muscles are far
wing) twists so that on the down stroke the wing larger (relative to body mass) than those of other
moves both down and forwards and on the up flying birds. The wrist joint is particularly flexible
stroke moves up and backwards. So the outer enabling the outer wing to twist almost upside down
wing is moving through the air in a sort of figure on the back stroke. When hovering, hummingbirds
of eight motion. As it moves forward and down- generate lift and thrust on both the forward and
ward on the down stroke the angle of attack of the back stroke, both of which sweep so far that the
wing is high and the lift generated has a forwards wing tips are brought close together. Their wing
direction—thrust. beat, describing a figure of eight in the air that is
To hover, to fly at a fixed point, birds have to almost horizontal to the ground, is remarkably fast.
generate lift sufficient to support their weight but Speeds of as much as 200 beats per minute have been
recorded from the Ruby-throated Hummingbird x-rayed it 200 times per second while it flew! From
Archilochus colubris during courtship hovering, the figure we can see that the humerus is almost
although speeds between 10 and 80 beats per sec- parallel with the body at the start of the sequence
ond might be more typical of the family. but that it moves upwards and rotates forwards as
So, we can see the path of the wing during flight the supracoracoideus contracts on the up stroke
and infer from that the movement of joints, etc. But (Figure 2.16B). The bones of the hand at this point
what is going on inside the bird? Figure 2.15 illus- are held at approximately 90° to the body. They
trates schematically the main anatomical compo- remain there as the wing closes (Figure 2.16C) and
nents of the wing. There are actually 45 different are swept backwards and down as the contraction
muscles in the bird wing, but only the two thought of the pectoralis causes the down stroke. This
to be most significant (and currently best under- research has also revealed the role of the furcula, or
stood) are shown. These are the pectoralis and the wishbone, during flight. As the humerus rotates
supracoracoideus, the two relatively large muscles forwards and moves downwards the heads of the
which attach to the deep keel (corina) of the sternum furcula move apart. As they bend, the arms of the
and between them provide the power responsible furcula act as a spring and store some of the force of
for the wing strokes of flapping flight. Contraction the down stroke. They then release the stored
of the pectoralis pulls the wing down and forwards energy as the furcula returns to its resting position
during the down stroke of flight. The supracora- during the up stroke. The exact function of this pro-
coideus pulls it upwards and backwards during the cess is not yet understood. The release of energy
up stroke. may assist the supracoracoideus in raising the wing,
The effect of these muscular contractions upon but it seems most likely that it has a respiratory
the bones of the wing can be seen in Figure 2.16 function because a relationship between the wing
which was obtained by Farish Jenkins and col- beat cycle, the action of the furcula, and the com-
leagues when they trained a European Starling pression of the air sacs has been identified.
Sturnus vulgaris to fly in a wind tunnel whilst being
Flight path: Energy, flight, and migration. page 59.
filmed using radiographic film. Essentially they
Carpometacarpus
Alular digit
Wrist joint
Major digit
Radiale
Shoulder joint
Ulnare
with trioseal canal Propatagium Minor digit
Vertebra Scapula Radius Ulna
Furcula Humerus
Rib cage
Elbow joint
Metapatagium
Coracoid
Tendon
Sternum
M. Pectoralis
M. Supracoracoideus (grey)
(black)
Carina
Figure 2.15 An overview of the anatomy of the avian wing and rib cage. From Videler, J.J. (2005) Avian Flight. Oxford University Press, Oxford.
(A) (B) (C) (D)
Figure 2.16 Skeletal movements of the European

Starling Sturnus vulgaris during flapping flight. From
Jenkins, F.A. Jr, Dial., K.P., and Goslow, G.E. Jr (1988)
A cineradiographic analysis of bird flight: The wishbone in
starlings is a spring. Science 241, 1495–8 , reprinted with
permission from AAAS.
surface area for oxygen transport. In mammalian

2.7.3 Respiration and flight energetics
lungs inhaled air passes along bronchioles (tubes) to
The lipids (fats), carbohydrates, and proteins of the alveoli (dead-end sacks) where oxygen is absorbed.
body provide the energy for metabolic activity, Exhaled air reverses back along these tubes in what
including flight. The ‘burning’ of these compounds is called a tidal fashion. The lungs of birds are very
in the presence of respiratory oxygen provides the different. They lack the alveoli and instead the bird
energy required for the splitting of cellular molecules lung is composed of a network of very thin tubes
of ATP (adenosine triphosphate), which in turn termed parabronchi (the bird lung is often therefore
provide the energy needed to control the contrac- referred to as a parabronchial lung), each of which
tion of muscle fibres. Oxygen and fuel from feeding divides into very many thinner capillaries where
(which will be discussed in chapter 6) are therefore gaseous exchange takes place. Inhaled and exhaled
essential for flight. Terrestrial vertebrates obtain air pass through the lung in the same direction (i.e.
oxygen when air is inhaled and the oxygen in it is a non-tidal flow) and in fact a complete cycle of res-
transferred across the walls of the lung to the blood piration involves not one but two breaths. This is
stream. Birds have a higher metabolic rate than possible because the lungs of birds are connected
other terrestrial vertebrates, they have higher body to a network of air sacks within the body cavity
temperatures and faster heart rates, and they use (Figure 2.17A).
more oxygen in flight than mammals do when run- During the first breath, inhaled air passes into
ning. We might therefore expect the lungs of birds and through the lung and into the abdominal air
to be particularly large, but in fact they are smaller sac. Contraction of the abdomen during exhalation
than those of similarly sized mammals. This is forces air back out of the abdominal air sacks, back
probably a necessary adaptation to keep down through the parabronchi of the lung and gas
body mass for efficient flight. So how do birds get exchange takes place (Figure 2.17B). During the sec-
the oxygen that they need? Well their lungs may be ond breath, the ‘stale’ air in the parabronchial lung
small—but size for size they have a larger internal is forced into the anterior air sacks on inhalation
(A) 1
2
2a
3
2b
6
(B) Inhalation 5 Exhalation

1
2 4
3
Figure 2.17 Gaseous exchange in the respiring bird. Figure (A) illustrates the parabronchial lung (7) and air sack (1–6) system of a generalized
bird. Air sacks labelled include: 1, the infraorbital sinus; 2, the clavicular air sack; 3, the cervical air sack; 4, the cranial thoracic air sack; 5, the
caudal thoracic air sack; and, 6, the abdominal air sacks. Figure (B) illustrates the pattern of air-flow through the system during both inhalation
and exhalation. From Pough, G.H., Janis, C.M., and Heiser, J.B. (2002) Vertebrate Life. 6th edn Prentice Hall, New Jersey.
and out of them, and out of the bird, during exhalation their muscle fibres are shorter, and the mitochon-
(Figure 2.17B). So in a bird oxygen uptake is hap- dria in those fibres are both more numerous per
pening on both inhalation and exhalation and bird unit area and closer to the cell surface. These adap-
lungs are far more efficient at oxygen uptake than tations combine to provide birds with the efficient
those of similar sized mammals. After uptake, oxy- and effective respiration system that is essential for
gen is transported through the bloodstream to the flight.
tissues of the body by the carrier molecule haemo-
globin. Avian haemoglobin has a lower affinity for
2.7.4 Flying high
oxygen than that of mammals, but for birds with a
higher metabolic rate this is actually advantageous Although a relatively lower haemoglobin-oxygen
because it results in a higher oxygen unloading rate affinity is advantageous for most birds there are
at the flight muscles and other tissues. Furthermore, situations when it could be something of a problem.
oxygen uptake by the flight muscles is very efficient As we have discussed lower affinity can be an
because volume for volume they have more blood advantage because it allows more efficient unload-
capillaries than comparative mammalian muscle, ing for cellular respiration, but this is only the case
because the system is optimal at the partial pressure haemoglobin function of a number of species of
of atmospheric oxygen close to the surface of the Andean hummingbird, some of which like the
earth. As altitude increases the partial pressure of Great-billed Hermit Phaethornis malaris live at lower
atmospheric oxygen decreases and under these altitudes and others like the Andean Hillstar
conditions haemoglobin with a low affinity for oxy- Oreotrochilus estrella live at altitudes up to 5,000 m
gen would be less efficient and respiration could above sea level. They found a positive relationship
be compromised. So what is the solution? Joana between altitude and haemoglobin oxygen affinity.
Projecto-Garcia and colleagues have compared the Furthermore, by comparing the haemoglobin of
Box 2.5 Formation flying saves energy
My home is right under the flight path that Pink-footed of free flying Great White Pelicans Pelecanus onocrolatus
Geese Anser brachyrhynchus follow as they migrate into the singly and in flocks. They trained eight birds to fly behind a
UK in the autumn. It’s a joy to hear them calling and to see moving motorboat and filmed them doing so. The birds had
their long, drawn out V-formations as they pass overhead. been fitted with heart rate monitors and from the data from
Even non-birders notice them and I am usually asked why do these (Figure 2.18), and the films that they made, it was pos-
they fly in a V? Quite simply I say large birds fly in a V to sible for the team to compare the individual heart rates and
conserve energy. I am sure that you have been told the same wing-beat rates of all of the birds. These measures are pre-
thing many times, but I guess it might surprise you to know sumed to correlate closely with energy expenditure during
that hard data to support this explanation are actually quite flight.
rare. Good data have however been recently provided by Gliding lone pelicans and birds flying 50 m and 1 m above
Henri Weimerskirch and co-workers. They have made the water flapped more often and had higher heart rates
detailed observations of the heart rates and wing beat rates than did birds flying in formation at 1 m (Figure 2.19). Birds
Figure 2.18 Flying in formation increases the individual flight efficiency of these migrating Pink-footed Goose Anser brachyrhynchus
(© Will Scott).
at the front of the V have a wing-beat frequency similar

to that of single birds at the same height, but those
behind the leader clearly benefit. Although from the fig-
ure you should note that the benefits diminish slightly
the further from second place a bird flies. The researchers
also noticed that birds at the rear of the formation con-
stantly adjusted their position relative to the group, pre-
105
wingheat frequency
sumably they were maximizing the energy savings that

90
75
they made.
(b.p.m)
Mean
60 1
45 2
3 4 5 Last
12
0
200
heart rate (b.p.m)
190
180
Mean
170 Figure 2.19 Variation in heart beat rate (a measure of

160 energy expenditure) of gliding, solitary and formation flying
150 pelicans. Reprinted by permission from Weimerskirch, H.,
Gliding Alone at Alone at In Martin, J., Clerquin, Y., et al. (2001) Energy saving in flight
50 m 1m formation formation. Nature 413, 697–8.
closely related groups of high, mid, and low alti- and therefore use more energy. This probably isn’t
tude hummingbirds they found that the same two a surprise to you. The relationship between power
amino-acid replacements in the haemoglobin mol- (flapping) and speed seems to be a straightfor-
ecule explained the differences in haemoglobin ward one. It is not however. Whilst it is true that
activity across several species groups suggesting flying fast is energetically expensive, so is flying
that the same adaptations had evolved several slowly (remember that hovering is very expen-
times, an example of parallel evolution. sive). Aerodynamic theory suggests that the
power curve (the relationship between power and
Key reference velocity) of flight should be U shaped. By flying
Projecto-Garcia J., Natarajan, C., Moriyama, H., et al. Magpie Pica pica, Barbary Dove Streptopelia risoria,
(2013) Repeated elevational transitions in haemoglobin
and Cockatiel Nymphicus hollandicus in wind
function during the evolution of Andean humming-
tunnels and directly measuring pectoralis muscle
birds. Proceedings of the National Academy of Science
110(51), 20669–74. activity, Tobalske, Dial, and colleagues have shown
that in the case of these species the power curves
which result are broadly U shaped (Figure 2.20).
2.7.5 Flight speeds
Obviously there are times when a bird will have to
Some birds alter their flight speeds relative to fly fast (to catch mobile prey or to escape a predator
flock-mates to conserve energy (see Box 2.5) and for example), or perhaps fly slowly (to locate cryp-
earlier in this chapter I described the way in which tic food or perhaps as part of a display, although in
a swift can adjust its flight speed by altering the such cases the function of the display may of
shape of its wings during a glide. But not all birds course be to advertise that you have energy to
are as accomplished at gliding as swifts and in spare) but based upon these observations we might
many cases to fly faster a bird must flap harder expect birds to select flying speeds that conserve
250
200
Pectoralis mass-specific
power (W kg–1)
Dove
150
100 Cockatiel
Figure 2.20 U-shaped power curves of three species of flying bird. Note that in all
50 cases slower and faster flight speeds incur a higher energy cost (i.e. more muscle
Magpie power is required). Reprinted by permission from Tobalske, B.W., Hedrick, T.L. Dial,
0 K.P., and Biewener, A.A. (2003) Comparative power curves in bird flight. Nature 421,
0 5 10 15 363–6; and Dial, K.P., Biewener, A.A., Tobalske, B.W., and Warrick, D.R. (1997)
Velocity (m s–1) Mechanical power output of bird flight. Nature 390, 67–70.
energy whenever practicable, to adopt optimal flying The ability of birds to assimilate external informa-
speeds. In fact it has proven very difficult to dem- tion has an impact upon collision avoidance during
onstrate that birds fly at an optimal speed in real flight, see Box 2.6.
life, perhaps because birds incorporate more infor-
Flight path: Flight can have a display or information
mation (about their momentum, their motivation, the
exchange function during foraging, territoriality or
weather etc.) into their decision-making than we
courtship. page 101 and 123.
have taken into account when making our prediction.
Box 2.6 Collision avoidance
How do birds avoid collisions? test the hypothesis that birds utilize fore-aft pattern velocity
I am always amazed at the ability of a hunting Sparrowhawk during flight to avoid collisions. They trained Anna’s
Accipiter nisus to dart in and out of a hedgerow chasing its Hummingbirds Calypte anna to fly along a tube to a food
passerine prey, or of a feeding hummingbird to flit from source. During the flights they projected moving and/or
flowerhead to flowerhead as little more than a blur—at static patterns onto the walls of the tube and monitored
such speeds how on earth do birds avoid collisions with one the behaviour of the flying bird. In one experiment for
another and with objects in their environment? example they projected patterns of vertical bars onto the
We know that insects use the motion of images across the walls of the tube, one side they kept static and the other
eye (something called pattern velocity) to provide information they moved forwards or backwards away from the feeder.
about their own movement relative to their surroundings. Bees under a similar treatment would be expected to fol-
Experiments involving honey bees have demonstrated that low a curved flight path, but the hummingbirds were able
pattern velocity is used to maintain course, to control speed to maintain their direction of flight straight down the mid-
and altitude, and to gauge distance travelled. From these dle of the tube—this demonstrates that birds, unlike bees,
experiments we also know that bees are particularly attuned do not steer by balancing nasal-to-temporal pattern
to react to nasal-to-temporal pattern velocity; more simply velocity. Further experiments revealed that in fact hum-
they modify their flight behaviour by monitoring the speed at mingbirds pay more heed to pattern velocity in the vertical
which objects appear to pass them laterally as they fly axis—to the changing apparent height of objects as they
through the environment. This is something that you will be move towards them. It is possible that this allows birds to
familiar with if you drive; you will notice that a sign that use apparent expansion in the size of the objects they
seems to take an age to reach as you look forwards seems to approach to judge speed and distance and to react
whizz by if you try to read it as it passes. By assessing changes accordingly (imagine running towards two identical hori-
in the apparent speeds of several signs you would be able to zontal beams, one a few metres ahead of you and one
determine your rate of acceleration or deceleration and per- further away—the close one would appear to grow at a
haps adjust your speed accordingly. faster rate). So rather than relying upon pattern velocity to
Roslyn Dakin and her colleagues have carried out some avoid collisions, birds utilize information about objects in
elegant experiments involving trained hummingbirds to their environment.
Tectofugal
Optic Tectum nRt
Pathway
Thalamofugal
OPT WULST
Pathway
LM
The eye Accessory
Optic System
nBOR
Figure 2.21 Key neuronal elements of the avian visual system including the tectofugal pathway (brightness, colour, pattern, and simple
motion); the thalamofugal pathway (spatial orientation, motion perception, and binocular vision; and the accessory optic system (ability to
follow an object whilst keeping the head stationary). Abbreviations are explained in the main text. Adapted from Wylie, D.R., Gutiérrez-
Ibàñez, C., and Iwaniuk, A.N. (2015) Integrating brain, behaviour and phylogeny to understand the evolution of sensory systems in birds.
Frontiers in Neuroscience 9(281).
Through experiments with pigeons, the neurons that pro- Hummingbirds

cess information about object expansion have been identi- Kestrel
fied within the nucleus rotundus, an area of the thalamus Spinebill
Kingfisher
which is known to be part of the tectofugal pathway, one of Grouse
three main neuronal pathways comprising the visual system Hawk
Nightjar
of birds (Figure 2.21). The tectofugal pathway is the major Owls
visual pathway in birds, accounting for 90 per cent of retinal Swifts
Pigeon
projections (the neuronal processes emanating from the ret- Songbirds
ina), and it is involved in the assessment of brightness, rec- Coot
ognition of colour, pattern discrimination, and both simple Shorebird
Egret
and complex motion. The thalamofugal pathway (comprising Duck
the principle optic nuclei of the thalamus and the wulst) is Frogmouth
Cockatiel
thought to be involved in spatial orientation, motion percep-
tion, and binocular vision. The Accessory Optic System (AOS) 0.0 0.1 0.2 0.3
comprising the LM (or nucleus lentiformis mesencephalic) LM % Brain
and the nBOR (nucleus of the basal optic route) is involved
in the processing of the optic-flow information generated by Figure 2.22 The LM (nucleus lentiformis mesencephalic) of the
self-motion. Integration of all of these pathways (and others) brain, which is involved in the ability of an organism to follow the
is essential for flight. The LM of the AOS is known to be movement of an object with their eyes while the head remains
important in the optokinetic response (OKR), the ability of an stationary, is more developed (expressed as percentage of volume)
in hovering birds such as hummingbirds, kestrels, and kingfishers.
organism to follow the movement of an object with the eyes
Adapted from Wylie, D.R., Gutiérrez-Ibàñez, C., and Iwaniuk,
whilst keeping the head stationary. The OKR is essential to a A.N. (2015) Integrating brain, behaviour and phylogeny to
hovering animal like a hummingbird and so we might expect understand the evolution of sensory systems in birds. Frontiers in
them to have a particularly well developed LM, and com- Neuroscience 9(281).
pared with other birds they do (Figure 2.22).
a pylon or wind turbine projecting tens of metres above the
Collisions do happen surrounding vegetation? Collisions with such static objects
But in spite of the adaptations enabling birds to avoid high have been estimated to be the most significant non-natural
speed aerial collisions, they do happen and often with cause of mortality amongst large soaring birds like Eagles,
catastrophic effects. It has been estimated that each year Vultures, Cranes, and Storks and as a result collision mitiga-
hundreds of millions of birds die as a result of collisions with tion is a pressing conservation issue. In his excellent book
man-made static objects: fences, buildings, power-lines, The Sensory Ecology of Birds, Graham Martin proposes a
wind turbines etc. Some of these we can perhaps under- possible explanation. Considering the plight and flight of the
stand—when a bird hits your window you assume that it
simply didn’t see the glass. But how is it that birds don’t see continued
Box 2.6 Continued
Griffon Vulture Gyps fulvus he suggests that two interacting than this. Martin also suggests that it is possible that birds
factors come together to explain the inability of these birds frequently fly at, or beyond, the limits of their perceptual
to avoid what to humans seem to be obvious obstacles. First, ability by which he means that they may not be in a position
unlike the new world Vultures that use their sense of smell to to process all of the high speed visual information they
locate their food, old world Vultures rely upon their vision. As receive as they move through their environment and that as
a result, soaring birds spend a lot of their time looking down. a result they often extrapolate or predict what is in front of
As Figure 2.23 illustrates, the eyes of a Griffon Vulture are them rather than actually seeing it—it may be that because
positioned such that it has relatively large ‘blind spots’ they don’t expect a fixed position obstacle in the open sky
above and below the head, and a Vulture’s forward vision they simply fail to notice it until it is too late.
has a lower acuity than it’s lateral vision. It seems likely
therefore that they collide with things simply because they Mitigation
can’t see them! But, perhaps there is slightly more to it What can be done to minimize collision risk? It may be pos-
sible for us to position turbines etc. in places that birds are
less likely to encounter them. But where there is a risk of
collisions efforts should be made to prevent them. It could be
possible to manipulate the environment around an obstacle
to divert birds away from it. Planting trees in front of power
lines might ‘force’ birds to lift above them. Putting flags,
discs or balls on the lines to increase their visibility has been
shown to reduce collision incidence in some cases (but it is
likely that if the birds don’t see a line because they are flying
beyond their perceptual ability they probably won’t see a
60° disc either!). In the case of turbines, it may be possible to
minimize collision risk by siting wind farms in areas less fre-
quently used by birds, for example away from known migra-
tion bottlenecks or the flightpaths used by birds moving to
and from a breeding colony. Alternatively, because an immo-
bile turbine probably poses less of a risk than the active tur-
bine (simply because the sweeping blades decrease the area
of ‘safe’ space through which to fly), operating the turbine
only during those periods during which collision is less likely
might be beneficial. Currently there do not seem to be any
really good solutions to the collision problem, but as increas-
ing numbers of wind farms (and other large fixed structures)
are being built, this is a fast moving field and hopefully
major breakthroughs will be made in the near future.
References
Dakin, R., Fellows, T.K., and Douglas, L.A. (2016) Visual guid-
ance of forward flight in hummingbirds reveals control
based on image features instead of pattern velocity.
Proceedings of the National Academy of Science 113(31),
Figure 2.23 Flying old world vultures need to scan the ground 8849–54.
below them for carrion. They also need to keep a look-out
Martin, G.R. (2017) The Sensory Ecology of Birds. Oxford
side-ways for other vultures who they might be able to follow
towards food. As they fly they pitch their heads through 60o as
University Press, Oxford.
shown in figure A. As a consequence they have fairly large blind Wylie, D.R., Gutiérrez-Ibàñez, C., and Iwaniuk, A.N. (2015)
spots above and in front of them (shaded blue in figures A and B). Integrating brain, behaviour and phylogeny to understand
Adapted from Martin, G.R. (2017) The Sensory Ecology of Birds. the evolution of sensory systems in birds. Frontiers in
Oxford University Press, Oxford. Neuroscience 9(281).
2.8 The evolution of flight birds had an anatomy and feather types that would
and flightlessness have facilitated gliding but perhaps not sustained
flapping flight. However, it is also the case that
most (but not all) of the ancestral and early birds
Flight path: evolution of birds from dinosaurs, page 6.
had hind legs that are more like those of running
dinosaurs than climbing animals and so the arboreal
Just as the question of the evolution of birds from hypothesis alone seems to be insufficient.
dinosaurs has generated controversy (see chapter 1)
so has the question of the evolution of avian Key reference
flight itself. So how and when did flight evolve? Dececchi, T.A., Larsson, C.E., and Habib, M.B. (2016)
The rich dinosaur, paravian, and avian fossil record The wings before the bird: an evaluation of flapping-
that we discussed in the previous chapter helps based locomotory hypotheses in bird antecedents.
PeerJ 4, 2159.
us to go some way towards answering this question
(Figure 2.24).
One school of thought suggests that flight So if the early birds and their ancestors were run-
evolved initially as gliding flight and then through ning animals, what support is there for the cursorial,
subsequent modification as powered flight, when WAIR, and vertical leap hypotheses? All of these
animals climbed trees (or cliffs etc.) and used flight behaviours, to initiate take off, can be seen amongst
either to slow their fall to earth or to extend their modern birds and so all seem plausible; wildfowl
leap from one high place to another, the tree-down run across the surface of a lake whilst flapping,
or arboreal hypothesis. A second school of thought passerines leap into the air and then flap, and
suggests that flight evolved as a means by which partridges have been observed to use WAIR to pro-
running animals could increase their stability dur- pel themselves up slopes that are otherwise too
ing an extended leap perhaps to escape a pursuing steep to climb. Alexander Dececchi and his col-
predator or to capture fleeing prey (the ground-up leagues have used biomechanical modelling tech-
or cursorial hypothesis). The third proposal, the niques taking into account wing and body size,
wing assisted incline running (WAIR) hypothesis anatomy, and inferred locomotory ability (running
suggests that wings were initially used to propel speed for example) in an attempt to establish the
animals forward as they ran up a slope that would possibility that non-avian theropods had the ability
otherwise be too steep to climb. Finally it may be to take off and fly in the manner of modern birds—
that flapping (and subsequently flapping flight) and to determine the most likely hypothesis for the
evolved as a means of increasing the height gained evolution of flapping flight. They found that whilst
during a vertical leap. So what evidence is there to a small number of paravians like Microraptor would
support these ideas? have been capable of powered flight, most of the
Evidence in support of the arboreal hypothesis winged ancestors of birds would not have been.
comes from a variety of sources; the fossil remains They did not find particular support for any one of
of many early birds seem better suited to gliding the cursorial, WAIR, or vertical leap hypotheses
than to powered flight; many of the dinosaur ances- over the others; although WAIR did receive the
tors of birds were able to climb; the evolution of least support it could not be ruled out entirely in the
flight in mammals (bats) is thought to have been case of small-bodied, large-winged animals like
‘tree-down’; there is a link between climbing and Archaeopteryx. Dececchi’s analyses do however sug-
gliding in a wide range of vertebrate taxa; using gest that flapping flight appeared independently
gravity to provide the initial power for flight is eas- several times in the dinosaur/bird lineage and so
ier and more efficient than fighting against it to take perhaps a single explanation for the evolution of
off from the ground; the flight stroke needed to pro- flight will always be insufficient. It may seem
long a glide is far simpler than that required to lift a somewhat paradoxical but from the fossil record
bird from the ground; and perhaps most signifi- (chapter 1) and Dececchi’s work it appears that
cantly a number of the fossil precursors of modern pennaceous-feathered wings and/or tails first
Psittacosaurus
Could not fly
Filaments Dilong
Protofeathers Could not fly
Pennaceous feathers
Bat-like skin membrane
Ornithomimus
Probably could not fly
Caudipteryx
Could not fly
Yi
Plausible glider
Protofeathers;
could not fly
Dinosaurs Microrptor
Plausible glider/incipient
flapping flight
Theropods
Maniraptoriforms Zhenyuanlong
Had wings, but Probably could not fly
probably could not fly
Pennaraptorans
Had wings; Possible
incipient flight
Anchiornis
Paravians Plausible glider/incipient
Had wings; Possible flapping flight
incipient flight
Archaeopteryx
Incipient or more advanced
flapping flight
Avians (birds)
Had wings; capable
of powered flight Modern bird
Flapping flight
Figure 2.24 Feathers and wings evolved in some early dinosaurs, but flight came later and it is likely that only birds were capable of full
powered flight. From Brusatte, S.L. (2017) A mesozoic aviary: Biomechanical models are key to understanding how dinosaurs experimented with
different ways of flying. Science 355(6327), 792–4. Reprinted with permission from AAAS.
evolved amongst the flightless theropod dinosaurs. either flight in search of food or flight off the island,
It is highly likely therefore that their initial function for whatever reason, is particularly important.
was not related to locomotion. From fossil evidence Amongst some marine birds the need to fly may be
we know that the feathers of these wings were secondary to the need to swim and in fact wings
highly pigmented, so perhaps they had a display may even be a hindrance under water, so they have
role in courtship or aggression. Or perhaps they been reduced (and as a result some strong swim-
were used as a shield against the elements during mers are weak fliers), or even changed completely
the care of young. through the course of evolution in the case of the
It was once presumed that flightless birds had penguins, to become flippers.
evolved from birds that had themselves never
evolved the ability to fly. We know today that this is
Summary
not the case and that extant flightless forms are in
fact derived from flying ancestors. If flight was suf- Feathers have a range of functions (insulation,
ficiently advantageous to the ancestors of modern display etc.) but are crucial to flight and have to be
birds why then should the ability to fly have been constantly maintained and regularly replaced by
lost? Well, there are situations where flight is no the process of moult. Flight is energetically costly,
longer advantageous. The evolution of flightless- but birds possess anatomical, physiological, and
ness is common for example amongst those species behavioural adaptations to optimize their efficiency.
of terrestrial birds inhabiting isolated islands. In Flightlessness in modern birds has evolved as the
such habitats, predators are often absent and so loss of flight rather than being the precursor of the
escape flight is not required, nor is it likely that ability to fly.
C H A PT ER 3
Movement: migration and navigation
‘The stork in the sky knows the time to migrate.’

The book of the Prophet Jeremiah, chapter 8, verse 7
The quotation that opens this chapter demonstrates

Concept
that the human appreciation of migration is not a
Categories of movement
new phenomenon. The prophet uses migration as a
It is possible to recognize two distinct categories of
metaphor to put across a point to his ‘audience’.
bird movements. The first includes those movements
This will only work if that audience understand the that are concerned with a proximate response to an
substance of that metaphor. actual resource shortage: foraging trips, commuting or
In this chapter I will assume that the reader is ranging between patches, and dispersal from a natal
more than a little aware of the phenomenon of area to an available local area to establish a home
migration but perhaps less aware of its detail. range. These movements conclude when the need for
I want therefore to consider some fundamental the resource involved is satisfied.
points about migration. Why does it happen? How The second category of movements are true
is it controlled? How are the bodies of birds adapted migrations, triggered by internal rhythms or by a
to facilitate migration? What are the consequences forecast of resource shortage. They are characterized by
the physiological suppression of the proximate response
of this behaviour both for the birds themselves, and
to resource need and their conclusion is a result of
in terms of their management and conservation?
physiological changes resulting from the movement
I also want to consider other movements of birds itself.
that whilst not strictly migrations per se, do have a
lot in common with them. Finally, I want to think
If they know nothing else about birds, most people
about the mechanisms that birds use to navigate
will be able to tell you that some of them migrate.
during migration, and to extend that discussion
They might not get the detail right, but they will be
to consider the navigation of birds during their
able to tell you that birds fly south (or north depend-
daily lives.
ing on your hemisphere of residence) to avoid bad
weather. The general phenomenon of migration,
the periodic mass movements of species along
Chapter overview
established routes, fills us with awe. In fact the level
3.1 The ecology of migration of interest in these long distance movements is such
3.2 Genes and migration that in 2004 and 2005 millions of people followed
3.3 Physiology and migration with rapt attention the progress of a handful of
3.4 The weather and migration Tasmanian Shy Albatrosses Thalassarche caute as
3.5 Navigation they undertook a journey of around 10,000 km
DOI: 10.1093/oso/9780198804741.003.0003
M O V E M E N T: M I G R AT I O N A N D N AV I G AT I O N 49
across the open waters of the Southern Ocean to Foundation and, in some senses most importantly,
and from South Africa. Tracking the birds was pos- by publicity-generating private individuals such as
sible because they had been fitted with electronic the model and actress Jerry Hall (who sponsored
satellite tracking devices and because their daily the 2004 winning bird ‘Aphrodite’) and the pub-
progress is mapped on an open-access internet site. lisher Nicholas Coleridge, a direct descendent of
The project, The Big Bird Race, was an innovative Samuel Taylor Coleridge author of Rime of the
collaboration between the business community (in Ancient Mariner, the classic poem in which the fate
this case the bookmaker Ladbrokes), the Tasmanian of an Albatross is somewhat prophetically linked to
State Government, the scientists of The Conservation the fate of man. The bets placed on The Big Bird Race
Box 3.1 Albatrosses in crisis
The Diomedeidae, the family to which the albatrosses Indian Ocean. Interestingly this area also supports a resident
belong, has been described as the world’s most threatened (breeding) population of Grey-headed Albatross, but one
bird family. In 2017 the IUCN Red List categorized all 22 that is relatively sedentary. Finally, some South Georgian
species as being under threat of extinction at some level. birds make one or more trips around the world between
Three of the species (Tristan Albatross Diomedea dabbenena, breeding attempts. Some of these birds fly close to 1000 km
Amsterdam Albatross Diomedea amsterdamensis, and per day and the fastest recorded circumnavigation took just
Waved Albatross Phoebastria albatrus, are all critically 46 days (in theory the fastest non-stop circumnavigation
endangered and therefore at high risk of extinction. A fur- would take 30 days). Satellite tracking has also revealed
ther 12 species are listed as being threatened, vulnerable or that in addition to annual migrations individual Wandering
endangered, and the remainder are classed as being near Albatross may make foraging trips of between 3,600 km and
threatened. In spite of the excellent work of ornithologists 15,000 km over up to 33 days when their mates are incubat-
and conservation organisations, 12 species still have a ing eggs. Once the chicks have hatched the trips shorten to
declining population trend. For two species the trend is around 300 km over three days.
unknown, four species are thought to be stable, and thank- It is crucial that the movement patterns of these seabirds
fully four are on the increase (but not yet secure). are established so that effective conservation strategies can
Despite their enigmatic status as lonely wanderers of the be developed. Unlike many birds, the albatrosses are not
oceans, we know surprisingly little about the biology of endangered because their breeding habitats are threatened,
these long-lived seabirds away from their breeding grounds they are dying out largely because they are the accidental
because historically they have been very difficult to study. For bycatch of human fishing activities. Specifically hundreds of
example, despite more than 20,000 Wandering Albatross thousands of seabirds fall victim to one fishing technique,
Diomedea exulans being ringed/banded during one 29-year longlining, each year. During longlining operations, thousands
study, only 81 of them were ever recaptured or found away of baited hooks on a line up to 130 km long are dragged
from their nest site. Through the use of increasingly sophis- behind a boat. Seabirds in general and albatrosses in particular,
ticated satellite tracking technology we are beginning to attempt to take this bait, are hooked, and drown. Mitigation
uncover the migratory and dispersive strategies and feed- strategies have been put in place around South Georgia,
ing behaviours of individuals and of populations of birds. including a partial closure of the Patagonian toothfish
Members of the British Antarctic Survey have, for example, Dissostichus eleginoides longline fishery and as a result
recently determined that in the case of adult Grey-headed albatross bycatch in the area has been reduced to a minimal
Albatrosses Thalassarche chrystostoma (Figure 3.1), three level. However, recent surveys of the South Georgia albatross
discrete movement strategies seem to be apparent. Some population carried out by Sally Poncet and her colleagues
birds stay in their breeding range in the South Atlantic on have reported that between 2004 and 2015 populations of
and around South Georgia. Others make regular return
migrations from here to a specific area of the southwest continued
Box 3.1 Continued
Figure 3.1 Grey-headed Albatross (© Ian Robinson).
Wandering and Grey-headed Albatross have declined by of longline fisheries and to improve the conservation sta-
18 per cent and 43 per cent respectively. tus of the birds concerned. In light of estimates that
The Grey-headed Albatross migration study suggests that between a third and a half of all longlining is being carried
for this species at least, only birds staging in the southwest out by illegal pirate fishing boats, with no specific national
Indian Ocean are likely to come into direct contact with allegiance, the pressure for change must be maintained lest
intensive longlining and so perhaps it is in this area that the albatross become a weight around our collective neck.
mitigation efforts should be concentrated. The good news is
that some mitigation is possible: by minimizing discards References
from fishing boats so that birds are not attracted to the Croxall, J.P. (2008) The role of science and advocacy in the
area, by setting the lines at night when most seabirds are conservation of Southern Ocean albatrosses at sea. Bird
not foraging, or by weighting the lines to sink the bait Conservation International 18, 13–29.
below the birds’ reach, it is possible to minimize the Croxall, J.P., Silk, J.R.D., Phillips, R.A., et al. (2005) Global
impact that longlining has. Of course this will only happen circumnavigations: Tracking year-round ranges of non-
if boat owners accept and implement these mitigation breeding albatrosses. Science 307, 249–250.
methods. Towards this end the governments of 13 coun- Poncet, S., Wolfaardt, A.C., Black, A., et al. (2017) Recent
tries have already become signatories to The Agreement trends in numbers of wandering (Diomedea exulans),
for the Conservation of Albatrosses and Petrels (ACAP). In black-browed (Thalassarche melanophris) and grey-
doing so they have agreed to take specific measures to headed (T. chrysostoma) albatrosses breeding at South
ensure that their national fishing fleets reduce the impact Georgia. Polar Biology 40, 1347–58.
raised vital funds towards the ‘Save the Albatross bird, the Swift Parrot Lathamus discolour also under-
Campaign’ administered by BirdLife International, takes an annual migration. This species breeds in
and the race itself brought to the attention of the western Tasmania and feeds largely on the blossom
public the plight of Albatrosses and of seabirds in and nectar of the seasonal flowers of Eucalyptus spe-
general (see Box 3.1). cies. As the breeding season draws to a close, the
Not all bird migrations are of the globe-trotting flowers become less common and the birds range
scale of the albatrosses. Another Tasmanian-breeding into eastern Tasmania before making a migration
northwards across the 300 km Bass Strait into south- this way—should we think of a temperate migrant
ern Australia. Throughout the southern winter the such at the Sedge Warbler Acrocephalus schoenobae-
parrots range across southern Australia in search of nus or the Yellow Warbler Dendroica petechina as a
food before re-crossing the straits in time to breed temperate bird that tolerates the heat and humidity
the following year. of the tropics to avoid the northern winter? Or, as a
tropical bird that takes advantage of the extended
foraging permitted by the longer temperate days?
Concept Whatever the reasons for migration, however, one
The Red List
thing is clear, migration must ‘pay’ because if it did
Since 1964 the International Union for the
not birds would not do it. Migration is costly in
Conservation of Nature (IUCN) has maintained a list
energy terms and in terms of risk, many species pass
of endangered species. This Red List, as it is known,
through geographical bottlenecks as they migrate
provides the public and policy-makers with an annual
assessment of the risk of extinction of thousands and at these times they are particularly vulnerable to
of species. Risk is categorized at several levels taking predators including man (it has been estimated that
into account population size, population trends, and only 60 per cent of the wildfowl that migrate south
geographical distribution. through the USA in fall each year return to breed
the following spring). At least one species of bird of
prey, Eleonora’s Falcon Falco eleanorae, takes advan-
3.1 The ecology of migration tage of the seasonal glut of migrating prey by timing
Why do birds migrate? In the northern hemisphere its breeding to coincide with the autumn passage
we tend to think of migrating birds leaving our of passerine migrants out of Europe across the
shores to winter in a place that offers a more benign Mediterranean Sea into North Africa. Equally how-
climate and guaranteed food resources. Similarly ever, if migration does pay why do some species
we think of the birds that winter with us as doing so stay put? Well for each species a balance is probably
to avoid even more harsh conditions at their breed- struck and we can go some way to understanding
ing sites. So we could argue that birds migrate to this balance if we compare key aspects of the life his-
avoid cold weather. We should remember however tories of generalized tropical residents, temperate
that not all migrations are a response to colder win- residents, and migrants (Table 3.1).
ter conditions. In the tropics many species migrate
in response to the seasonal patterns of rainfall and Key reference
drought. But in the case of both tropical and tem- Ketterson, E.D. and Nolan, V. Jr. (1983) The evolution
perate bird species it would appear that migration of differential bird migration. Current Ornithology 1,
is at least in part an evolutionary response to pre- 357–402.
dictable climate variability. Migration must there-
fore also be in part a response to seasonal variations In their study of the Dark-eyed Junco Junco hyemalis,
in food resources that accompany these climate Ketterson and Nolan have compared the migration
fluctuations. But it has also been suggested that behaviour of males and females. They have shown
migrations may have evolved in response to sea- that each sex responds in a slightly different way to
sonal changes in the inter- and/or intraspecific the selective pressures acting during migration,
dominance relationships between birds—the idea
being that at some times of the year the level of
Table 3.1 Comparison of key life history traits of generalized
competition faced by some birds is such that they migrant and resident species
migrate to lessen it. You may notice that my lan-
guage in the preceding paragraph has been quite Trait Temperate Migrant Tropical
negative, but perhaps we shouldn’t see migration resident resident
just as a drastic measure taken to avoid hardship. Productivity High Moderate Low
We could equally well think of it as a strategy
Adult survival Low Moderate High
adopted by birds to allow them to take advantage
Juvenile survival Low Moderate Moderate/High
of a seasonally available opportunity. Think of it
with the results that this species exhibits a differ-

ential migration. Dark-eyed Juncos breed through- Opaque
out the northern USA and Canada and populations Circular Screen
winter throughout the USA and in southern
Canada. But within a population the sexes migrate
different distances. Females migrate further south Wire Screen Top
than males. In this case a longer migration is an
advantage, females have a higher rate of over-winter Blotting-paper
Funnel
survival than males. If migrating a little further 2-Quart
south is such an advantage, why do males risk Pan
dying by travelling less far? Why don’t they over- Rubber
winter in the same place as the females? The answer Tubing
Ink pad
to this question relates to the fact that for males a
second selective pressure exerts a significant influ- Figure 3.2 A migratory bird held in a funnel cage. The bird’s
ence. Birds that undertake a shorter migration, and footprints on the side of the funnel indicate its motivation to migrate
survive the winter, have less far to return to their and preferred direction of flight. From Able, K.P. (2004) Birds on the
summer breeding grounds. Once there, a strong cor- move: Flight and Migration. Illustration by Robert Gillmor, © Cornell
Lab of Ornithology. In Handbook of Bird Biology. Podulka, S.,
relation exists between early arrival on territory
Rohrbaugh, R.W. Jr, and Bonney, R. (eds) The Cornell Lab of
and increased productivity. Simply put, the first Ornithology, Ithaca.
birds back get the best spots and raise the most
young. So there is an advantage to male juncos in
not flying too far south that outweighs the risk of when the bird becomes restless, it will flutter against
dying during the winter. the sloping sides of the funnel. Evidence of this
activity is recorded on the funnel wall by the inky
Concept footprints left by the bird. From this relatively sim-
Migration strategies ple arrangement two important pieces of informa-
Migrating birds adopt a number of migration strategies. tion can be gained: the number of footprints equates
Some species make single, long haul flights, others a to the level of restlessness of the bird, or the strength
series of short hops, refuelling en route. Some species
of its drive to migrate, and their position on the fun-
are funnelled through migration bottlenecks and others
nel wall indicates the direction in which the bird
migrate across a broad front. The males and females of
was driven to fly.
some species migrate separately, or migrate to different
destinations (often referred to as differential migration).
Different breeding populations of a species often use Key reference
different wintering areas and may leap-frog over one Schwabl, H. (1983) Ausprägung und bedetung des teil-
another to reach them. zugverhaltens einer südwestdeutschen population der
amsel Turdus merula. Journal of Ornithology 124, 101–6.
3.2 Genes and migration

As a result of observations made of birds in funnel
During the migratory period passerine birds exhibit cages, and of the migratory behaviours of wild
a behavioural change. At night they become rest- birds, it is well established that individuals of a spe-
less. This migratory restlessness offers researchers a cies can differ from one another in terms of their
means by which levels of motivation to migrate migratory behaviour. From these observations it has
might be measured and compared. been assumed that there is a genetic component to
Captive birds can be housed, singly, in funnel the control of migration. For example when Schwabl
cages such as that shown in Figure 3.2. The floor of tested in funnel cages the offspring of blackbirds
the cage is an inkpad, the roof of the cage is a wire Turdus merula from German populations known to
screen through which the bird has sight of the night be migratory or resident, the offspring of migrants
sky. A non-migrating bird will be inactive at night demonstrated migratory restlessness but those of
and will stand on the pad. But during migration, residents did not. Presumably these birds had
inherited their migratory tendencies from their atricapilla, an old world warbler found throughout
parents. Before we look in more detail at the link Europe and on several North Atlantic islands (the
between genes and migration, it is important how- Azores, Madeira, the Canary Islands, and the Cape
ever to recognize the role that environment may also Verde Islands). Peter Berthold and colleagues have
play. In Britain, the Herring Gull Larus argentatus is a carried out extensive field and laboratory studies of
sedentary species, while the closely related, Lesser this bird, and no discussion of the genetics of migra-
Black-backed Gull Larus fuscus, is migratory. When tion could be complete without consideration of
Harris cross-fostered the young of these species (i.e. their work.
placed young fuscus in argentatus nests and vice Blackcaps demonstrate a range of migratory
versa) he found that the young Lesser Black-backed behaviours. Populations in northern and eastern
Gulls raised by Herring Gulls migrated normally— Europe are migrants, most of them spending the
presumably having inherited their migratory northern winter months around the Mediterranean
behaviour from their genetic parents. However, or in North Africa. Those of southwest Europe,
Herring Gulls raised by Lesser Black-backed Gulls the Azores, the Canaries, and Madeira are partial
also migrated, although not as far as their foster par- migrants (some migrate but others remain on their
ents. These birds had not inherited a migratory breeding territories all year round). Populations
behaviour pattern and so must have been respond- of birds found on the Cape Verde Islands are
ing to an external environmental cue—possibly the wholly resident and never migrate. Berthold and
movement of their foster parents. This demonstrates co-workers have compared migratory restlessness
that whilst genes are clearly important, environmen- levels of birds from these populations and, as would
tal factors do have a part to play. be expected, have found that birds from Germany
(migrants) have higher levels of restlessness than
Key reference partial migrants from the Canary Islands (Figure 3.3).
Harris, M.P. (1970) Abnormal migration and hybridisa- When hybrids are formed between these two popu-
tion of Larus argentatus and L. fuscus after inter spe- lations the resultant offspring show an intermediate
cies fostering experiments. Ibis 112, 488–98. level of restlessness, demonstrating that there is a
genetic basis for their migratory behaviour.
The most thoroughly investigated case of the role of Other work carried out by Berthold and his team
genes in bird migration is that of the Blackcap Sylvia has demonstrated the genetic basis for migratory
10
Number of Thirty-Minute Periods per Night with
Southern Germany Population

Obligate Migrants
8
Migratory Restlessness
6 S. Germany × Canary
Islands Hybrids
2
Canary Islands Population
Partial Migrants
0
0 50 100 150
Number of Days After Migratory Restlessness Began
Figure 3.3 Comparison of differing levels of migratory restlessness exhibited by German and Canary Island Blackcaps and exhibited by hybrids
between them. From Berthold, P. and Querner, V. (1981) Genetic basis of migratory behaviour in European warblers. Science 212, 77–9, reprinted
with permission from AAAS.
orientation—the compass bearing followed by selected against, and is not expressed in natural
actively migrating birds. Blackcaps breeding in cen- populations.
tral Europe and migrating to Africa could fly due We are used perhaps to thinking about natural
south and perhaps by doing so minimize their selection as an evolutionary force that has its effect
migratory distance. But if they did, they would also over long, perhaps very long, periods of time.
maximize the time that they spent airborne over the However, from experiments with captive birds it is
Mediterranean Sea. This sea passage would be clear that the results of selective pressures can be
arduous indeed and few birds would survive it seen remarkably quickly. In fact Berthold has shown
without significant physiological cost. Instead, east- experimentally that in just three generations of selec-
ern birds migrate initially in a south-eastern direction for migration a captive population of partially
tion, following a route around the eastern edge of migrant Blackcaps can become completely migra-
the Mediterranean and into north-east Africa. Birds tory, and in just six generations members of the same
from the west, on the other hand, set off in a south- population could all be made to behave as residents.
westerly direction and make the crossing into Africa Presumably this is exactly what has happened to the
via the narrow Straits of Gibraltar. Berthold found resident Blackcaps of the Cape Verde Islands, and
that hybrids between members of these two popu- to the now-resident populations of the typically
lations demonstrate a mixed strategy (Figure 3.4), migratory Dark-eyed Junco found on the island of
some flying south-east and some south-west, but Guadalupe 250 km off the Californian coast. The loss
some flying due south. From these observations we of migratory behaviour is a common phenomenon
can deduce that the potential for an initially south- amongst species that have colonized remote islands.
bound migration has been present in Blackcaps
from central Europe, but that it has been strongly Flight path: changing environmental pressures can
result in rapid evolutionary change. page 11.
N The Blackcap does offer us another example of the

evolutionary flexibility of migratory behaviour. The
British breeding population is a migratory one
which spends the winter months in southern Spain
and North Africa, but in the closing decades of the
twentieth century bird watchers in Britain started to
record Blackcaps during the winter months. It was
W E assumed that this was because the British climate
had warmed and people had begun to maintain
gardens more suited to the needs of over-wintering
birds. The British public were also providing food
for birds in increasing amounts (by 2000 some 60
Austrian per cent of UK households were feeding wild birds
SW German
birds
birds in winter). Initially it was thought that these winter
S
birds were members of the British breeding popula-
Hybrids tion that had chosen for whatever reason not to
migrate. However, as the winter Blackcap popula-
Figure 3.4 Directions of migration of Austrian Blackcaps (inner
circle, white triangles), south-west German Blackcaps (inner circle, tion grew, evidence initially from ringing recoveries
shaded triangles), and of hybrids between them (outer circle, shaded and latterly from stable isotope analyses (see Box 3.2
triangles). From Scott, G.W. (2005) Essential Animal Behavior. for an explanation of this technique), and from the
Blackwell Science, Cambridge. Adapted with permission of Springer, tracking of individual birds using geo-locators, has
from Helbig, A.J. (1991) Inheritance of migratory direction in a bird
revealed that they are migrants. In fact they are mem-
species: a cross breeding experiment with SE- and SW- migrating
Blackcaps (Sylvia atricapilla). Behavioural Ecology and Sociobiology, bers of a population of birds breeding in north-west
42, 9–12. Europe (Belgium, the Netherlands, and Germany)
Box 3.2 Stable isotopes and genetic variation as tools to unravel migration
Ringing studies allow us to pin-point exactly where birds go. But does the theory work? Well the answer to this ques-
But they depend upon our ability to capture a bird at one tion is yes it would appear that it does. As an example con-
location and then recapture it at a later date and in another sider the work of Chamberlain and co-workers. They have
place (perhaps thousands of kilometres away). Recapture collected feather samples from Willow Warblers Phylloscopus
rates are very low for the majority of migratory species, per- trochilus of two recently diverged (in evolutionary terms),
haps as few as one in a hundred thousand ringed passerines but discrete sub-species P. trochilus trochilus and P. trochilus
will be re-trapped in this way. Therefore the detailed infor- acredula. Willow Warblers (Figure 3.5) are common through-
mation that we have about the breeding and wintering loca- out Europe, but the birds that they studied come from an
tions of specific populations of birds, and of the staging interesting Swedish population where the ranges of the two
posts that they habitually visit during migration has until sub-species come into contact. Acredula breed in the north
recently been quite limited. As technology has developed, a of the country, trochilius breed in the south, and the breed-
range of methods which enable the tracking of individual ing ranges of the birds overlap slightly at 62°N latitude.
birds are providing us with fascinating insights into large Limited evidence from ringing recoveries suggests that the
scale migratory movements and small scale daily habitat populations of the two sub-species winter in different areas
use. Unfortunately the current costs involved and the limita- of sub-Saharan Africa (see Figure 3.6). If this is the case, one
tions of the equipment (size and power principally) means might expect tissues produced during the winter to vary in
that even this technology fails to fill as many of the gaps in terms of their isotope ratios in a way that would reflect vari-
our knowledge as we might like. ation in the environmental isotope ratios in these different
Chemistry however, may provide us with an answer to at regions. Willow Warblers undergo a complete moult during
least some of the questions that we have. You may recall the winter and when feathers from birds that had returned
that chemical elements such as carbon (C) each have a spe- to Sweden after migration were analysed, it was found that
cific atomic number, which equates to the number of protons the makeup of the feathers of the two different sub-species
found in the nucleus of one atom of that element—so car- varied significantly in terms of their carbon and nitrogen
bon for example has 12 protons and the atomic number 12. isotopes. What is more, the researchers found a sharp
But whilst the number of protons in a carbon atom is con- change in their data in samples collected on either side of
stant, the number of neutrons is not. So carbon can exist in
various forms or isotopes. Examples are carbon-12 (C12),
carbon-13 (C13), and carbon-14 (C14). Atoms of these iso-
topes all have 12 protons, but a C12 atom has 12 neutrons,
C13 has 13, and C14 14. During photosynthesis, plants fix
atmospheric carbon and the ratio of C12 to C13 that is fixed in
this way can be characteristic of particular vegetation com-
munities. This particular ratio can be detected in the carbon
containing tissues of birds that have grown while they were
feeding on plants, or on animals that had fed on plants, in an
area dominated by that vegetation community type. So if we
trap a bird in one area of known C12:C13 ratio and find that
its feathers exhibit a different ratio we can be sure that it
grew them elsewhere. In fact the distributions of these
plants results in the existence of a latitudinal gradient of the
isotope C13. A latitudinal gradient of the hydrogen isotope
deuterium also exists (related to a latitudinal gradient in
annual rainfall), and gradients or variations in the isotopes
of other elements also exist. By comparing information from
the isotopes of a range of elements in bird tissues with those Figure 3.5 Willow Warbler Phylloscopus trochilus trochilus
from the environments through which a bird might have (© Ian Robinson).
travelled, we might be able to pin-point the areas that a bird
has actually visited more precisely. continued
Box 3.2 Continued
the 62°N line of demarcation between the breeding popula- rather it correlates with differences in breeding altitude and
tions. The evidence of the chemistry therefore supports the latitude and involves a gene (RYR2 ) known to be involved in
evidence of ringing studies and the technique could be heart muscle activity and to be under selection in high alti-
important in making the links between far distant habitats tude species. The variations in chromosomes 1 and 5 do cor-
that are essential to specific populations of migrating birds. relate with migratory strategy and involve genes that are
Max Lundberg and his colleagues have used whole- known to be involved in metabolic processes. The authors
genome sequencing to compare the genetic profiles of speculate that this genetic variation may be related to differ-
P. trochilus trochilus and P. trochilus acredula and correlated ent adaptations for fuel use associated with the different
the differences that they have found with the migratory migratory strategies of the two sub-species.
phenotypes of the two sub-species. Their analysis has
revealed that although their genotypes are almost the same Reference
(which we would expect given their close evolutionary rela- Lundberg, M., Liedvogel, M., Larson, K., et al. (2017) Genetic
tionship and recent divergence) they differ in three key areas differences between willow warbler migratory pheno-
of chromosomes 1, 2, and 5. The variation found in chromo- types are few and cluster in large haplotype blocks.
some 3 does not seem to be related to migratory strategy, Evolution Letters 1(3), 155–68.
Figure 3.6 The distribution of Swedish breeding

populations of P.t. trochilus (dotted pattern) and P t.
acredula (striped pattern) and the contact zone between
them (black area). Arrows indicate the presumed migratory
route of both sub-species and the sites of recoveries of
ringed birds in Africa are marked. From Chamberlain, C.P.,
Bensch, S., Feng, X., et al. (2000) Stable isotopes examined
trochilus across a migratory divide in Scandinavian willow warblers
acredula (P. trochilus trochilus and P. trochilus acredula) reflect their
African winter quarters. Proceedings of the Royal Society B:
Biological Sciences 267, 43–9.
that was previously assumed to migrate south-west north-east. Before the conditions changed, any
to winter around the western Mediterranean. We central European birds that migrated to Britain
now know that in fact the Blackcap population of would not have survived the winter months. As
north-west Europe exhibits at least two migratory conditions became more favourable though, birds
strategies, and whilst the majority of birds do that migrated to Britain and survived were at an
migrate south-west, an increasing number migrate advantage compared with those that wintered
further south because their return trip was a shorter via a series of shorter hops with periods of refuelling
one and so they tend to arrive back on the breeding along the way. The migration facilitating behav-
grounds first. As a result these birds have access to iours (and life-cycle consequences) of these differ-
the best territories and have better breeding success. ent migratory strategies have a significant impact
They also tend to mate assortatively (pairs of upon individuals and populations.
birds tend to migrate to the same area) and there is
evidence that the north-west and south-east Concept
Hyperphagia
migrating populations are differentiating genetic-
ally and morphologically. Because the offspring of Birds that are about to undertake an endurance flight
these birds share their parents migratory orientation as part of their migration, or have just completed
such a flight, typically exhibit a heightened motivation
(remember there is a genetic component to this
to feed. This ‘over eating’ is termed hyperphagia, a
novel migratory behaviour), the population will
behaviour that is often also associated with a dietary
continue to increase unless conditions in Britain switch as birds increase the rate at which they store fat,
change again and birds are no longer able to survive the main fuel for migration.
the winter months.
Key references
3.3.1 Seasonality and coordination of migration
Bearhop, S., Fiedler, W., Furness, R.W., et al. (2005)
Assortative mating as a mechanism for rapid evolution In my hometown in northern England the autumn
of a migratory divide. Science 310, 502–4. migration is heralded by the sudden departure of
Heimer, D., Salewski, V., Fiedler, W., et al. (2018) First the Swifts Apus apus. One day flocks of screaming
tracks of individual Blackcaps suggest a complex migra-
swifts can be seen chasing one another up and
tion pattern. Journal of Ornithology 159(1), 205–10.
Rolshausen, G., Segelbacher, G., Hobson, K.A., and
down our streets and then seemingly all at once
Schaefer, H.M. (2009) Contemporary evolution of repro- they are gone. The conditions for their epic flight to
ductive isolation and phenotypic divergence in sympatry southern Africa are right and in one coordinated
along a migratory divide. Current Biology 19, 2097–101. movement they leave. Synchronized autumnal
migration is a commonly observed phenomenon,
and one that requires some explanation given that
3.3 Physiology and migration
other life-cycle milestones are less synchronous for
Whilst it is certain that there is a genetic component some species. For example some young Yellow-
to the control of migration, it is important to remem- green Vireos Vireo flavoviridis are hatched early in
ber that genes operate in environments; using the the breeding season while others are hatched some
word environment here in its traditional ecological weeks later and yet, as a population, they typically
sense and also in the sense that the expression of the embark upon their autumn migration at roughly
gene or the activity of its protein product will be the same time. Prior to migration all young vireos
effected by the internal or physiological environ- must fledge (leave the nest), undergo a partial
ment of the body, and the social environment of the moult, and store the fat that they will need to fuel
bird concerned. The control of migration must their migratory journey. From the research of John
therefore integrate behaviours conducted over a Styrsky and his colleagues it seems that individual
range of timescales and a range of strategies. In vireos vary the relative timing of each of these steps
terms of timing, the onset of migration needs to be according to their hatch date. Under experimental
managed at the seasonal/annual scale and on a conditions they found that whilst the earlier hatched
day-to-day basis during the migration period itself. birds might take as many as 145 days before they
For example, usually diurnal species often need to begin their post-juvenile moult, the latest hatched
switch their behaviour patterns to become mobile at birds (hatched as many as seven weeks later) begin
night; and before/after migratory flights birds often their moult after just 70 days. This of course results
exhibit a shift in diet or hyperphagia. Some migrants in the birds being relatively synchronous in the tim-
undertake a single long haul flight, others migrate ing of their moult (and it turns out in the deposition
of fat and the initiation of migratory restlessness). and the onset of migration and there is some evi-
The birds involved in this experiment had all been dence that the seasonality of migration is linked to
collected from the wild when just a few days (six to the production by the adipose tissue of hormones
eight) old and then raised in standard conditions. So such as adiponectin and visfatin. Testosterone has
whatever it was that triggered the accelerated devel- been implicated in the onset of pre-migratory fuel-
opment of the late birds must have had its effect dur- ling and restlessness, and at the smaller scale
ing those first few days of life. It seems likely that the levels of the hormone melatonin have been impli-
birds even at this early stage were sensitive to photo- cated in the timing of nocturnal migratory activity.
period and took their developmental cue from the But currently the hormone that is most studied
day length that they experienced immediately after and therefore perhaps best understood in the con-
hatching—a phenomenon described as a calendar text of the control of migration is the glucocortic-
effect. Remarkably in this study day lengths across oid corticosterone. In their studies of migrating
the hatching period varied by just 33 minutes. European Robins Erithacus rubeclua and Pied
Flycatchers Ficedula hypoleuca, Karen Falsone and
Key references her colleagues found that baseline corticosterone
Falsone, K., Jenni-Eiermann, S., and Jenni, L. (2009) Cor- levels in birds that were captured during their
ticosterone in migrating songbirds during endurance natural migratory flight were higher than those of
flight. Hormones and Behaviour 56, 548–56. birds that were resting. They suggest that the hor-
Styrsky, J., Berthold, P., and Robinson, M.D. (2004) mone has a role to play in the management of
Endogenous control of migration and calendar effects
energy supply during endurance flying, and in
in an intratropical migrant, the yellow-green vireo.
particular in the regulation of use during migra-
Animal Behaviour 67, 1141–9.
tion. This is because when fat reserves are
exhausted corticosterone levels increase, facilitat-
3.3.2 Hormones and the control of migration ing a shift to protein metabolism and subsequently
It is highly likely that hormones are key to the con- a shift to landing behaviour and feeding (refuel-
trol of life-cycle steps such as the timing of moult ling) as is discussed in Box 3.3.
Box 3.3 Putting on fat for migration
To elucidate the role of corticosterone in the control of pre- Wheatear Oenanthe oenanthe at a shared stop-over site;
migratory fattening and the onset of migratory flights, Cas the North Sea island of Helgoland off the coast of Germany.
Eikenaar and colleagues compared the hormone levels and In spring birds of the sub-species O.o. oenanthe (Figure 3.7)
migratory behaviours of two sub-species of Northern which breeds in northern Europe have a relatively short
Figure 3.7 Northern Wheatear Oenanthe

oenanthe oenanthe breaking its migration for
just a few hours on the English Yorkshire coast
(© Will Scott).
onwards journey to their breeding grounds or next stop-over test the hypothesis that rather than promoting refuelling,
(a sea crossing of 50–250 km); but O.o. leucorhoa, which levels of corticosterone are important in triggering the shift
breeds in Iceland, Greenland, the Faroe Islands, and Canada in behaviour from refuelling to migratory flight.
has a far longer journey to make (a sea crossing of 1,000– Their results supported their hypothesis (Figure 3.8). They
2,500 km). The researchers hypothesized that if cortico- also found that hormone levels were positively correlated
sterone promotes refuelling, leucorhoa should have higher with the date in the migration season and the occurrence of
levels than oenanthe, and that the rate at which birds feed winds that are conducive to migration, both of which are of
(store fat) should be positively correlated with hormone course also positively correlated with the motivation of a
levels. They found however that although leucorhoa do put bird to migrate. It would appear therefore that in this species
on more weight at a faster rate than oenanthe, they in fact at least corticosterone is involved in the control of shift from
had lower levels of corticosterone and that their rate of fat pre-migratory feeding to migratory flight.
deposition was negatively related with hormone levels. So in
this species at least it would appear that corticosterone does Reference
not promote refuelling. Eikenaar, C., Fritzsch, A., and Bairlein, F. (2013) Corticosterone
So what does it do? In a second experiment Eikenaar and and migratory fuelling in Northern wheatears facing
co-workers studied Wheatears on Helgoland during the autumn different barrier crossings. General and Comparative
migration (without distinguishing the two sub-species) to Endocrinology 186, 181–6.
(A) (B)
350
departure time (min after sunset)
12
300
corticost erone (ng ml–1)
10
250
8 200
6 150
4 100
50
0
0
1 2 3 4 5 6 7 8 9 10 11 12
departing staying Cortieosterone (ng ml–1)
Figure 3.8 Wheatear with higher levels of corticosterone are more likely to initiate their migratory flight than those with lower levels (A);
and corticosterone levels are negatively correlated with departure time after sunset (B). From Eikenaar, C., Müller, F., Leutgeb, C., et al. (2017)
Corticosterone and timing of migratory departure in a songbird. Proceedings of the Royal Society B 284, 1–6.
3.3.3 Fuelling migration stop cannot be made. Shifts from fat to protein
metabolism also take place when birds become
Fat is stored in often extensive reserves across the
dehydrated during migratory flights because pro-
body of a bird, but principally under the skin, in the
tein releases around six times as much water as fat
muscles, and in the peritoneal cavity. As a fuel fat is
per calorie of energy produced. On average birds
highly efficient, potentially yielding more than
increase their body fat from around 5 per cent of
seven times as much energy as an equivalent mass
their total mass when not migrating to 25–35 per
of protein or carbohydrate. However, stored fat is
cent during migration. These increases in stored fat
not instantly available for energy release and at the
inevitably lead to increased body mass and in the
onset of an endurance flight a limited amount of
extreme case of the Ruby Throated Hummingbird
protein or carbohydrate metabolism is essential.
Archilochus colubris, a doubling of mass from 3 g to 6 g
When fat reserves are depleted a switch back to pro-
is needed if this tiny bird is to successfully make
tein metabolism will be necessary if a refuelling
an 800 km crossing of the open water of the Gulf of
Mexico as part of its annual migratory journey. next. In some species the same sites are used by the
There is of course an upper limit to the extra fat that same individuals year after year. After migration, or
a bird can carry if it is to continue to fly efficiently during a stop-over during migration, birds need to
and birds have adapted to cope with this limitation rapidly restore their reserves but because there may
in a number of ways. Some species strategically bal- be a lag-time before they are able to feed again, they
ance their lean muscle to fat ratio to ensure the opti- often continue to metabolize residual fat reserves
mal mass for long distance flights, and we will look for a short period. Although as Box 3.4 illustrates,
at this in more detail a little later. Other species take modern agricultural practices may be negatively
advantage of the fact that their migratory routes impacting stop-over feeding behaviour.
pass through sites that are ideal as refuelling sta-
Flight path: Foraging behaviour is flexible and
tions. They store just enough fuel to make the ‘hop’
responds to changing physiological needs. page 125.
from one of these staging posts or stop-overs to the
Box 3.4 Pesticides can hamper migratory refuelling
In the mid 1990s a new family of pesticides appeared on the Even relatively low dosage exposure is known to impact
market. These neonicotinoids were originally thought to be negatively upon condition, survival, and behaviour, and
less likely to harm vertebrates because their ability to bind to recently Margaret Eng and her colleagues have demon-
vertebrate neuro-receptors was less strong than their ability strated an impact upon bird migration.
to bind to the receptors of the invertebrates they were The researchers captured White-crowned Sparrows
designed to target. Unfortunately scientists are beginning to Zonotrichia leucophyrs (Figure 3.9) during their spring
realize that the indiscriminate nature of the effect of these migration, recorded their weight and the amount of fat that
pesticides is having a devastating impact upon essential pol- they were carrying, and then exposed them to very low sub-
linators like bees, and is having a direct impact upon birds. lethal oral doses of the neonicotinoid imidacloprid. Some
Birds can be exposed to neonicotinoids directly (during birds were exposed to a low dose, some to a higher dose,
spraying) or by ingestion of contaminated soils and seeds. and some to a control substance (sunflower oil). The doses
Figure 3.9 White-crowned Sparrow Zonotrichia leucophyrs (© Peter Dunn).

involved were typical of those that birds might encounter of them resuming their northwards journey very soon after
naturally as they migrated through recently treated agricul- release. Weather permitting, the median time to departure
tural land. The researchers held the birds overnight and then was just 12 hours and all of these birds had departed within
re-weighed them and fitted them with a tracking device four days. Birds that had been exposed to the chemical
before releasing them back into the wild. Comparisons of delayed their departure (low dose median three days, high
the birds’ weights showed that during the first six hours dose four days, with some birds waiting as long as nine days).
after being exposed to the pesticide they lost fat and weight, It is likely that these extended stop-overs are a consequence
and the effect was more pronounced in those birds that of the birds having lower fat stores and a reduced level of
received higher doses (Figure 3.10). They also found that feeding and therefore refuelling after exposure. Although it is
birds that had received the highest doses consumed far less known from laboratory studies that birds exposed to similar
food in captivity than the birds that received no pesticide or doses do make a full recovery, and, from this study that once
a low dose. the birds did set off on their migratory flight, direction and
Monitoring of the birds post-release revealed that the duration was as would be expected, the delay and even short
birds that had not been exposed to the pesticide tended to term loss of condition that these birds suffer is likely to have
spend a shorter period at the migratory stop-over site, most individual fitness and population level effects.
(A) (B)
50
% Change Body Mass
0
% Change Body Fat
25
0
–0.5
–25
Control Low High Control Low High

Treatment Treatment
(C) (D)
4 30
% Change Lean Mass
Food Construption
20
0
10
–0.4
Control Low High Control Low High

Treatment Treatment
Figure 3.10 The effect of the neonicotinoid imidacloprid on migrating White-crowned Sparrows. Compared to control birds, treated birds
lost body mass (A), and fat (B) and had a reduced appetite (D) they also suffered a loss in lean mass (C) although not a statistically
significant one. From Eng, M.L., Stutchbury, B.J.M., and Morrisey, C.A. (2019) A neonicotinoid insecticide reduces fuelling and delays
migration in songbirds. Science 365, 1177–80. Reprinted with permission from AAAS.
3.3.4 Long haul flights long haul migration as their baueri ‘cousins’, but
they do make a 9,000 km migration between
Not all migratory routes allow refuelling. For
breeding grounds on the Russian Taymyr penin-
example, the geographical distribution of sight-
sular and the mudflats of west Africa, and in par-
ings of Bar-tailed Godwits Limosa lapponica of the
ticular those of Mauritania and Guinea Bissau.
race baueri suggested to Robert Gill and colleagues
However, these birds do not make the trip as a
that these birds were likely to make the annual trip
single flight. Instead they divide the journey into
from their New Zealand wintering areas to their
two approximately equal flights each lasting
Alaskan breeding grounds in a series of short
around 60 hours. Between these two flights they
hops, refuelling en route, but that the return trip
spend a month refuelling on the rich mudflats of
was probably completed as a single trans-Pacific
the Dutch Wadden Sea.
flight. Using theoretical models that incorporated
When Landys-Ciannelli and co-workers exam-
information about the known flight metabolism of
ined the bodies of Bar-tailed Godwits at various
godwits and the weather systems prevalent along
points during the refuelling period, they found the
their presumed migration routes, Gill and his col-
amount of fat that the birds carried increased with
leagues proposed that the birds would be capable
time (from around 10 per cent to 30 percent of total
of making this 11,000 km trip without refuelling. In
body mass); exactly what one would expect if, dur-
2007 their proposal was validated when a satellite-
ing refuelling, birds are replacing fat used up on
tagged female godwit made the trip north to
the first leg of the journey and then laying down a
Alaska via China in two ‘hops’, one of 10,200 km
store for use on the second. They also found some
and a second of 5,000 km. It then went on to make
extremely interesting changes in muscle mass sug-
the 11,500 km return trip in just eight days (and
gesting that the birds may be varying the mass that
remember that unlike a seabird, a godwit cannot
they carry in a strategic way. The mass of the mus-
rest at sea).
cles associated with flight varied in line with fat
To achieve these astonishing long haul trips, the
load. Birds had a lower muscle mass when they
birds metabolize a large fat reserve (migrating birds
arrived at the stop-over site than they did when
may carry 41 per cent of their mass as fat), and have
they left—so we can assume that some flight muscle
evolved a migratory strategy that takes advantage of
is lost during flight and presumably birds build up
the fact that the dominant atmospheric pressure sys-
their flight machinery so as to be as prepared as
tems across the Pacific during the migration season
possible for the coming journey. Variations were
reliably generate favourable winds. But it is likely that
also found in the mass of the stomach, kidneys,
as in the case of other godwits and other species of
liver, and intestines, i.e. in the organs associated
bird, that some protein metabolism is also necessary—
with digestion. Newly arrived birds arrived with
with the effect that body condition may suffer.
low mass and very quickly gained mass in all of
these components of the digestive system. We
Key references
would expect them to do so given that they are
Gill, R.E. Jr, Piersma, T., Hufferod, G., et al. (2005)
about to engage in a bout of prolonged hyperpha-
Crossing the ultimate ecological barrier: evidence for
gia. But unlike the continuing weight gain observed
an 11,000-km-long non-stop flight from Alaska to New
Zealand and Eastern Australia by bar-tailed godwits. in fat stores and in flight muscles, this weight gain
The Condor 107, 1–20. peaked during the early part of the refuelling
Landys-Ciannelli, M.M., Piersma, T., and Jukeman, J. period—mass remained constant during the mid-
(2003) Strategic size changes of internal organs and dle period, and then as departure neared mass fell
muscle tissue in the bar-tailed godwit during fat storage again as the digestive system atrophied. In this way
on a spring stopover site. Functional Ecology 17, 151–9. the birds seem to manage their ‘baggage-allowance’
they do not carry extra mass associated with a
Bar-tailed Godwits of the race Limosa lapponica redundant function (godwits cannot feed on the
tamyrensis may not undertake as impressive a wing) and must therefore ‘save fuel’.
they have started they pause. To birdwatchers this

Flight path: Birds strategically manage their mass to
is particularly noticeable at migratory bottlenecks
maximize flying efficiency. page 30.
or ahead of major geographical barriers, such as the
Gulf of Mexico. Then, when a window of opportunity
arises and weather conditions are favourable they
3.4 The weather and migration
depart en masse. For a number of years the only
Local weather conditions, and the broad scale insights we had into the effects of weather on migrat-
weather patterns that they predict, have important ing birds came from these large-scale observa-
consequences for migrating birds. The majority of tions of birds at particular locations and often in
them prefer to set off under fine anticyclonic condi- the face of unusual or extreme weather phenomena.
tions with little or no cloud cover and favourable But recent advances in technology have allowed an
tail winds. At night when most passerines and other unprecedented level of insight into the day-to-day
smaller birds are on the move, clear skies make decision-making of individual birds. Raymond
celestial navigation possible. During the day, clear Klaassen and his colleagues have studied the annual
skies enable the development of thermals and oro- migrations of Montagu’s Harriers Circus pygargus
graphic uplift that enable larger soaring birds like migrating to and from their breeding grounds in
raptors and storks to travel huge distances with lit- the Netherlands and their winter quarters in sub-
tle energy expenditure. But as you are no doubt Saharan Africa. These harriers adopt a mixed fly-
aware the weather is not a constant and in the face ing style during migration, using flapping flight
of changing conditions birds must alter their behav- when they have to but taking advantage of ther-
iour to maximize their chances of success. When mals and soaring when they can. Because the birds
birds make the ‘wrong’ decision things can end ter- were fitted with GPS-loggers, Klaassen was able to
ribly as Norman Elkins describes in his excellent record their position several times per hour during
book Weather and Bird Migration. In the book the day and several times each night. For some
Elkins provides an account of an extreme fall (‘fall’ birds data was collected every few seconds which
being the term used to describe a mass grounding provided highly detailed information about flying
of migrating birds) that occurred in south-east behaviour. Their results revealed that the harriers
England on a single day in 1965. High pressure over are a diurnal migrant, resting at night, and that
Scandinavia had created the ideal conditions for they alternate flying and foraging throughout the
the initiation of migration, but as they crossed the day even when crossing the Sahara (suggesting
North Sea the migrating birds encountered a warm that it is a less harsh environment than might have
front associated with a small but intense low pres- been assumed). The importance of weather was
sure system. Encountering cloud, rain, and confirmed because the birds flew for longer and
unfavourable winds, the birds were forced away flew further on days when they benefitted from
from their usual southwards route. Thousands of stronger tailwinds. As might be expected the har-
dead birds were washed up along the English coast, riers were also recorded as resting more on days
presumably their energy reserves had run out as with strong headwinds, presumably they were
they struggled against the wind. Enormous numbers waiting for the wind to change rather than ‘wast-
of birds did make landfall however—one recorder ing’ energy flying into it.
estimated more than 30,000 displaced migrants along
just 4 km of the coastline and half a million along a Key references
40 km stretch. Reports of the day even suggest that Elkins, N. (1983) Weather and Bird Migration. T. &
such was the shortage of trees in some towns that A.D. Poyser, Calton.
birds fluttered onto the shoulders of people! Klaassen, R.H.G., Schlairch, A.E., Bouten, W., and
Koks, B.J. (2017) Migrating Montagu’s harriers fre-
Radar studies have revealed that when the
quently interrupt daily flights in both Europe and Africa.
weather is less than optimal for migration birds
Journal of Avian Biology 48, 180–90.
choose not to set off on their migratory flight, or if
Box 3.5 Impacts of light ‘pollution’ on migration
There are numerous examples of migrating birds being drawn and if necessary mitigate the effect of light pollution on
off course and congregating around artificial light sources migrating birds, they are essential.
such as offshore installations (oil and gas platforms, wind Benjamin Van Doren and his colleagues have taken
farms, and larger passenger ferries for example). Birds are advantage of a unique ‘natural experiment’ to assess directly
often killed when they collide with these structures and may the impact of bright city lights on the behaviour of birds
starve when grounded around them. It is likely that millions of migrating over New York City (Figure 3.11). Their work
migrating birds are killed when they collide with illuminated focused on the impact of the iconic light installation of The
city buildings each year. There is a tendency to assume that National September 11 Memorial and Museum’s Tribute in
this kind of direct impact of artificial light on migrants is con- Light. The Tribute in Light consists of 88 searchlights
fined to nights when the conditions for migration are poor arranged close to the World Trade Centre, together they
because conditions are overcast. I have personal experience of produce two vertical beams of intense light that are visible
grounded birds around a fogbound lighthouse on a Scottish from a distance of some 60 miles. Van Doren combined
island but anecdotal observations can do only so much to weather surveillance radar data together with acoustic and
advance our understanding of this potential problem. visual monitoring of birds to compare the numbers and
The scale of the potential problem has been demon- behaviours of migrant birds in the sky above the Tribute in
strated by James McLaren and his co-workers who have Light on nights during peak migration when the tribute was
used data from weather surveillance radar to show that illuminated and not illuminated. When the searchlights were
birds migrating through northeastern USA are attracted to switched on, the team found that even on nights with a clear
the sky-glow above major urban areas. They have also estab- sky, very large numbers of birds congregated around the
lished that as a result these birds are more likely to make beams, circling and calling, suggesting that they were dis-
migratory stop-overs in sub-optimal habitat which will orientated. Over a period of seven nights across seven years
almost certainly have an impact upon their fitness. Carrying the team estimated that 1.1 million birds were directly
out experimental manipulations of the light levels experi- affected. This result is significant because it is possible that
enced by birds during their migrations is particularly chal- as a result of being attracted to the light and then being
lenging, but if we are to understand the detail of the problem ‘held’ around it (although the team’s data modelling
(A) (B)
Tribute in Light Sept 12, 2015 02:12
New York
off
Tribute
in Light
500 birds
0 km1 km 2 km with 0.5 km
(C) Sept 12, 2015 02:32
New York
Individual
migratory on
Tribute
birds in Light
15,700 birds
0 km1 km 2 km with 0.5 km
Low Number of birds High
Figure 3.11 Migrating birds are attracted to the bright lights of the city. From Van Doren B.M., Horton, K.G., Dokter, A.M., et al. (2017)
High-intensity urban light installation dramatically alters nocturnal bird migration. Proceedings of the National Academy of Science 114(42),
11175–80.
suggests that in this case at least birds possibly moved on mitigate the impact of light sources by managing their use at
after around 30 minutes), birds may be more likely to collide times of peak migration.
with buildings, be more susceptible to predation, become
exhausted, or be required to alter their stop-over behaviour. Reference
When the beams were switched off these birds very quickly McLaren, J.D., Buler, J.J., Schreckengost, T., et al. (2018)
dispersed and their calling rates decreased. This would sug- Artificial light at night confounds broad-scale habitat use
gest that by working with stakeholders it may be possible to by migrating birds. Ecology Letters 21(3), 356–64.
3.5 Navigation eventually regain their ability to home to it, but they
will never learn to home to a new loft. The hip-
We tend to think of migrants as having special sta- pocampal cells are clearly therefore involved in both
tus in terms of their navigational abilities. There is the acquisition and storage/retrieval of spatial infor-
something awe inspiring about the fact that an 8 cm mation (see also Box 3.6).
long passerine can return with pin-point accuracy But is the hippocampus involved in navigation
to its breeding area having first flown across the during migration? There are hippocampal differ-
best part of two continents to get there. But surely ences between migratory and non-migratory bird
the ability of a bird to relocate its nest again and species (some migrants have larger hippocampi,
again during the course of the foraging day, or to some have hippocampi that have more neurons
accurately relocate a cached seed in a complex habi- per unit volume), and differences are apparent
tat is equally amazing. At both scales these move- between species with different migratory strategies.
ments require the individual to navigate. For example Semipalmated Sandpipers Calidris
At the local scale there is evidence that birds pusilla and Spotted Sandpipers Actitis macularia
make use of visual landmarks, a class of navigation have similar numbers of hippocampal neurons, but
involving spatial memory and referred to as pilot- the Spotted Sandpiper has a larger hippocampal
ing. The early evidence for this came from experi- formation and a greater number of hippocampal
ments in which homing pigeons were fitted with microglia. These differences are correlated with
frosted contact lenses prior to being released some differences in migratory behaviour. Semipalmated
distance from their home loft. These birds, by the Sandpipers have a longer migration that crosses
means that we will discuss below, are able to return large expanses of open water whereas the migra-
to the general vicinity of the loft. But being unable tory journey of the Spotted Sandpipers is a shorter
to see it they simply land and wait to be carried in. and a visually more complex land-based route,
Experiments involving a range of vertebrates have leading to a suggestion that the hippocampus has a
shown that specific areas of cells in one region of the role in navigation at both the local and landscape
brain, the hippocampus, are essential to tasks involv- level where landmark recognition and learning are
ing spatial memory. In rats a class of hippocampal important. There is currently however no concrete
cells termed place cells have been shown to become evidence that the hippocampus has an important
active in response to the animals encountering a spe- role in navigation at the larger geographical scale.
cific landmark, or to groups of landmarks that have a
specific relationship to one another and to the spatial
Key reference
position of the test animal. In pigeons hippocampal
Bingman, V.P. and MacDougall-Shackleton, S.A. (2017)
lesions (which destroy these cells) disrupt the ability The avian hippocampus and the hypothetical maps
of the birds to home even short distances over famil- used by navigating migratory birds (with some reflec-
iar ground. Such birds do set off in the right direction tion on compasses and migratory restlessness). Journal
so the hippocampus is not it would appear related to of Comparative Physiology A 203, 465–74.
compass sense, but they get lost en route, presumably
having lost their map sense. If the lesioned birds are Navigation at the larger scale, involving the types
confined to their lofts for a sufficient period they will of orientations and movements characteristic of
Box 3.6 Finding stored food
Important evidence for the key role of the hippocampus in In an attempt to answer this question the researchers have
spatial memory comes from comparative studies of the for- compared the hippocampal volumes of birds of both species.
aging behaviour of passerine birds. The members of some Consider first the data in Figure 3.12, which relates to juven-
passerine species are well known for their ability to hide and ile birds of both species. The data show that when hippocam-
then retrieve seeds. This caching behaviour is obviously to pus size is expressed relative to the size of the telencephalon
the advantage of the birds concerned. Caching allows them (an area of the brain not related to spatial memory and there-
to take advantage of a greater proportion of a food resource fore not expected to vary between these species) bigger
than might be possible without storage. It may also provide brained juvenile Marsh Tits do have a bigger hippocampus,
them with the food they need to live through the lean times, but so do bigger brained juvenile Blue Tits and size for size
but only of course if they can remember where they hid it. there is no difference between them. This might seem to be a
David Sherry has shown experimentally that captive Black- disappointing result, but look at the figure again and this
capped Chickadees Parus atricapillus can do just this. He pro- time pay particular attention to the data collected from adult
vided birds with an opportunity to store sunflower seeds in birds. The hippocampus volume of the adult Blue Tits is no
70 holes drilled into posts in an aviary. When the birds had different to that of either juvenile Blue Tits or juvenile Marsh
cached four or five seeds they were ushered out of the aviary Tits, but that of the adult Marsh Tits is appreciably larger than
and Sherry cleaned it, removed the seeds and then covered all of these. So why is there a difference in adults but not
every one of the holes with an identical Velcro flap before juveniles? It seems that the juvenile marsh tits had not yet
allowing the birds to return. In the wild chickadees are con- had the opportunity to store food whereas the adult birds
stantly on the move, lifting bark, turning leaves, and probing had. In effect the juvenile Marsh Tits were behaving ecologic-
crevices—opening Velcro flaps would be second nature to ally more like a typical Blue Ttit. It would appear therefore
them. So when they got hungry would the birds remember that a larger hippocampus is related to spatial memory, but
where the seeds had been hidden and open the right stores? that hippocampal enlargement is a response to food storing
Yes they did. They spent almost ten times as much time behaviour rather than a prerequisite for it.
exploring the holes in which they had stored seeds compared
Reference
to the sites they had not used. They were also far more likely
to visit a previous cache than an unused site. Taken together Sherry, D.F. (1984) Food storage by black-capped chicka-
these observations strongly suggest that the birds do remem- dees: Memory of the location and contents of caches.
ber where they have hidden food. Further work in the field Animal Behaviour 32, 451–64.
has shown that the birds only use each cache once, put just
one item of food into each cache and can remember where 30
Juvenile marsh tits
they have hidden a seed for almost a month. Juvenile blue tits
Hippocampal volume (mm3 )
The role of the hippocampus in this context has been estab- Adult marsh tits
Adult bule tits
lished via a range of studies but I think that one in particular 20
is worthy of some consideration, providing as it does an excel-
lent example of the comparative approach in biology. Sue
Healy and co-workers have compared the foraging behaviour
and related brain structure of two species of European Parid 10
closely related to the Black-capped Chickadee. Their work
involved the Blue Tit Cyanistes caeruleus and the Marsh Tit
Parus palustris. Marsh Tits, like the chickadee, are avid food
storers. Individual birds are known to store up to 100 seeds in 0
0 100 200 300 400 500
a morning, and across the course of a typical winter will store,
Telencephalon volume (mm3 )
and perhaps more importantly retrieve, literally thousands of
items of food. Blue Tits on the other hand do not store food
Figure 3.12 Adult Marsh Tits who have had experience of food
and given this fundamental difference in the foraging ecol- storing have a more developed hippocampus than do inexperienced
ogies of the two species we might hypothesize that they will juvenile Marsh Tits or adult/juvenile non-storing Blue Tits. From
have different spatial memory abilities and adaptations. Healey, S.D., Clayton, N.S., and Krebs, J.R. (1994) Development of
Specifically Healy and her co-workers have asked the question hippocampal specialisation in two species of tit (Parus spp).
do they have differently developed hippocampi? Behavioural Brain Research 81, 23–8. With permission from Elsevier.
The Hague,
The Netherlands
Natural
wintering area
of Hague
Starlings
Recoveries of
adult Hague
Starlings released in
Switzerland
Switzerland
Recoveries of juvenille
Hague Starlings
released in
Switzerland
Figure 3.13 Recoveries of migrating juvenile (filled circles) and adult (open circles) European Starlings Sturnus vulgaris following their
translocation from the Netherlands to Switzerland. Adult birds compensated for their new start point, juveniles did not. Re-drawn from data in
Perdeck, A.C. (1958) Two types of orientation in migrating Starlings Sturnus vulgaris L. and Chaffinches Fringilla coelebs L., as revealed by
displacement activities. Ardea 46, 1–37.
migrations seem likely to involve two processes: a It seems likely that during their first migration
compass orientation—often termed vector naviga- young birds learn their route and the locations of
tion and, a goal orientation which is often termed their breeding and non-breeding areas with refer-
true navigation. The distinction between these is ence to cues from the environments around them.
possibly best explained by reference to an example, With this acquired information they are then able to
and in this case no discussion of the topic could be develop their mental map and then to use it during
complete without reference to the classic example subsequent journeys. Several cues seem to be
afforded by the work of Perdeck in the 1950s. important and it seems likely that when they are
Perdeck captured more than 10,000 Starlings available they are used in combination.
Sturnus vulgaris, a mixture of adults and juveniles, in
the Netherlands at the onset of the autumn migra-
tion. Typically these birds would have undertaken a 3.5.1 Navigational cues
relatively short south-westerly migration to winter
The sun and the stars
in the southern half of the United Kingdom and
along the northern coasts of Belgium and France. Birds navigate by day and by night and use celestial
The birds were marked so that their movements cues to enable them to do so. By day the sun is the
could be tracked, and then transported almost 400 dominant cue and at night it is replaced by the stars.
miles to the south-east prior to release in Switzerland. That the sun can be used as a navigational cue was
During the following winter around one third of first demonstrated by Kramer in the 1950s. In a
these birds were relocated, having completed their series of influential experiments he first established
migration. But where had they gone? In fact as can the preferred orientation of starlings exhibiting
be seen from Figure 3.13, two types of movement migratory restlessness (through the use of funnel
had taken place. Some of the birds had flown in a cages). He then positioned mirrors around the cages
north-westerly direction towards their traditional in order to shift (from the point of view of the birds)
wintering grounds, a few had even made it there. the position of the sun by 90° and found that the
Others had found novel wintering grounds in south- orientation of the birds changed to compensate for
ern France and on the Iberian peninsula. The birds this. Further experiments have established that
had separated into two discrete populations according the specific cue used is in fact the position of the
to age; the juveniles had headed south-west while sun relative to the horizon, or more precisely the
the adults had flown north-west. Remember that position of an imaginary line from the sun to the
juveniles would not have previously migrated and horizon referred to as the azimuth.
had no experience upon which to draw. Remember Of course the sun is not a stationary body. The
also that earlier in this chapter we saw that the initial azimuth moves during the course of the day and so
migratory orientation is innate. So it would seem birds using it for navigation must use a bi-coordinate
that these birds were able to set off in the right direc- system that takes account of both solar position
tion using a compass sense, but lacking a map sense and time. Clock shifted starlings, that is birds that
they had no way of knowing that they were going to have been conditioned in captivity to be out of
the wrong place. This is an example of vector-based ‘sync’ with natural day time have been used in
navigation. experiments to demonstrate this. If starlings are
The adult birds on the other hand had presum- conditioned so as to be clock shifted by six hours
ably migrated to and from the traditional wintering (so that at noon they ‘think’ that it is in fact 6 am)
area at least once before, and in doing so had estab- they will demonstrate a 90° shift in their orienta-
lished a map sense which allowed them in some tion. By this I mean that when tested against the
way to establish a link between their current loca- natural position of the sun at 6 am they will fly in
tion and their ultimate goal. Translocated to an inappropriate direction for the real time of day.
Switzerland they demonstrated true navigation and Because the azimuth moves by 15° per hour they
were able to undertake a journey across unfamiliar demonstrate the 90° shift and fly in a direction
country to reach a familiar goal. more appropriate to a flight undertaken at noon.
So it would appear that these birds do cross refer- overcast sky. However, there is also considerable
ence the position of the sun and time when direc- evidence that birds make use of a range of other
tion finding. cues to compensate for the ‘loss’ of the sun or the
At night the sun is no longer available and in its stars because birds are able to orientate appropri-
place the stars are used instead. Experiments ately in the absence of a visible sky.
involving funnel cages in a planetarium (so that
the star map experienced by the birds can be The magnetic field
manipulated) have shown that young birds Homing pigeons have no problems finding their
observe the apparent rotation of the pattern of lofts on sunny days when they are made to fly with
stars above them as the earth rotates beneath a bar magnet attached to them, but they lose the
them. In this way they learn the position of the ability to home when carrying the magnet on a
centre of the map, which in the northern hemi- cloudy day. The magnet will cause a localized dis-
sphere is Polaris, the North Star. This means that ruption of the magnetic field experienced by the
once they have learned this they are able to cor- bird and so it seems likely that geomagnetism is
rectly determine north as long as they can see that important in orientation (presumably the pigeons
star and some of those around it. With this infor- are unaffected on sunny days because they are able
mation northern hemisphere migrants can fly to utilize their sun compass).
south (away from the star) in the autumn and The magnetic poles of the earth maintain a pre-
north (towards it) in the spring. But what happens dictable magnetic field across the surface of the
when clouds obscure their view? There is some planet with a south to north orientation. At the
evidence that suggests that birds may choose not poles the field dips towards the surface of the earth
to migrate on cloudy nights. Blackcaps Sylvia atri- at an angle of 90° and at the equator the angle is 0°.
capilla and Red-backed Shrikes Lanius collurio Birds have been shown experimentally to be able
have both been observed to show migratory rest- to detect this field, or more precisely to detect the
lessness on cloudless nights but not under an angle of dip of the field as it varies with latitude.
(A) N (B) N
1
2
4
W E W E
S
Control Days 1, 2, and 4
(C) N (D) N
5 10
8 10+
W E W E
Figure 3.14 Migratory direction preferences of Silvereyes

prior to (control) and following exposure to a strong magnetic
pulse. It is clear that over time the disruptive effect of the
S S pulse wears off. From Scott, G.W. (2005) Essential Animal
Days 5 and 8 Day 10 and later Behavior. Blackwell Scientific, Cambridge.
This should in theory allow them to establish the Erithacus rubecula at least, the magnetic compass sense
directions north and south, and to position them- might be related to up-regulation (increased avail-
selves on the surface of the earth. Current evidence ability) of mRNA coding the protein Cryptochrome
suggests that birds may use the magnetic field in 4 (Cry4) in double-cone cells of the retina. Their
two ways; as a compass to determine direction, and research recorded a significant increase in Cry4 activ-
as the basis of a map. Considering the compass ity during the migration season. Cryptochromes are
first, Wolfgang Wiltschko has shown that a strong light sensitive proteins that form radical pairs, the
magnetic pulse is enough to disrupt the migratory free electrons of which have different but correlated
orientation of Silvereyes Zosterops l. lateralis. As spins as a result of photo-excitation. It seems likely
Figure 3.14 shows these birds usually follow a that through their interaction with the magnetic field
southerly route from their non-breeding range on these radicals enable birds to perceive it in some
the Australian mainland to their Tasmanian breed- way. The magnetic map sense however seems likely
ing grounds. A magnetic pulse disorientates them to be related to an as yet unidentified and undis-
for some days, but the data do suggest that they are covered iron-based receptor located somewhere in
able to either recover from the disruption, or to at the neural architecture of the optical system.
least accommodate its effect after 10 days or so.
Such a disruption may be possible under natural Key references
conditions as a result of a solar storm for example. Günther, A., Einwich, A., Sjulstok, E., et al. (2018) Double-
Ian Henshaw and colleagues have carried out cone localisation and seasonal expression pattern
elegant experiments to investigate the use of a mag- suggest a role in magnetoreception for European Robin
Cryptochrome 4. Current Biology 28(2), 211–23.
netic map by Thrush Nightingale Luscinia luscinia
Henshaw, I., Fransson, T., Jakobsson, S., et al. (2008)
on their migratory route from Sweden to southern
Food intake and fuel deposition in a migratory bird is
Egypt. These birds would typically pause before affected by multiple and single-step changes in the
crossing the Sahara and through hyperphagic magnetic field. The Journal of Experimental Biology
fuelling behaviour significantly increase their 211, 649–53.
body mass prior to the arduous desert crossing. The Heyers, D., Elbers, D., Bulte, M., et al. (2017) The mag-
researchers found that by altering the magnetic netic map sense and its use in fine-tuning the migra-
field parameters experienced by birds to mimic tion programme of birds. Journal of Comparative Phys-
iology A 203(6–7), 491–7.
those experienced during migration they were able
to induce levels of hyperphagia and mass gain typ-
ical of birds about to cross the Sahara in birds that Following your nose
were actually still in Sweden. These results suggest There is something special about the smell of sea-
that the birds were using magnetic field informa- bird guano on a warm summer’s day. I appreciate
tion as a map to determine their location and alter- that it may not be to everyone’s tastes, but it is one
ing their behaviour accordingly. of my favourite smells, and it is an important smell
So how do birds ‘read’ magnetic fields to deter- because research suggests that it helps seabirds to
mine compass direction and map position? Although relocate their colonies and even their individual
the details are not fully elucidated it seems likely that nests. Data have been available for some time that
two discrete mechanisms may be involved. It is suggest that homing pigeons learn the smell around
known that the sites of activity in the brain when their loft and use it, among other cues, to relocate
birds do respond to changes in magnetic fields are in home when they have been displaced by their
the visual system and that they can only be recorded owners for racing purposes. Now Enrica Pollonara
if the retina is intact and operational and if the bird is and her colleagues have carried out experiments on
exposed to particular wavelengths of light (specific- Scopoli’s Shearwaters Calonectris diomedea breeding
ally they appear to need light at the blue end of the on a small island colony off the coast of Italy. The
spectrum). Recent research by Anja Günther and her researchers captured incubating shearwaters (taking
co-workers suggests that in the European Robin care to protect their eggs) and moved them to a release
point some 400 km away (and 100 km offshore). Prior As would be expected all of the control birds
to release, the birds were assigned to one of three were recaptured at the colony, back on their nests,
experimental groups and fitted with a data logger within a few days. Similarly all of the birds that
that enabled the researchers to determine the route had magnets fixed to them were able to find their
they took back to their next when they were eventually way home suggesting that even if the magnetic
recaptured. Some birds were simply tagged, relocated, sense is important in the navigation of this species
and released—these control birds were free to there are other cues that can be used to excellent
behave normally. The other birds were subjected to effect. But compare their quite direct routes
one of two experimental manipulations: some had home with flightpaths of the anosmic birds in
magnets attached to their heads to disrupt their Figure 3.15. Without their sense of smell the birds
ability to use the earth’s magnetic field to navigate seem to be initially ‘lost’—wandering back and
by, and others were rendered anosmic. This means forth around the release site before heading to an
that their ability to smell was temporarily removed adjacent coastline. Then the birds fly back and
(the effect would last for just a few weeks). forth along the coast until eventually something
(A) (B)
(C) (D)
Figure 3.15 The flight lines of Scopoli’s Shearwaters that had been displaced from their colony. Control birds (A) and birds fitted with magnets
to disrupt their ability to read the earth’s magnetic field (B) made relatively direct flights home. In comparison anosmic birds did not (C and D).
From Pollonara, E., Luschi, P., Guilford, T., et al. (2015) Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird:
displacements with shearwaters in the Mediterranean Sea. Scientific Reports 5, Article number 16486, 10.
changes and their flight becomes much more Summary

direct. Still hugging the coast they fly back to the
island and their colony. The researchers interpret Migration allows birds to make the most of the
this as suggesting that without smell the birds resources available to them. It has a genetic com-
cannot find their colony in a featureless sea. Once ponent but is a response to environmental cues.
they find the coast however, they are probably Migrating birds face numerous hazards and conser-
able to use visual landmarks to navigate by and vation of migrants relies upon efforts made in a
although the route may be circuitous they do number of countries. Birds use a wide range of
eventually make it home. navigational cues to facilitate their movements and
in some cases have excellent spatial memories.
C H A PT ER 4
Eggs, nests, and chicks
‘The avian egg is a miracle of natural engineering’

Noble S. Proctor and Patrick J. Lynch (1993)
Eggs, particularly perhaps those of domestic fowl, divide at meiosis they produce gametes (sperm)
are something that we are probably all very familiar that have either an X or a Y. Male mammals are there-
with, but just how much do we know about them? fore described as the heterogametic sex. But our
In this chapter I want to consider the egg from its mothers (and other female mammals) are homo-
conception, through laying and incubation to hatch- gametic, i.e. they have a pair of X sex chromosomes
ing; and to think about chicks. and so their gametes are all the same (X). This of
course means that the sex chromosome that we
inherit from our mother will always be an X
Chapter overview
chromosome, but from our father we may inherit
4.1 Sex and the gonads of birds either an X or a Y. If our paternal sex chromosome is
4.2 The egg a Y then we are male, if it’s an X we are female. Birds
4.3 Clutch size too have one heterogametic sex and so sex is deter-
4.4 Egg shell colouration and patterning mined in the same way, but with two notable differ-
4.5 Nests ences. The first is a difference in terminology—instead
4.6 Incubation of X and Y chromosomes birds have W and Z
4.7 Hatching chromosomes. The second difference is perhaps
4.8 Chicks biologically more significant; whereas in mammals
sex is determined by the material inherited from
male parents, in birds it is determined by the material
4.1 Sex and the gonads of birds
coming from the female because it is the female that
Birds reproduce sexually; a male and a female copu- is the heterogametic sex having a ZW pair of sex
late, sperm are transferred, an egg is fertilized chromosomes (males have two Z chromosomes).
(internally) and assuming that all goes well a new Chromosomes consist of a double helix of DNA,
bird is the eventual result. Genetically this new specific sections of which act as templates for the
individual will be a combination of its parents hav- production of proteins. These protein coding sec-
ing inherited half of its genetic material from each tions are what we refer to as genes. Each individual
of them. gene always codes for the same protein or part of a
As humans one of the chromosomes we inherit protein (some are the product of a number of genes
from our father determines our sex. Human sex working together) and so the expression of a par-
chromosomes come in two types, labelled X and ticular gene will always affect the same character of
Y. Our fathers (like all male mammals) have paired the organism’s behaviour, physiology, develop-
sex chromosomes consisting of one X chromosome ment, etc. The observable effects of the expression
and one Y chromosome and when their germ cells of genes are an organism’s phenotype, but we
DOI: 10.1093/oso/9780198804741.003.0004
Ovary
Infundibulum
Magnum
region Ovum and
albumen
Isthmus Ovum and

region shell membranes
Uterus
region
Large intestine
Vestigial right oviduct

Vagina
region
Cloaca
Figure 4.1 The oviduct and the formation of eggs. After its release from the ovary, the egg typically takes 24 hours to develop fully: Spending
around 30 minutes in the upper area of the oviduct (the infundibulum); around 3 hours in the magnum region where it is coated with albumen; an
hour in the isthmus region where shell membranes are deposited; and, spending up to 24 hours in the uterus where the hard outer shell and
associated pigmentation is laid down. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure and Function. Yale
University Press, New Haven.
E G G S, N E S T S, A N D C H I C K S 75
should not think of phenotype (be it behaviours of the female and ejaculates directly into her. In the
observed, physiological characteristics or plumage passerines the male cloaca does swell and protrude
colour) as being solely determined by genotype. during the breeding season and this may serve to
Phenotypes also depend upon the environment in increase the efficiency of sperm transfer. In a similar
which they are expressed, something that we will way some species of duck and members of a small
return to later in this chapter. number of other families develop a penis-like
The genes found on the Z and W chromosomes are protuberance that is involved in copulation.
referred to as being sex-linked. For example, only a After transfer, sperm swim from the area of the
female bird can have any of the genes that are found female cloaca towards the top of the oviduct, to the
solely on the W chromosome, so these genes are infundibulum and ovary, where the mature ovum is
linked to being female. We are only beginning to fertilized (Figure 4.1). In some species females have
understand the specific details of the impact of sex- special storage organs around the junction of the
linked genes upon the development and life of the vagina and uterus where sperm may be retained in a
individual but in chapter 5 we will consider one viable state for some days or even weeks prior to
exciting example of the clear link between a sex- their release which is timed to coincide with ovula-
linked gene and sex specific development, bird song. tion. The significance of this is discussed in chapter 5.
Flight path: Development and control of bird song. Flight path: sperm storage and breeding strategies.
page 105. page 95.
Although the details have yet to be determined, it can

be assumed that the basic genetic difference between 4.2 The egg
male and female birds also in some way determines
In their excellent Manual of Ornithology Nobel
the differentiation of their tissues into gonads that are
Proctor and Patrick Lynch refer to the egg of a bird
either male (testes) or female (ovaries). Males have a
as ‘. . . a miracle of natural engineering. Light
pair of internal testes which produce sperm. These
and strong, it provides everything a developing
are enlarged during the breeding season but shrink
bird embryo needs.’ And this quote does I think
away to almost nothing during the rest of the year.
sum up an egg perfectly.
Females of most bird species have only one devel-
oped ovary (usually the left one), although there are
Key reference
exceptions and the females of some species of bird of
Proctor, N.S. and Lynch, P.J. (1993) Manual of
prey do have two ovaries (although they may not
Ornithology: Avian Structure and Function. Yale
both be functional). As in the case of the male testes, University Press, New Haven.
the female ovary is far larger during the breeding sea-
son than it is during the rest of the year. Presumably Essentially the egg is a zygote, a fertilized ovum,
this seasonal development of gonad tissue is of sitting in a relatively huge store of nutrients and
benefit to birds that have to carefully balance their encased in a protective shell. But as Figure 4.2 illus-
body mass to maximize their flight efficiency. trates, there is rather more to it than that.
Flight path: seasonal modification of tissue mass, Flight path: Yolk volume correlates with chick
flight efficiency, and migration. page 62. developmental strategy. page 96.
Birds on the whole do not possess an external sex At the centre of the egg is the yolk, rich in fats, pro-
organ such as the mammalian penis and copulation teins, and other nutrients. The yolk may comprise as
is usually a very brief affair lasting just seconds, much as 70 per cent of the content of an egg in the
although it can last for 25 minutes in the case of the case of the Brown Kiwi Apteryx australis, or as little
Aquatic Warbler Acrocephalus paludicola. Both males as 20 per cent in the case of small passerines. When
and females have a cloaca, and during copulation we crack open an egg to cook it the yolk appears to
the male places the opening of his cloaca over that be a relatively uniform yellow body but in fact if
Germinal spot
Shell
(blastodisc)
Yellow yolk Outer shell membrane
White yolk
Inner shell membrane
Dense albumen
Chalaza
Air space
Chalaza
Light (thin)
albumen
Figure 4.2 The internal anatomy of a generalized bird’s egg. From Proctor, N.S. and Lynch, P.J. (1993) Manual of Ornithology: Avian Structure
and Function. Yale University Press, New Haven.
prepared properly its real structure can be seen and and acting as a kind of external stomach, allowing
it is revealed as being a series of alternating layers the embryo to absorb nutrients directly from the yolk.
of nutrient-rich yellow and less rich white yolk. Shortly before hatching the yolk sack is absorbed
These layers are built up over a period of days as into the body of the chick and it may serve as a
the yolk is formed and the difference in their colour nutrient reserve to enhance its chances of survival
is an indication of differences in nutrient availabil- during the first few days after leaving the egg.
ity (layers laid down at night are less nutrient-rich). As embryonic development progresses, the chick
So, just as we can age a tree by its growth rings, we absorbs the calcium needed for bone growth from
can determine yolk age (or at least measure the time the shell of the egg, thereby weakening it and pre-
taken for its development) by counting the layers sumably increasing the ease with which the chick
within it. The developing embryo (beginning as a will be able to crack it when the time comes.
group of germ cells termed the blastula) sits on top The second membrane, the chorioallantois, devel-
of the yolk. Specifically it sits on top of a column of ops on the inner surface of the egg shell, eventually
white yolk and because white yolk is less dense covering most of it. This highly vascularized mem-
than yellow yolk this column ensures that as the brane provides for the transport of oxygen into, and
egg rotates, the embryo (and the white yolk under carbon dioxide and excess water vapour out of the
it) floats to retain its position above the yolk mass embryo. These gases enter and leave the chorioal-
rather than underneath it. The yolk is contained lantois and the egg via pores in the outer shell.
within the vitelline membrane to maintain its integ- The yolk is surrounded by the albumen, com-
rity and is held in place by the chalazae, gelatinous monly referred to as the white of the egg because of
albumen structures which allow the aforemen- the transformation that it undergoes on cooking;
tioned yolk rotation but limit its movement other- changing as it does from an almost transparent gel
wise. To facilitate the uptake of nutrients from the to a white solid. If you fry an egg sunny side up
yolk and to permit the exchange of gases with the you will notice that there are two layers of albu-
environment, the developing embryo produces two men, a dense inner layer in contact with the yolk
extra-embryonic membranes. One of these, the yolk and a less dense outer layer. Consisting of around
sack, is a vascularized sheath surrounding the yolk 90 per cent water and 10 per cent protein, the
albumen is the water reserve for the developing Bolund and her colleagues have demonstrated that
chick. The albumen layer also acts as a physical when they are paired with a low quality mate,
cushion, protecting the embryo from sudden jolts female Zebra Finches increase the volume of the
as the egg moves, and as an insulating membrane eggs that they lay and increase the carotenoid con-
reducing the cooling of the yolk and embryo when tent of their yolks. In essence they lay better eggs.
incubation is interrupted. This is presumably an attempt by them to offset the
The outer shell of an avian egg is composed of a poor genetic quality (low attractiveness) of their
number of discrete layers, the most obvious being mate by giving their offspring a bit of a head start.
the hard outer layer of calcium carbonate crystals
arranged in a lattice of flexible collagen fibres. This
gives the shell the strength that it needs to bear 4.3 Clutch size
the weight of an incubating parent, the resilience
Female albatrosses invariably lay a single egg whilst
required as it is jostled against other eggs in the clutch,
the clutch of a Blue Tit Cyanistes caeruleus can have
and against its surroundings (remember that not all
as many as 17 eggs in it. There is clearly therefore
eggs are laid into a comfortable nest, some such as
considerable variability in clutch size. Females of
those of cliff nesting seabirds are laid directly onto
some species are extremely limited in terms of the
unyielding rock). Beneath this outer layer are two
variation in clutch size that they can achieve (e.g.
flexible inner membranes to which the brittle outer
female Spotted Sandpiper Actitis macularis always
layer adheres, further contributing to the overall
lay four eggs, the implications of which are dis-
stability of the shell. The innermost shell membrane
cussed in chapter 5). On the other hand the females
is in direct physical contact with the vascularized
of many species are able to vary the number of eggs
chorioallantoic membrane through which embryonic
that they lay between nesting attempts/seasons. In
respiration takes place. To facilitate the transport of
these cases the question ‘how big should a clutch
gases into and out of the egg, the shell has permanently
be?’ is one that has been a focus of considerable
open pores allowing the inner membranes of the egg to
interest to ornithologists.
communicate directly with the external environment.
General patterns of variation in clutch size have
Most birds lay eggs at the rate of one per day for
been described and interpretation of these does
a fixed period (depending upon clutch size, the
allow the formulation of some apparently straight-
determination of which is discussed later in Box 4.1).
forward explanations for the phenomenon. For
There are of course exceptions—some birds lay
example the clutches, and therefore broods, of altri-
every other day, and as an extreme the Masked
cial species (whose young are highly dependent
Booby Sula dactylatra lays the two eggs in its clutch
upon their parents) tend to be smaller than those of
six or seven days apart. The reason for the inter
precocial species (with young that are quite inde-
egg interval probably relates in part to the time it
pendent). It seems clear that in these cases the abil-
takes for an egg to be produced (see Figure 4.1) and
ity of the parents to feed, brood, and protect the
the need on the part of female birds to maintain
chicks is a key determinant of clutch size. It has also
flying efficiency, carrying one almost fully formed
been noted that species utilizing open nests have
egg is probably a sufficient burden in the context
smaller broods than those with a more secure cavity
of aerodynamics.
nest. Presumably the increased protection from pre-
Key reference
dation afforded by a cavity nest is important, but it
Bolund, E., Schielzeth, H., and Forstmeier, W. (2009)
is also possible that open nest broods are smaller to
Compensatory investment in zebra finches: females enable faster fledging and so minimize predation
lay larger eggs when paired to sexually unattractive by cutting short the risky period during which
males. Proceedings of the Royal Society of London:B chicks are in the nest. There must also be a heritable
276, 707–15. component to clutch size, after all artificial selection
for increasing ‘clutch size’ has allowed humans to
Female birds do it seems have some control over the develop varieties of domestic fowl that are able to
size and quality of the eggs that they lay. Elisabeth lay an egg a day almost all year round.
Early observations of clutch size took the view 5 Initial clutch size laid
that the number of eggs laid by a female should be 8
Number of young fledged

the same as the maximum number of young that 4
could be successfully reared during a breeding
attempt, after all to produce more eggs than this 3
would be a waste of resources, to produce fewer 7
would be a waste of opportunity. Field-based obser- 2
vations suggest that in fact clutches are most often
1 6
slightly smaller than would be expected. This dis-
parity between theoretical and actual clutch size 5
can be explained if, rather than considering a single 4 5 6 7 8
breeding season, the prediction is made that the opti- Experimental brood size
mal clutch size will be the one that allows a female
to maximize her productivity over her lifetime. In Figure 4.3 Experimental manipulation of brood size demonstrates
effect by producing slightly fewer eggs in any one that female Magpies Pica pica consistently lay that number of eggs
that their territory can support. From Högstedt, G. (1980) Evolution of
clutch, females are ensuring that they will have
clutch size in birds: adaptive variation in relation to territory quality.
the reserves/survivorship potential to lay further Science 206, 1148–50. Reprinted with permission from AAAS.
clutches in future.
Goran Högstedt, who noted that the clutches laid
by individual females of the Swedish Black-billed have a capacity to lay varying numbers of eggs dur-
Magpie Pica pica population that he studied, varied ing a single breeding attempt. Initially it was sug-
in size between five and eight eggs, provides evi- gested that clutch size was determined by food
dence for this kind of subtle brood manipulation. To availability (Ashmole’s hypothesis), the idea being that
test the idea that these females somehow ‘knew’ females with access to less food during the breeding
what the optimal number of eggs to lay was, he season would be restricted in the number of eggs
manipulated brood sizes over three breeding sea- that they could lay, or that they would be able to rear
sons. Some broods were not manipulated and these fewer young (or both). Numerous studies have pro-
females were allowed to rear all of the chicks that vided support for this resource availability hypothesis
they hatched. Some females had their brood size demonstrating that increased food availability
reduced, and the newly hatched chicks that were during the breeding season is directly related to
removed from them were used to increase the increased productivity, and/or that seasonal food
broods of others. The data presented in Figure 4.3 shortages during the period prior to breeding results
show that in all cases the optimum clutch size (the in increased adult mortality. Increased adult mortal-
one resulting in the most chicks still alive at the point ity in turn leads to reduced competition during the
of fledging) was the same as that laid by the female. subsequent breeding season and a relative increase
Through further work Högstedt was able to show in available resources enabling larger clutches.
that the main factor determining clutch size was, in However, there are other potential explanations for
this population, territory quality and that at some variation in clutch size. For example, a number of
level females were able to relate territory quality to hypotheses have been proposed suggesting that
clutch size and consistently lay the optimum clutch. variable predation risk (nest, fledging, and adult
Figure 4.3 also highlights some of the consequences predation) can explain variable clutch size. These
of not laying the optimal clutch; lay too many or too predation risk hypotheses suggest that the likelihood of
few eggs and productivity will decline. This story adult or young birds/eggs being predated both
will be returned to in chapter 5 when we consider have an impact upon optimal clutch size. This is
Magpie parenting behaviour. because larger broods require adult birds to visit
A number of hypotheses have been proposed to them more often to provide food to developing
explain the evolution of clutch size in species that chicks and as a result both adults and nests might be
more conspicuous to predators. Therefore, in areas this case they found no direct support for the
of high predation risk, optimal clutch sizes should resource availability hypothesis but it is important to
be smaller to minimize visit rates and thereby min- bear in mind that because these warblers are
imize the chances that adult birds or eggs/nestlings migrants it is possible that resource availability
will be killed and eaten. prior to breeding does have some effect. However,
But how to tease apart the relative importance of the clutches of birds exposed to the caged chip-
these hypotheses? Ornithologists typically adopt munk were on average smaller than those of birds
one of two approaches to a question like this one. that were not subjected to an increased perceived
In some cases they carry out an experiment to test predation risk (and the same size as the clutches of
predictions of the hypotheses in the case of one or birds exposed to the chipmunk and given extra
a small number of study species. Alternatively food). So in this case at least it would appear that
they determine the significance of complimentary the predation risk hypothesis best explains the
or competing hypotheses through an interrogation observed variation in clutch size (Figure 4.4).
of a large comparative data set. An example of the
former is the work undertaken by Kristen Dillon Key references
and Courtney Conway who have conducted an Martin, T.E. (2014) A conceptual framework for
elegant experiment involving a population of Red- clutch-size evolution in songbirds. The American
faced Warblers Cardellina rubifrons inhabiting the Naturalist 183, 313–24.
mountain ranges of Arizona. The researchers Harmáčková, L. and Remeš, V. (2017) The evolution of
observed that across their range the clutches of clutch size in Australian songbirds in relation to
climate, predation and nestling development. Emu
these birds varied from five eggs at lower eleva-
Austral Ornithology 117(4), 333–43.
tions to three or four eggs at higher elevations.
Based upon their knowledge of the species and the
area, they hypothesized that invertebrate food Lenka Harmáck ̌ ová and Vladimír Remeš have
available to the warblers might decrease with alti- adopted a different approach to understanding the
tude but also that levels of predation risk might factors driving the evolution of clutch size. They
increase. So in this case both the resource availability have explored a data set containing life history infor-
hypothesis and the predation risk hypothesis might mation of 313 species of Australian Passeriforme
influence clutch size. songbirds and used it to test a number of hypotheses
To test the relative effects of resource (food) avail- including the resource availability hypothesis and the
ability and perceived predation risk upon clutch linkage between resources, seasonality and latitude,
size, Dillon and Conway designed an experiment and the predation risk hypothesis and an extension of it
that enabled them to manipulate both in a con- (Martin’s hypothesis) that they describe as the fledg-
trolled way and counted the numbers of eggs laid ling development gradient. Martin’s hypothesis sug-
by birds subjected to each experimental condition. gests that whereas increased predator risk should
To vary food availability they simply provided result in smaller clutch sizes (as described previ-
some birds with additional food in the form of trays ously) in those cases where nest predation is highest,
of wax moth larvae placed close to their nests. To vary young birds should fledge early to minimize risk
perceived predation risk a caged Cliff Chipmunk (and as a result will leave the nest at an under devel-
Tamias dorsalis was placed in the territory of some oped state being less heavy and with only part grown
birds for a short period each day. In total four primary feathers). This means that adult birds must
experimental treatments were applied: a control compensate by expending more energy provisioning
condition (no manipulation); increased food avail- mobile, dependent fledglings that are themselves at
ability; increased predation risk; and, increased risk of predation. As a result, the interaction of juven-
food availability plus increased predation risk. ile mortality, level of fledgling development, and
Their results revealed that increased food avail- resource availability determines clutch size. In
ability during breeding did not result in a change in essence species with young that spend longer in the
clutch size compared to the control treatment. So in nest should lay bigger clutches (when adult body
Control Chipmunk Supplemental Food Supp.Food + Chipmunk
Clutch Size
4
10 5 0 10 5 0 10 5 0 10 5 0
Figure 4.4 Female Red-faced Warblers provided with extra food lay clutches that are similar in size to control birds. Birds that have an increased
perception of predator risk lay smaller clutches. Dashed lines indicate average clutch sizes. From Dillon, K.G. and Conway, C.J. (2018) Nest
predation risk explains variation in avian clutch size. Behavioural Ecology 29(2), 301–11, by permission of Oxford University Press.
size is taken into account). From the results of their predation risk hypothesis. However, they did find some
analysis, Harmácková̌ and Remeš conclude that in evidence to support Martin’s hypothesis suggesting
Australia at least, although clutch size does generally that some interaction of local resource availability
increase with latitude (something that has also been and age-specific predation risk may explain the rela-
observed in the northern hemisphere), they did not tive clutch sizes of Australian songbirds, but exactly
find any evidence to support the resource availability what factors exert the most influence on clutch size
hypothesis, nor did they find evidence to support the may vary across the globe.
4.4 Egg shell colouration and patterning 4.4.1 Camouflage

Eggs are quite simply beautiful objects. Their form is As a student I was told that the colour of an egg was
particularly pleasing to the human eye for some rea- an adaptation to facilitate camouflage. This, it was
son, and the diversity of their colours and patterns is explained, was why white eggs were laid by cavity
quite amazing. There are two components to egg nesting birds and why patterned eggs were laid by
shell colour–the base colour (usually white, pale birds that had open nests (with the colour and pat-
brown, or pale blue, but deep reds, blacks, and tern matching the habitat around the nest). There
greens are also found), and the pattern (streaks, spots may be some truth to this in that some eggs are
or blotches in a range of colours that are usually, but camouflaged—personally I have often had great
not always, darker than that of the base). The natural difficulty in locating the nests and greenish/brown
beauty of eggs sparked a frenzy of egg collecting and mottled eggs of Oystercatcher Haematopus ostrala-
their study (oology) during the Victorian period. geus despite their being laid on open ground in
Over the period of their academic study a host of nothing more elaborate than a scrape (Figure 4.5).
explanations as to the significance of their colour and In my local Oystercatcher population the eggs are
pattern have been proposed. These are very well ‘lost’ amongst the gravel mix of the upper shore on
summarized by Underwood and Sealy in their con- which they are laid.
tribution to the monograph Avian Incubation. However, not all eggs that are laid in the open
are camouflaged and not all cavity nesters lay white
Key reference eggs. So whilst this explanation might explain the
Underwood, T.J. and Sealy, S.G. (2002) Adaptive colouration of a proportion of eggs, it is insufficient
significance of egg colouration. In Avian Incubation. as an explanation of the colouration of all eggs. The
Deeming, D.C. (ed.) Oxford University Press, Oxford.
camouflage explanation for egg colour is one of a
Figure 4.5 Although obvious when pointed out, this Oystercatcher nest containing a clutch of three eggs was particularly difficult to locate on
the shore (© Graham Scott).
family of explanations that ascribe a signal function Egg recognition is also important in the reduction
to the appearance of the egg (the cryptic pattern is of the impact of brood parasitism, the behaviour by
effectively a dishonest signal to a predator). Others which a female lays her eggs in the nest of another
in this family of explanations include the evolution bird. Brood parasitism can occur between individ-
of patterns to facilitate egg recognition by incubat- uals of the same species (when it is more usually
ing parents and/or the evolution of patterns to referred to as egg dumping), but is probably better
signal female quality (presumably to male birds). known as an interspecies activity. Brood parasitism
in the traditional (interspecific) sense is a compara-
tively rare breeding strategy found in less than
4.4.2 Egg mimicry 1 per cent of bird species but having evolved in a
In an attempt to stay one step ahead of the competi- broad range of taxa, notably the cowbirds Icteridae,
tion some brood parasites such as the Cuckoo whydahs Viduidae, honeyguides Indicatoridae,
Cuculus canorus lay eggs that accurately mimic those and the cuckoos Cuculidae. It is also exhibited in a
of their host, thereby making their discrimination number of species that have precocial young (quite
and rejection harder. At the population level, female independent at hatching), often as part of a wider
Cuckoos lay eggs of a range of colours and patterns reproductive strategy that does involve incubation
but each individual female lays only one type and of own young. So for example brood parasitism
preferentially parasitizes only one or a small number amongst the various species of duck Anatidae is
of the wide range of hosts available. Those that she widespread and with one exception all of the spe-
chooses are the ones with eggs most similar to her cies involved do most commonly rear their own
own. This host specificity is thought to be genetically young. The exception in this case is the Black-
controlled and sex-linked to the W chromosome. headed Duck Heteronetta atricapilla which is an
There is experimental evidence to support the utility obligate brood parasite (i.e. it never rears its own
of this egg mimicry in that in a range of host/para- young) and has been recorded laying its eggs in the
site pairs, hosts have been found to reject a higher nests of 18 different species including gulls, ibises,
proportion of non-mimetic than mimetic eggs. herons, coots, rails, and even birds of prey.
Flight path: Brood parasitism is just one of a wide

4.4.3 Egg recognition range of reproductive strategies, page 97.
Recognition of one’s eggs is likely to be important Egg dumping is common, for example, amongst
in two key situations: when trying to find them in a some species of colonially nesting African weaver
crowded colony; and, when trying to separate them birds Ploceidae, females of which occasionally lay
from others laid alongside them within a clutch. In an egg in the nest of one of their neighbours. This
the former case it is important that incubating birds might be to their advantage as both an insurance of
are able to discriminate between their own eggs and their output against the risk that their own nest will
those of their neighbours in a colony. In many col- suffer predation and as a means by which they can
onies the eggs of open nesting birds are laid in very increase their total productivity. Of course from the
close proximity to one another and although birds viewpoint of the recipient of the dumped egg,
returning to incubate are likely to gain information investment in the incubation and rearing of the
from a variety of cues relating to nest position in the young of another pair is not an advantage, it reduces
colony and perhaps directly from their partner, if it the investment that can be made in one’s own
is in attendance at the nest, the ability to recognize young. Weaver egg patterns are very diverse, per-
one’s own eggs is clearly important. It has been haps as an adaptation to increase the ability of
shown experimentally that Guillemot are able to females to recognize their own eggs and enable
discriminate between their own egg and those of them to remove those of their competitors. Some
their neighbours on a crowded cliff ledge because weaver bird species are the hosts of the Diederik
they recognize the colour and blotch pattern of their Cuckoo Chrysococcyx caprius, a brood parasite in the
own particular egg. traditional interspecific sense of the term, laying its
Box 4.1 When does it pay hosts to accept brood parasites?
Natural selection seems to favour those host birds able to predation rates (as do unparasitized eggs) and the most
recognize and eject the eggs of brood parasites. Numerous likely predator in this case is the cowbird.
examples of the ‘arms-race’ between the egg mimicry ability Hoover and Scott interpret their findings as follows: When
of the parasite and egg recognition abilities of the host have they reject a cowbird egg, warblers induce a high price—a
been described. But it seems that there may be instances visit from the cowbird and predation of their clutch. It there-
when the parasite can get the upper hand and it will pay the fore pays them to accept the egg in a scenario that is some-
host to accept the cost of rearing the cuckoo in the nest. what like a mafia protection racket! By predating warbler
Jeffery Hoover and Scott Robinson have carried out an nests the cowbirds act as ‘farmers’ inducing the laying of
elegant series of experiments involving the relationship second clutches which provide new parasitism opportunities.
between Brown-headed Cowbirds Molothrus ater and their
Prothonatory Warbler Protonotaria citrea hosts. In this sys- (A) 80
tem, unlike that of other brood parasites, hosts raise the
Nest predation (%)

alien chick alongside their own brood—paying an energetic 60 a
cost and producing weaker chicks as a result.
40
The researchers wanted to investigate two interesting
b
hypotheses: That the cowbirds may ‘farm’ their hosts, i.e. 20
induce parasitism opportunities; and, that the warbler hosts c c c
may be ‘intimidated’ into accepting parasitism by the conse- 0
quences of not doing so. In essence they suspected the para- 1 2 3 4 5
sites of mafia-like behaviour—punishing those warblers Treatment category
that ejected their eggs by returning to destroy their clutches. (B) 5
Warbler offspring/nest
To test their ideas Hoover and Robinson established a c c

4
nest-box breeding population of warblers in an area fre- b bc
quented by cowbirds and carefully monitored nesting 3
attempt outcomes. They noted parasitism rates and manipu- 2 a
lated parasitized nests. Some they allowed to develop natur-
1
ally but from some they removed the cowbird egg. Some,
but not all, of these manipulated nests then had their 0
1 2 3 4 5
entrance hole reduced to permit warbler access whilst
Treatment category
excluding cowbirds.
Look carefully at the results of the experiment (Figure 4.6).
Figure 4.6 The figures show predation rates (A) and warbler
Treatments 3, 4, and 5 show that in ideal conditions (no success (B) in each of five experimental treatments. Under treatment
parasitism or egg removed but no possibility of a return to 1 cowbird eggs were removed and cowbirds were allowed
the nest by the cowbird) a Prothonatory Warbler pair might subsequent access to the nest. Treatments 2 and 5 include all nests
expect to raise three or four chicks per breeding attempt, that were not parasitized (in 2 cowbird access would be possible, in
and that these nests were rarely predated. Treatment 3 also 5 it would not). Under treatment 3 the cowbird egg was accepted
reveals a cost to the warblers of accepting the parasite in by the warblers, and cowbirds always had access to the nest. Under
that warbler productivity is lower in these nests than in the treatment 4 the cowbird egg was removed and access to cowbirds
nests of treatments 4 and 5. The cost paid by accepting the subsequently denied. From Hoover, J.P. and Scott, K. (2007)
Retaliatory mafia behaviour by a parasitic cowbird favours host
parasite (about one chick) is however far lower than that
acceptance of parasitic eggs. Proceedings of the National Academy
paid by birds that reject the egg (treatment 1)—who on
of Science 194(11), 4479–83. Copyright (2007) National Academy
average raise only one of their chicks. These nests suffer high of Sciences, USA.
eggs in the nest of another species and leaving its most colourful eggs so they did invest more in the
young to be raised by these unwitting foster par- chicks of healthy females (presumably these females
ents. It is possible therefore that egg recognition by produce healthy chicks). Thus it is possible that egg
weavers is also a strategy to minimize the effect of colour was used as a cue by males.
this behaviour. Cruz and Wiley provided compel-
ling evidence to support this argument when they Key references
reported that a population of Village Weaver Ploceus Moreno, J., Morales, J., Merino, S., et al. (2006) More
cucullatus, introduced to the Caribbean island of colourful eggs induce a higher relative paternal
investment in the pied flycatcher Ficedula hypoleuca:
Hispaniola, lost most of their egg recognition ability
a cross fostering experiment. Journal of Avian Biology
during the 200 years of brood parasite-free exist-
37(6), 555–60.
ence that they enjoyed prior to the establishment of Martínez-de la Puente J., Merino, S., Moreno, J., et al.
a population of Shiny Cowbird Molothrus bonarien- (2007) Are eggshell spottiness and colour indicators of
sis. After just 16 years of coexistence with this brood health and condition in blue tits Cyanistes caeruleus?
parasite the discriminatory ability of the weavers Journal of Avian Biology 38, 377–84.
had almost completely returned.
On the other hand José Martínez-de la Puente
Key reference and co-workers have demonstrated a correlation
Cruz, A. and Wiley, J.W. (1989) The decline of an between egg shell patterning and a measure of low
adaptation in the absence of presumed selection female quality in the Blue Tit Cyanistes caeruleus.
pressure. Evolution 43, 55–62.
Blue Tit eggs are white with red-brown spots that
are the result of the incorporation of protoporphy-
rins in the matrix of the shell. The presence of these
4.4.4 Signals of quality
pigments in the shell seems to be a consequence
Egg colouration may also be a signal used by males of elevated protoporphyrin levels in the laying
to judge the quality of a female and of her offspring. female. These pigments are oxidants rather than
Juan Moreno and co-workers have shown that the anti-oxidants and at elevated levels they can indi-
eggs of a Spanish population of Pied Flycatcher cate and even cause poor health in the adult bird.
Ficedula hypoleuca vary in the intensity of their blue- Specifically the researchers have shown that
green colouration (measured in terms of the intensity females in poor body condition, indicated by their
of their reflectance of light in the blue-green region of having a higher cellular level of a protein HSP70
the visible spectrum); eggs are similar within a which is known to be linked to stress, laid spottier
clutch, but variation between clutches is marked. eggs. So perhaps increased patterning is a means by
The blue-green colouration of the eggs of this species which females can rid their bodies of excess proto-
is a result of the deposition in the matrix of the shell porphyrins and improve their own health status.
of the pigment biliverdin. This pigment has antioxi- There is no evidence currently that male Blue Tits
dant properties and is positively correlated with respond either positively or negatively to this
immunocompetence in adult birds. It is likely that potential signal.
only healthy females will have a sufficient surplus of
biliverdin to produce really blue-green eggs. Egg
4.4.5 Pigments and shell quality
colour could therefore be a signal of female health
status or quality, but what evidence is there that An alternative explanation of the significance of
males actually take note? To explore this question the protoporphyrin pigments in passerine egg shells has
researchers made observations of male provisioning been proposed by Andrew Gosler and co-workers.
rates at nests of known egg colour type (they also Their study involved working with the eggs of a
cross-fostered clutches to ensure males really were population of Great Tits Parus major, which like
responding to egg colour and not to laying female Blue Tits have a white egg patterned with brown
behaviour or other cues). They found that males made spots. Birds in their study population (at Wytham
more provisioning visits to the nests containing the Woods near Oxford, UK) laid rounder, spottier eggs
(A) (B)
Figure 4.7 A Great Tit clutch (A) and eggs from five clutches to illustrate their variability (B). The eggs shown here in ‘columns’ are from five
separate clutches and the ‘rows’ are the first (top), middle, and last (bottom) eggs of the laying sequence in each of them (© Andrew Gosler).
if their territories were low in calcium, and more really no more than a ‘nest-site’—a suitable patch of
elliptical, less spotty eggs if their territories were largely unmodified bare ground/wood onto which
high in calcium (Figure 4.7). an egg is placed. Many species of wader for example
lay their eggs directly into a shallow depression or
Key reference scrape on the ground (see Figure 4.5). Similarly cliff
Gosler, A., Higham, J.P., and Reynolds, S.J. (2005) Why nesting auks such as Guillemot Uria aalge and
are birds’ eggs speckled? Ecology Letters 8 1105–1113. Razorbill Alca torda lay their eggs directly onto what
seem to be the narrowest of rock ledges. The house-
The significance of these observations seems to be keeping in establishing these simple nests may
that the brown spots are coincident with thinner involve the rearranging or removal of materials, but
(less calcium rich) areas of the shell, and spottier no real construction takes place. However, when we
eggs therefore had generally thinner shells. A thin- think of a nest we are more likely to imagine a
ner shell is a weaker shell and this might explain the clutch of eggs nestling in a cup that has been built
recorded difference in egg shape because a rounder by a bird from a range of suitable materials. You
egg is stronger than an elliptical one. This difference probably have a mental image now of a cup with a
in shell quality can be easily explained. Female strong outer casing woven from twigs and strong,
birds must obtain calcium from their environment thick grasses within which nestles a smaller cup
and in a calcium-poor environment they will prod- lined with soft down feathers? This is one kind of
uce poorer eggs. But what about the spots? Being nest, but in fact the variety of nests, nest locations,
coincident with thinner areas of shell it is presumed and nesting materials is so enormous that it is
that they play an important structural role and act beyond the scope of an introductory text such as
as strengthening agents. this and I would recommend that the interested
Of course it is possible that the potential health reader consult Mike Hansell’s excellent book Bird
status signal and egg shell strengthening roles of Nests and Construction Behaviour. Nests are placed
protoporphyrins are not mutually exclusive—birds within cavities or burrows; stuck to vertical surfaces
low in calcium might be in generally poor condi- with mud, faeces, and saliva (Figure 4.8); they float
tion, producing poor quality eggs. ‘tethered’ to emergent vegetation; they hang over
water; they are placed in vegetation at ground level,
in shrubs and in tree-tops (Figure 4.9). Some are so
4.5 Nests
small that females straddle them rather than sitting
Nests are the places and structures where eggs are on them when incubating eggs and others are so
laid and incubated. The most simple nest of all is large that their weight can bring down the tree in
where, in the case of altricial species, chicks can be

safely reared. Nests tend to be quite messy places
and so nest hygiene is important (Box 4.2). In
order for the embryo inside to develop, eggs must
be kept warm. In fact the eggs of most species
require a fairly constant temperature of around
38ºC (100ºF) and above ambient humidity (to pre-
vent water loss from the egg through the porous
shell). Relatively few birds experience such tem-
peratures in their environment and for those that
do environmental temperatures are likely to fluc-
tuate to too great an extent to make ambient incu-
bation a possibility. Australasian megapodes do of
Figure 4.8 The mud nest of the Red-rumped Swallow Hirundo course practice environmental incubation, bury-
daurica (© Robin Arundale). ing their eggs under mounds of earth and organic
matter, which as it decays releases the steady heat
that they require. The majority of species however
practice direct incubation with parent birds ‘sit-
ting’ on the eggs until they hatch. In many cases
both sexes share incubation duties, but there are
numerous examples of female only incubation
and more rarely examples of male only incuba-
tion. Birds are able to influence incubation tem-
perature and humidity in a number of ways. They
may simply choose a nest site that is likely to pro-
vide the conditions required (or make it easier
to achieve them). As an example, in their edited
volume, Charles Deeming and Jim Reynolds
describe the fact that Palestine Sunbirds Cinnyris
osea typically position their nests so that the open-
ing faces away from the prevailing wind in order
to prevent cooling of the eggs, and in shade (rather
Figure 4.9 The intricately woven nest of a weaver bird (Ploceidae) than full sun) to minimize fluctuations in ambient
(© Graham Scott). temperature. Birds are also able to vary the mater-
ials that they use when constructing their nests to
which they have been built (the huge colony nests
accommodate local conditions. In a comparative
of some social species of African weaver bird for
study Vanya Rohwer and James Law have ana-
example).
lysed the properties of the nests of Yellow Warblers
breeding in two different parts of their Canadian
Key references range. They found that those birds breeding in
Hansell, M. (2000) Bird Nests and Construction Manitoba built larger, less porous nests with more
Behaviour. Cambridge University Press, Cambridge. insulation than those built by birds breeding in
Deeming, D.C. and Reynolds, S.J. (eds) (2015) Nests, Ontario. This is significant because the Manitoba
Eggs and Incubation: New ideas about avian climate is colder and windier than that of Ontario
reproduction. Oxford University Press, Oxford.
(which is wetter), and so in Manitoba nests that
are windproof and well insulated are best, whereas
The primary function of a nest is to provide a safe in Ontario too much insulation would hamper
place in which eggs can be laid and incubated and drying.
Box 4.2 Nest hygiene
Many birds attempt to maintain nest hygiene by defecating poulty from ectoparasites. On the streets of Mexico City birds
over the lip of the nest, although this can make nests conspicu- have a ready supply of pre-packaged repellent in the form of
ous and perhaps for this reason the chicks of many passerines cigarette butts. Constantino Macías Garcia and his colleagues
produce discrete faecal pellets that are collected and ingested explored the relationship between the amount of material from
or carried away for disposal by the parent birds. This copraphagy cigarette butts in the nests of birds and the numbers of
may seem unpleasant to us, but it has been shown to make a ectoparasites in those nests. They found that nests with more
significant contribution to the nutrition of some breeding birds. cigarette material had lower ectoparasite loads (Figure 4.10),
To further maintain nest health some species regularly add fra- but also that material from butts that had been smoked
grant green vegetation to their nests It has been suggested appeared to be more effective than unsmoked material, per-
that the volatile chemicals given off by these plants may act as haps because burning releases higher levels of the pesticide.
insecticides or arthropod deterrents and by including them Furthermore, in a subsequent experiment the researchers dem-
birds may be able to limit the harmful effects of nest parasites. onstrated that house finches actively add butts to nests when
For example, Adèle Mennerat and her co-workers have shown the researchers had added extra live ticks suggesting that the
that Blue Tit chicks raised in nests with aromatic plant frag- incorporation of the pesticide is a response to an actual parasite
ments have higher blood haemocrit levels than those raised in load and that the birds are in effect ‘self medicating’.
nests without added vegetation. Haemocrit levels are related
to the oxygen-carrying capacity of the blood and are an indica- References
tor of general health, so it does seem that there is a benefit to Mennerat, A., Perret, P., Bourgault, P., et al. (2009) Aromatic
the addition of this material to the nest in that it may in some plants in nests of blue tits: positive effects on nestlings.
way enable birds to better withstand parasite attack. Animal Behaviour 77, 569–74.
In Mexico City House Sparrows Passer domesticus and House Suàrez-Rodríguez, M. and Macìas Garcia, C. (2017) An
Finches Carpodacus mexicanus have found a novel way to experimental demonstration that house finches add cig-
utilize nicotine and other chemicals from the tobacco plant to arette butts in response to ectoparasites. Journal of Avian
maintain nest health. Farmers use the same chemicals to protect Biology 48(10), 1316–21.
100
no. ectoparasites in the nests
75
50
Figure 4.10 House Sparrow (black circles) and House Finch

25 (grey circles) nests that include more material from cigarette
butts typically contain fewer ectoparasites. From Suàrez-
Rodríguez, M., López-Rull, I., and Macìas Garcia, C. (2013)
Incorporation of cigarette butts into nests reduces nest ectopara-
0 5 10 15 site load in urban birds: new ingredients for an old recipe?
weight of cellulose from cigarette butts (g) Biology Letters 9(1), 20120931.
Key reference 4.6 Incubation

Rohwer, C.G. and Law, J.S.Y. (2010) Geographic
Incubation periods vary greatly—the eggs of some
variation in nests of yellow warblers breeding in
Churchill, Manitoba, and Elgin, Ontario. The Condor species of African weaver bird (Ploecidae) hatch in
112(3), 596–604. just nine days, whereas those of some penguin spe-
cies take 65 days, and those of kiwis can take an
amazing 85 days to hatch.
Flight path: Reproductive strategies vary between
A few days before the onset of incubation physio-
species. page 97.
logical changes occur in the parent bird. Levels of
the hormone prolactin circulating in the blood need to be warmed it shrinks away and the feathers
stream increase and at the same time levels of circu- regrow when the bird next moults.
lating testosterone decrease. This hormone shift is By adjusting the position of eggs in the nest
thought to be a trigger for the onset of incubation (Figure 4.12) and by raising and lowering their
and parenting behaviours and for a reduction in the body over the eggs, birds can control their tempera-
performance of behaviours related to territoriality ture and in extremes of heat some species of open
and courtship. All of these behaviours will be fur- nesting bird stand above the eggs to give a parasol
ther discussed in chapter 5, but at this stage I do
want to briefly describe the development in the
incubating bird of a specialized ‘organ’ to facilitate
the transfer of body heat to the egg. Feathers on
the lower breast and belly are lost (they drop out or
are pulled out, and may then be used in nest insula-
tion) and the bare skin beneath them swells with
fluid. The blood vessels beneath this skin dilate
thereby increasing blood flow to this region. This
brood patch as it is termed (Figure 4.11) is concealed
by the contour feathers in a non-incubating bird,
but as it settles onto the nest, the feathers are drawn
back such that the hot skin of the patch makes direct
contact with the eggs. The brood patch is a tempor-
ary feature of incubating birds and once the eggs Figure 4.11 The unfeathered belly skin of this female European
have hatched and the developing brood no longer Goldfinch Carduelis carduelis is stretched taught and heavily
vascularized to create a brood patch (© Chris Redfern).
Figure 4.12 This Oystercatcher has just adjusted the position of her eggs and is settling down to continue their incubation (© Graham Scott).
Box 4.3 Birds, eggs, and agricultural chemicals
The second half of the twentieth century began with a global apparent reason (they were not the victim of trauma for
expansion in and intensification of agriculture. This involved a example), and clutches of eggs were found broken and/or
worldwide increase in the application of new pesticides and abandoned. In 1970 Derek Ratcliffe published a keystone
herbicides, designed to boost crop yields by decreasing popula- paper in the Journal of Applied Ecology in which he demon-
tions of crop pests and competitors. There are even pesticides strated that the main cause of the population declines was
designed to directly target bird species in soft fruit growing breakage of eggs in the nest, a phenomenon that he showed
areas. However from the ornithologists perspective perhaps the to have arisen quite suddenly in the mid/late 1940s. After
most notorious of these chemicals were not those intended to making measurements of shells laid during the period of the
control birds but those which had an indirect impact upon them. decline, and comparing them with collected eggs from earlier
During the 1950s and 60s marked declines in numbers of in the century, he proved that the increase in egg breakage
birds of prey were recorded throughout the countries of the coincided with a sudden change in the quality of egg shells, in
developed world. Adult birds were found to have died for no simple terms the shells of the eggs had become thinner
2.30
2.20
2.10
2.00
1.90
L(mm) x B(mm)
Weight (mg)
1.80
1.70
1.60
Eggshell index
1.50
1.40
1.30
1.20
1.10
1.00
0.90
1900 1910 1920 1930 1940 1950 1960 1970
Year
Figure 4.13 Note that eggshell thickness for UK Peregrine Falco peregrinus remained fairly constant during the period 1900–1945 but
that during the post-war years (1945–1970) shells became considerably thinner on average. This was coincident with increased use of DDT.
Adapted from Ratcliffe, D. (1970) Changes attributable to pesticide in egg breakage frequency and eggshell thickness in some British birds.
The Journal of Applied Ecology 7, 67–115.
continued
Box 4.3 Continued

1.3
(Figure 4.13). Ratcliffe’s paper did more than just demonstrate
the incidence of thinning. It also provided correlational evidence
to support the idea that the most likely cause of the thinning 1.2
was an accumulation in the birds concerned of residues of
Shell index
organochlorine pesticides such as DDT which had come into 1.1
widespread use in the period 1946–1950. Subsequent experi-
mental work has confirmed that the breakdown products of
1.0
organochlorines (DDE from DDT, HEOD from dieldrin and
aldrin, and PCBs) do all impact upon the calcium metabolism
of birds thereby directly causing egg shell thinning. 0.9
Having identified organochlorine pesticides as a main 1960 1970 1980 1990 2000
factor in the decline of bird populations, many governments Year
legislated against the general use of organochlorines and
Figure 4.14 Shell index (thickness) values for UK Merlin Falco
against the use of DDT, aldrin and dieldrin in particular (they
columbarius have increased during the post-DDT era, almost
were banned in the UK in 1986 for example). But has it done returning to pre-DDT levels (index c. 1.25). Reproduced from
any good? Well thankfully it has. Take for example the case Newton, I., Dale, L., and Little, B. (1999) Trends in organochlorine
of the Merlin Falco columbarius a small raptor common and mercurial compounds in the eggs of British Merlins Falco
throughout North America and northern Europe. It is a bird columbarius. Bird Study 46, 356–62, with permission of BTO.
that is known to have suffered egg shell thinning and
reduced breeding success throughout its range. Ian Newton White-backed Vulture (Gyps bengalensis) on the Indian sub-
and colleagues have shown that in the case of the British continent fell by a staggering 95 per cent for example. Initial
Merlin population legislation has probably saved them from speculations suggested an epidemic specific to vultures
the brink of extinction. By the 1980s their numbers had might be to blame, but very quickly diagnostic tests revealed
fallen to just 500 or so pairs in the whole of the British Isles, that a pollutant was the causal agent. Specifically, in 2004
just ten years later the population had more than doubled to Lindsay Oaks and co-workers demonstrated that the anti-
an estimated 1300–1500 pairs. This increase coincided with inflammatory drug Diclofenac was causing renal failure in
both a fall in the detectable levels of organochlorines, such the birds. This drug was in widespread use in the treatment
as DDE, in eggs from failed broods and an increase in an of domestic livestock. When treatment was unsuccessful
index of egg shell quality approaching the pre-1946 level livestock carcasses were simply left to be scavenged by the
(Figure 4.14). vultures; the birds ingested the drug and died as a result. By
So have we as a society learned a valuable lesson from 2006, just two years later, India had announced its intention
this potentially disastrous episode? The answer to that ques- to ban the use of Diclofenac in an attempt to halt the decline
tion is a qualified yes. It took decades to recognize the issue of vulture populations and hopefully protect these birds from
relating to organochlorine use, decades for positive remedial extinction. In the years that have followed vulture friendly
action to be taken and only now, decades later, are we see- drugs such as Meloxicam have been developed as alterna-
ing the full benefit of those actions (and it should be remem- tives to Diclofenac and captive breeding programmes of the
bered that high levels of these chemicals in the environment most affected vulture species have been established in an
are still having their effect in a number of parts of the world). attempt to boost populations. It would appear therefore that
But as a society we continue to rely upon the introduction although we have not yet learned to avoid such mistakes
of chemicals into the environment to solve our agricultural completely, we have learned to identify them and respond to
problems and all too often we come to realize their negative them positively more quickly.
environmental impacts only in the face of a catastrophe.
Take for example the sudden and dramatic demise of the Reference
worlds vultures during the opening years of the twenty-first Oaks, J.L., Gilbert, M., Virani, M.Z., et al. (2004) Diclofenac
century. Populations of some vulture species declined residues as the cause of vulture population decline in
massively between 1990 and 2000; numbers of Oriental Pakistan. Nature 427, 630–33.
effect—if this is insufficient they make a trip to a thinner areas of shell. In fact the qualities of the
local water supply, wet their breast feathers and pigment/shell matrix that strengthen it against
then return to drip cooling water directly onto the forces from outside of the egg may in fact operate
eggs. In heavy rain birds spend less time away from in reverse against forces from within—effectively
their nests than on dry days, presumably to keep making it easier for the chick to break the shell. In
their eggs dry and prevent chilling. You will recall the Great Tit it has been noted that maximum areas
that at the time of laying, the embryo within the egg of pigmentation coincide with the shoulder of the
is little more than a cluster of cells on the surface of egg—the area first breached by the chick.
the yolk (Figure 4.1). As incubation progresses these The process of hatching (or pipping as it is some-
cells repeatedly divide and differentiate and the times called) can take anything from a few hours in
embryo becomes recognisably a bird. the case of a small passerine, to a few days in the
case of some of the larger birds. Often the chick com-
pletes the process unaided but there are examples of
4.7 Hatching
a helpful parent assisting in the final stages of the
You will recall from Figure 4.2 that within the egg break out. Having hatched, parental assistance is
there is an air space. This is particularly significant almost always essential. Newly hatched chicks are
during the period immediately prior to hatching. exhausted, wet, and extremely vulnerable to
Once it has fully developed, the chick begins to push predators. As a minimum parents brood chicks until
with its beak against the membrane of the air space. they dry, but the extent of the care that they provide
This marks the beginning of hatching—a process beyond that will vary from species to species.
that is thought to be triggered when the chick has
quite simply outgrown its space. Specifically the
4.8 Chicks
onset of hatching coincides with increased hypoxia
and hypercapnia, i.e. the chick is simply not able to Newly hatched chicks demonstrate a range of levels
take up enough oxygen, or expel enough carbon of development. At one extreme the chicks of
dioxide via the chorioallantoic respiratory system, Australasian megapodes (Megapodiidae), hatching
and in effect it needs to hatch before it suffocates. To from eggs that have been incubated for a prolonged
assist it the chick has two temporary anatomical period in a mound of compost or fermenting vegeta-
features related to hatching. One is an overly devel- tion, require no parental care. They hatch feathered
oped hatching muscle (more properly termed the and are able to fly almost at once. They are also able
complexus muscle) at the back of the head and neck to thermoregulate and to forage for themselves. Such
that provides the extra strength needed to break out chicks are classed as being superprecocial. At the
of the shell. The other is the egg tooth, a sharp pro- other extreme are the newly hatched chicks of the
cess at the tip of the upper mandible of the beak that passerines (Box 4.4). Hatching blind, naked, and
is used to pierce the air space membrane. Once the helpless these altricial chicks rely entirely upon their
air space is broken into, the chick begins to use it parents for warmth, food, and protection. Interestingly
lungs to breath air directly. The chick uses the egg it has been suggested that such helplessness is only
tooth to scrape the inner surface of the shell and by possible because passerines have evolved the ability
a combination of scraping and pushing it eventu- to construct a complex nest which protects chicks
ally makes a tiny hole. By repeating this process, from predators and from inclement weather.
and at the same time rotating the egg, the chick Between these two extremes there are various
eventually weakens the shell sufficiently to cut off grades of precocial/altricial development. In his
the cap and break out. review of the subject Starck suggests that eight
Interestingly the protoporphyrin pigments of different classes of chick can be recognized: the
brown speckled eggs that were discussed in an earl- superprecocial, three grades of precocial chick,
ier section of this chapter may be important in semiprecocial and semialtricial, and two grades of
hatching too. If you remember there is a suggestion altricial development which differ principally in
that these pigments play a strengthening role in therate of their growth.
find their own food and so must be fed by their

Key reference parents (who place food in front of hungry chick
Starck, J.M. (1993) Evolution of avian ontogenies. In and demonstrate pecking behaviour to them).
Current Ornithology Power, D.M. (ed.) Plenum Press,
The semiprecocial chicks of most gulls and terns
New York.
are down-covered and fed/brooded by their par-
According to Starck’s classification precocial chicks ents at the nest (Figure 4.15). However, when threat-
are mobile and sighted upon hatching and require ened they will leave the nest that is typically quite
varying degrees of parental care. For example the exposed, and run/swim for cover, returning to the
chicks of ducks and pheasants follow their parents nest when it is safe to do so. Interestingly, but per-
and are protected by them. They are initially down- haps not surprisingly, the young of cliff nesting
covered and so must be brooded by a parent to sur- Kittiwakes Rissa tridactyla differ from those of their
vive cold/wet weather, but like megapodes’ chicks gull cousins in that when danger threatens them
they are able to feed themselves from hatching. The they do not flee the nest (a bad thing to do if you
precocial chicks of coots and rails are very similar to live on a cliff face!). Instead they crouch in the nest
those of pheasants but they are initially unable to cup and as a result of their cryptic plumage can be
(A) (B)
Figure 4.15 (A) These newly hatched semiprecocial Arctic Tern Sterna paradisaea chicks will stay in their nest for only a few days (© Ian Grier).
(B) In contrast, these altricial Cormorant Phalacrocorax carbo chicks will be nestbound for several weeks (© Les Hatton and Shirley Millar).
Box 4.4 Speed is of the essence but there is a price to pay
Typically during the early summer I am able to assign the difference in the structure of these feathers? This is exactly
passerine birds that I catch as part of my data collection to the question that Lea Callan and her colleagues at Cornell
one of two age classes. Juvenile birds (those that have University and the US Geological Survey, Montana set out
hatched and fledged during the preceding weeks) typically to answer.
have very loose and fluffy body feathers whereas the body Specifically the researchers tested the hypothesis that
feathers of adult birds (birds at least one calendar year old) loosely textured juvenile feathers are the result of a trade-off
tend to be more substantial. In essence these juvenile that takes place during the nestling phase between growth
feathers could be thought of as being less good quality. rate and risk of predation. Essentially they asked the ques-
Given that I stressed the importance of good quality fea- tion: do some juvenile birds have loosely textured feathers
thers in chapter 2, the question that you may be asking because the risk of being predated whilst in the nest is a
yourself is why should this be the case? What explains this greater potential fitness cost of fledging with them, and
suffering an associated cost of say, poorer thermoregulation more adult-like feathers. But the analysis did not support
or reduced flight efficiency, for example. either of these ideas. What the team did determine was that
To test their hypothesis the research team studied 123 species that spend a longer time in the nest grew more
altricial species and measured the quality (the number of adult-like feathers compared to those that fledge at an earl-
barbules per centimetre of rachis) of the flank feathers of ier stage (Figure 4.16A). For 67 of the species that were
adult birds and of juvenile birds a few days after they had included in the analysis, the researchers had access to infor-
left the nest. In some species juvenile feathers were very mation about relative nest predation rates and when that
different to those of adult birds, and in other species the data was included in the analyses it was found that species
feathers of the two age categories were not easily suffering the lowest rates of nestling predation grew the
distinguishable from one another. most adult-like feathers (Figure 4.16B). These results confirm
It might have been expected that birds in warmer places that increased nestling predation risk is an important select-
would have had lower quality (more open) feathers because ive pressure that drives rapid chick growth and early fledg-
the pressure to retain body heat is lower. Or perhaps those ing, but at a cost. Faster growth results in less good feather
species that do not undergo a post-juvenile moult and so do quality, but presumably the fitness benefits of early fledging
not replace their feathers prior to migration would have outweigh this cost.
(A) (B)
juv ad juv ad
1.0 a b
1.0 1.0
0.9 0.9 0.9

Feather structure
Feather structure
Feather structure
0.8 0.8 0.8
0.7 0.7
0.7
0.6
0.6 juv ad 0.6
juv ad
0.5
0.5
0.00 0.02 0.04 0.06 –0.03 –0.01 0.01 0.03
10 15 20 25 30 Daily rates of nestling predation Daily rates of nestling predation
Time in the nest (days) controlling for time in the nest
Figure 4.16 (A) The feathers of nestlings that spend longer in the nest are higher quality in both tropical and temperate species, and
those of tropical species are on average of lower quality than those of temperate species. Figure 4.16(B) The indirect (a) and direct (b) effects
of nest predation risk on feather quality. (a) shows the indirect effect because predation risk is strongly correlated with time spent in the
nest. (b) shows a direct effect because even taking into account the effect of time in the nest, those species at high risk of predation still
grow less adult-like feathers. From Callan, L.M., La Sorte, F.A., Martin, T.E., and Rohwer, V.G. (2019) Higher nest predation favours rapid
fledging at the cost of plumage quality in nestling birds. The American Naturalist 193(5), 717–24.
quite difficult to see. These chicks would be classed of nest, and incubation vary greatly from species to
as being semialtricial. species. In some cases birds do not care for their
own young and such egg dumpers/cuckolds are
involved in an evolutionary arms race with their
Summary
hosts. Some chicks are independent soon after
Eggs permit the external development of young, hatching, others depend upon the care of their par-
allowing female birds to maximize output without ents for some time. As eggs and chicks, young birds
compromising flight. Females routinely lay opti- are particularly vulnerable to predation and to the
mally sized clutches although clutch size, location consequences of pollution.
C H A PT ER 5
Reproduction
‘The dunnock’s sex life is an arrangement of huge complexity.’

Mark Cocker (2005)
In chapter 4 I outlined the basic sequence of events but in other species females are promiscuous and
from the laying of an egg to the hatching of a chick. post-copulatory competition (competition between
In chapter 5 I want to explore the diverse mating sperm after insemination, see Box 5.1) becomes more
systems exhibited by birds in more detail and to important. In birds at least it also appears that there
consider behaviours such as courtship and territori- is an advantage associated with a higher number of
ality that precede egg laying, and those that follow sperm reaching the site of fertilization. Although in
hatching during the raising of chicks to independence. mammals penetration of the egg by many sperm
(polyspermy) is damaging to the ovum, research
conducted by Nicola Hemmings and Tim Birkhead
Chapter overview on Zebra Finch Taeniopygia guttata and domestic
fowl has demonstrated that in birds a level of poly-
5.1 Males and females are different spermy is advantageous. Their results suggest that
5.2 Mating systems penetration by too few sperm results in reduced
5.3 Courtship and mate choice embryonic survival. They have also shown that if
5.4 Song fewer sperm are inseminated a greater proportion
5.5 Raising a family than expected reach the ovum. This suggests that
some mechanism exists which allows females to
regulate the numbers of sperm that are destroyed,
5.1 Males and females are different ejected, or ‘allowed’ to proceed. Why are birds and
Males and females are different. I made the point in mammals different? Hemmings and Birkhead sug-
chapter 4 that the gonads of males and females dif- gest that the answer to that question might be
fer, and of course associated with that difference related to the fact that while a mammalian egg is
their gametes, the products of the gonads, also typically fertilizable for up to 24 hours, a typical
differ. Male gonads produce millions of sperm (the avian egg has a window for fertilization of just 15
male gamete) at each ejaculation even though only minutes and so perhaps polyspermy is necessary to
a small number need reach the egg (the female gam- ensure a sufficient number of sperm reach the ovum
ete) to ensure successful fertilization and most of in good time.
the sperm produced are destroyed or ejected by
Key reference
the female. This may seem to be a wasteful process,
Hemmings, N. and Birkhead, T.R. (2015) Polyspermy
but it is necessary for a number of reasons. As
in birds: sperm numbers and embryo survival.
we will see later in this chapter the males of some Proceedings of the Royal Society B: Biological Sciences
species compete with one another to monopolize 282, 20151682.
opportunities to mate (pre-copulatory competition),
DOI: 10.1093/oso/9780198804741.003.0005
REPRODUCTION 95
Box 5.1 Sperm competition
The realization that a female bird might mate with more the existence of within-female competition between the
than one male during a reproductive cycle has resulted in a sperm of different males and the potential consequences of
dramatic shift in the way in which ornithologists perceive extra-pair copulations (EPCs). The results of some of these
competition between males to pass on their genes. Prior to experiments are summarized in Figure 5.2.
this paradigm shift pre-copulatory competitive behaviour The first experiment (Figure 5.2A) was designed to simu-
was presumed to be the means by which male precedence late a situation in which a single female mates with two
was determined. However we now know that sperm compe- males, switching rapidly between them but mating with
tition, a post-copulatory phenomenon, is widespread and each in turn. In this case the result was that the second male
highly significant. (and last to mate with the female) fathered the majority of
We saw in chapter 4 that at copulation sperm are trans- the eggs that were laid. The second experiment (Figure 5.2B)
ferred from the male to the female and that they must then simulates the situation in which a female that mates regu-
travel through the oviduct to the infundibulum in order to larly with her mate (the first male) is involved in just one
fertilize the egg. Not all of the transferred sperm make this extra-pair copulation with the second male (significantly this
journey. Some of them enter sperm storage tubules at the EPC is the last copulation in the mating sequence). Again the
junction of the uterus and vagina (see Figure 4.1, chapter 4) figure shows that even this single mating by the second
where they can remain viable for periods of many days. male results in his fathering the majority of the eggs that are
Sperm from these tubules can be released to fertilize eggs laid. Taken together these two experiments demonstrate
produced over several days without the need for further sperm competition and a significant feature of this system—
copulation. Tim Birkhead and his co-workers at the University last male precedence.
of Sheffield have established that in the case of the Zebra The third experiment (Figure 5.2C) demonstrates the
Finch Taeniopygia guttata around 10 per cent of eggs laid effectiveness of a well known male strategy presumed to
13 days after the last copulation have been fertilized reduce the impact of EPCs and last male precedence—
(Figure 5.1). retaliatory copulation. In this experiment each male copu-
Birkhead and his colleagues have also investigated the lates with the female once, but these copulations follow one
effect of multiple male matings upon the paternity of eggs another almost immediately (simulating the situation in
laid by a female. Their work has demonstrated very clearly which a male might observe his mate copulating with a rival
100
80
% Eggs fertile
60
40
20
0
0 2 4 6 8 10 12 14 16 >16
Days after last possible copulation with fertile made
Figure 5.1 Egg fertilization levels decline with time following a copulation event but stored sperm may remain viable for up to 13 days.
From Birkhead T.R. and Møller A.P. (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, Copyright
Elsevier, Netherlands. Data from Birkhead, T.R., Pellat, J.E., and Hunter, F.M. (1988) Extra-pair copulation and sperm competition in the zebra
finch. Nature 334, 60–2.
continued
Box 5.1 Continued
Experiment: A B C
1.0
Probability of fertilization
1st Male
0.5
2nd Male
0
p<0.001 p<0.001 NS
Figure 5.2 The outcomes of experiments (A, B, and C) to investigate sperm competition in the Zebra Finch expressed as the proportion of
eggs fertilized by each of two competing males (see text for explanations of individual experiments). From Birkhead, T.R. and Møller,
A.P. (1992).
or might infer a recent copulation having witnessed his effective means by which a male might reduce the impact of
female return from the territory of a rival). In this case the an EPC because both males fathered a similar proportion of
data presented demonstrate that retaliatory copulation is an the eggs that were laid.
It is also significant that following ejaculation, stores

Concept
of sperm can be quickly replenished and so males are
Anisogamy
in theory capable of multiple matings and could
Males and females have different sized gametes.
potentially sire large numbers of offspring during a
Those of males (sperm) are small, mobile, and relatively
period of reproductive activity. Sperm are therefore inexpensive. Those of females (eggs) are relatively large,
often thought of as being relatively inexpensive to immobile, and expensive.
produce and each individual sperm is in itself prob-
ably not a particularly significant investment on the In basic terms we presume that all individuals seek
part of the male. Eggs on the other hand are relatively to maximize their own reproductive output by
large and they are relatively expensive to produce. which we mean that they seek to pass on as many
Eggs are also in finite supply and so each of them has copies of their own genes as possible. We can there-
significant value to the female, representing as it does fore assume that individuals of both sexes behave
one of a very limited number of reproductive oppor- in a way that will maximize their reproductive suc-
tunities available to her. This fundamental difference cess in terms of both the quantity of offspring pro-
in gamete size is termed anisogamy and it is import- duced and/or the quality of those offspring. As a
ant because the reproductive strategies of birds (and result of anisogamy it is the case that males and
other animals) are largely a consequence of it. females can probably maximize their reproductive
output in different ways. Because a male can mate
Flight path: the relationship between the genetic repeatedly, taking advantage of his easily replen-
make-up of the sexes and their behaviour, page 73. ished store of cheap sperm, we might reasonably
REPRODUCTION 97
assume that males can most easily increase their necessary to consider both the social basis of the
output by fathering as many young as possible. relationship between parent birds (do they work
Females on the other hand cannot usually adopt the together to raise young or does one partner desert
same strategy. They are constrained by a limited the other for example) and the genetic relationships
supply of eggs, and by the fact that there is a delay between offspring and social parents (i.e. the birds
between successive ovulations. For a female there- which rear them but are not necessarily their bio-
fore the most effective way to maximize reproduct- logical parents). Table 5.1 provides a brief descrip-
ive output is for her to maximize the quality of her tion of the main avian mating systems, many of
young. Females should therefore be expected to be which are described in more detail in section 5.3.
choosy about their mates, seeking to maximize the The fidelity unto death of a pair of birds has often
quality of the contribution made by the male parent been presumed as being a given truth. On the basis of
in terms of either the quality of his genetic material this commitment pairs of birds are often used as a
or of the resources that he is able to provide. symbol of fidelity in human society (St Valentine’s
One further consequence of the differences between day has bird associations for example). However, the
male and female birds is that although actual sex advent of genetic paternity analysis has revealed that
ratios may be close to 1:1 (i.e. there are the same num- in fact socially monogamous birds are often quite
bers of males and females of a species present in a promiscuous. A brood of apparent full siblings might
population), operational sex ratios may depart from in fact be sired by several males. Why should this be?
this significantly. This is because once a female bird Remember that male birds can maximize their repro-
has successfully mated she is likely to be unavailable ductive output by fertilizing as many eggs as pos-
for mating with another male because of the time she sible, and during that period of time when a female is
spends laying her fertilized egg and then in the major- incubating her eggs, her male partner will often seek
ity of cases because she will then invest time and matings with other females presumably to increase
energy in the successful incubation and rearing of her the number of offspring that he sires. Females on
eggs and chicks. During this period of time the male the other hand are limited in their ability to increase
is not similarly constrained and may be free to seek the number of offspring that they produce and so
another mate. As a breeding season progresses there- would be expected to focus on the production of
fore the operational sex ratio of the population will
skew towards the relatively numerous males and
away from the available females. In effect, females Table 5.1 Avian mating systems
can be thought of as being the rarer sex. Charles
Darwin recognized that anisogamy is one of the phe- System Main features of system
nomena underpinning the process of sexual selection,
Social One male and one female cooperate to raise a brood
an important evolutionary force, by which the mem- monogamy of young. Genetic monogamy describes the situation
bers of the rarer sex can be choosy about their mates, in which these birds are both the genetic parents of
and those of the more common sex will be forced to the chicks being raised.
compete at some level for access to mates. Polygyny A male bird sires the offspring of a female and then
deserts her (temporarily or permanently) to seek
other females with which to mate. Deserted females
5.2 Mating systems raise young alone or with reduced help from a
returning mate.
Although some species of socially monogamous
Polyandry A female bird abandons her eggs to be raised by her
(one male and one female) birds may be genetically male partner (this male is not always the genetic
monogamous i.e. no extra-pair copulations (EPCs), parent of the brood that he will raise). Deserting
more than 85 per cent of those species that have been females may seek to mate with further males in the
subjected to DNA paternity studies have been found same breeding season.
to be sexually polygamous (multiple males and or Polygynandry A group of males and females cooperate to rear
young. The resulting broods are produced by several
females contributing genetic material to a single
females and sired by several males.
brood). So when thinking about mating systems it is
fewer higher quality offspring. It has been suggested similar mate were no more likely to seek EPCs, but
that females could seek EPCs for a number of reasons. that when they did, their offspring were more genet-
Perhaps they need to increase the chance that their ically similar to one another than when they only
mate will be able to fertilize their egg, or that their mated with their social partner. It may be that in this
mate will be healthy. They may choose to mate species mating in a way that reduces genetic diversity
with males who have features that are more attractive may be advantageous because the population is a
to ensure that their sons will also be attractive. Anders highly out-bred one with high levels of immigration
Møller has provided evidence in support of this sexy and the potential for considerable variation. In such a
sons hypothesis by demonstrating that female Barn population out-breeding may risk the loss of genes
Swallows Hirundo rustica find males who have long and gene complexes that are adapted to local condi-
tail streamers particularly attractive and are more tions. These apparently contradictory situations (Blue
likely to attempt to secure EPCs with long-tailed Tits minimizing in-breeding and American Redstarts
males if their own mate has a shorter tail. More minimizing out-breeding) suggest that different
recently however advances in molecular ecology and populations (relatively closed versus relatively open)
genetics have enabled us to investigate the incidence require different strategies to optimize out-breeding.
and consequences of genetic compatibility and
incompatibility in birds. For example, research car- Key reference
ried out by Katharina Foerster and her colleagues Foerster, K., Delhey, K.J., Lifeld, J.T., and Kempenaers, B.
has shown that the extra-pair offspring of Blue (2003) Females increase offspring heterozygosity and
Tits Cyanistes caeruleus are more heterozygous than fitness through extra-pair matings. Nature 425, 714–17.
within-pair offspring and that they exhibit higher Hajdasz, A., McKellar, A.E., Ratcliffe, L.M., et al. (2019)
levels of fitness. This suggests that female Blue Tits Extra-pair offspring are less heterozygous than within-pair
who have genetically similar mates seek out EPCs offspring in American redstarts Setophaga ruticilla.
Journal of Avian Biology 50: doi:10.1111/jav.02084
to increase the genetic diversity of their offspring.
Møller, A.P. (1988) Female choice for male sexual tail
In contrast however Adrianne Hajdasz and her col-
ornaments in the monogamous swallow. Nature 332
leagues have demonstrated that female American (6165), 640–2.
Redstarts Setophaga ruticilla paired with a genetically
Box 5.2 Leks
A lek site is the traditional location at which a group of The hot-spot hypothesis suggests that leks of males form
males come together to compete and display to visiting in particular locations that are regularly visited by the
females. As a system lekking, as the behaviour is termed, females in a population. This would maximize the chances
is rare but it has evolved several times and is found in a that males would encounter potential mates. Some support
number of bird groups. for this hypothesis does come from the observation that males
Lekking is an unusual mating system in that males are typically choose particular habitat features when establish-
chosen by the females as mates but they do not then provide ing a display arena. Male Houbara Bustard Chlamydotis
any parental care or any direct territorial/resource benefit. undulata choose to lek in open areas where their displays
The females gain nothing other than the genes that their can be seen by females who more typically inhabit dry wadis
offspring will inherit. One of the features of a lek is that mat- and scrubby cover. On the other hand, the locations of the
ings are actually achieved by relatively few (sometimes only leks of Blue-crowned Manakin Lepidothrix coronata have
one) of the males that are present. This fact has been viewed been shown to be at sites no more likely to be visited than
as something of a paradox, the question being asked if most any other areas of their range. Similarly when the dominant
males will not mate why do they attend the lek? In an Great Snipe Gallinago media is removed from its position at
attempt to resolve this paradox four main hypotheses the centre of a lek its place is not occupied by another bird,
have been proposed: hot-spots, hot-shots, kin selection and instead the lek collapsed. This suggests that in this case hot-
female preference. shots rather than hot-spots are significant. The hot-shot
REPRODUCTION 99
hypothesis suggests that inferior males cluster around a quality males. If this were the case then we would expect to
superior a male hoping to gain access to at least some of the see a female preference for larger rather than smaller leks
females attracted to him and in some species it has been and exactly this result has been obtained through observa-
shown that those males with a territory/lek position close to tion of Little Bustard Tetrax tetrax lek sites.
the alpha bird do have better breeding success than those Interestingly it has been suggested that leks might not be
on the fringes of the lek. so far removed from conventional territorial breeding sys-
The kin selection hypothesis suggests that leks are com- tems as was previously thought and it has been suggested
posed of related males in effect cooperating to attract that clusters of territories may act as ‘hidden leks’ clustered
females and gaining an indirect fitness benefit when genes around a high quality male or location (hot-shot or hot-
that they have in common with a more successful relative spot), clustered around a group of related males (kin-
are inherited by his offspring. It has been shown that captive selection) or to facilitate female comparison of males
male Peacock Pavo cristatus reared in isolation tend to form (female-preference).
leks with relatives, but lek mates have been shown to be
unrelated in a number of other species including several Further reading
of the manakins Pipidae and the Greater Sage Grouse Fletcher, R.J. and Miller, C.W. (2006) On the evolution of hid-
Centrocercus urophasionus. den leks and the implications for reproductive and habitat
As an alternative the female preference hypothesis sug- selection behaviours. Animal Behaviour 71(5), 1247–51.
gests that leks form as a result of females seeking out larger Högland, J. and Alato, R.V. (1995) Leks. Princeton University
groups of males in order to compare them and secure high Press, Princeton.
5.3 Courtship and mate choice behaviour of their mates. Jon Brommer and his col-
leagues have demonstrated one such effect through
As the ‘rarer’ sex females are most often the choos- their study of a Finnish Tawny Owl Strix aluco popu-
ier sex (see Boxes 5.2 and 5.3) but how do birds lation. They found that females who had chosen to
attract a mate? Males of many species sing repeti- mate with larger males were more likely to lay their
tive or complex songs that are energetically costly eggs earlier in the breeding season. This could, they
to produce and may expose them to predators. suggest, be related to the possibility that larger
Others sport elaborate ornamentation, think of the males provide more food for their mates during the
fanned tail of the male Indian Peacock Pavo cristatus pre-laying courtship-feeding period. Interestingly
for example. Male bowerbirds create bowers in although male owls continue to feed their mates
carefully maintained arenas that they decorate with during the incubation period, they did not find a
colourful objects, and the males of some species of relationship between male size and clutch size, in
raptor carry out apparently death defying acrobat- spite of the fact that earlier clutches do tend to be
ics diving and tumbling downwards through the larger. This suggests that clutch size is a trait deter-
sky. Some males defend a territory, a space in which mined by the female (see chapter 4, section 4.3).
a brood of chicks could be successfully raised;
others provide a female with gifts of food. Whatever Flight path: females vary their clutch sizes in relation
the method of courtship these behaviours enable to environmental factors, page 78.
members of the choosing sex to discriminate in
some way between potential suitors. Females of Key reference
some species make the choice on the basis of the Brommer, J.E., Karell, P., Aaltonen, E., et al. (2015)
promise of a resource communicated by a signal Dissecting direct and indirect parental effects in a wild
whereas the females of other species seem to be bird of prey: dad affects when but not how much.
making the choice on the basis of the signal itself. Behavioural Ecology and Sociobiology 69(2), 293–302.
5.3.1 Resource provision Great Grey Shrikes Lanius excubitor (Figure 5.3) are
socially monogamous, raptor-like passerines that
Through their courtship behaviour male birds form territorial breeding pairs. It is usual for both
can have an indirect effect upon the reproductive male and female to contribute to the raising of their
mate). Cheating females benefit from these EPCs

because they have an opportunity to mate with
high quality males (presumably males of higher
quality than their own mates). Their cuckolded
partners however do lose out because they will
invest resources raising the chicks of a rival male.
However it would be quite wrong to think of these
hapless males as being unable to avoid the costs
associated with promiscuity and there is abundant
evidence that males do their utmost to avoid being
the ‘victims’ of EPCs.
Francisco Valera and co-workers have made simi-
Figure 5.3 Great Grey Shrike Lanius excubitor (© Ian Robinson). larly detailed observations of the breeding behaviour
of a population of Lesser Grey Shrikes Lanius minor,
young. Male shrikes are well known for their habit of a close relative of the Great Grey and another butcher
impaling food items (large insects, small mammals, bird that uses food as a nuptial gift. They noted that
birds, and reptiles) on thorns or barbed wire fences, a territorial intrusions by males, that they presumed to
habit that has earned them the title butcher birds. The be actively seeking EPCs, were seven times more
quality of this larder, the size and nutritional value of common during the fertile period of the resident
the food it contains, has been shown experimentally female. During this period the resident male was
to be one of the key factors used by a female when she particularly attentive to his mate, spending almost 80
chooses her mate. Larger prey items are presumed to per cent of his time within 50 m of her. He was also
require a greater effort on the part of the male in terms particularly aggressive towards male intruders,
of his ability to capture them and the energy that he attacking them and chasing them away. So mate
expends manipulating them; they are therefore likely guarding seems to be an effective EPC minimization
to be an indicator of his physical quality. strategy. But what about the 20 per cent of the time
I said earlier that these shrikes are socially monog- he didn’t guard his mate? To find out what would
amous. Remember that in saying this I mean that happen if males had apparent reason to suspect that
two birds (one of each sex) form a breeding pair that an EPC had occurred the researchers captured
rears young together. You should also remember females during their fertile period and removed
however that this does not imply that these birds are them from their territory for one hour. They then
necessarily faithful to one another. Great Grey Shrike released them back into an adjacent territory so that
males do cuckold their neighbours, fertilizing an when they returned to their mate it would appear
egg that is raised by an unsuspecting foster parent. that they had visited his rival. Males responded to
But why do the females take part in these promiscu- this apparent infidelity by punishing their mate,
ous liaisons, surely they have a suitable mate? Piotr attacking her and in many cases aggressively forcing
Tryjanowski and Martin Hromada have made copulation. Such retaliatory copulations are of course
detailed observations of a population of these birds an important paternity assurance strategy (see
and have shown that in fact the males effectively Box 5.1). The same did not however happen if the
pay for sex with already mated females by provid- removal had taken place outside of the fertile period
ing them with choice items of food from the larders (during incubation or chick rearing for example).
that initially impressed their own mates. There is also a suggestion that unlike males the
Their data (Figure 5.4) show that males are more females in this population are reluctant to seek EPCs,
likely to be successful when they offer a female a they rarely leave their territory during their fertile
better gift, and that they tend to offer the best phase even if their male has been temporarily
gifts (the most energetically valuable) to their ‘mis- removed. Genetic paternity analysis has revealed
tresses’. These gifts they estimate to contribute 66 that male mate guarding and female punishment are
per cent of the daily food requirement of a female an effective strategy in the case of this species because
(compared to the 16 per cent they provide their mixed paternity broods are extremely rare.
REPRODUCTION 101
14
12
Number of prey items
10
6
Figure 5.4 Male Great Grey Shrikes provide more (and
4 better) gifts when seeking extra-pair copulations (solid bars)
than when seeking to mate with their partner (open bars).
2 Tryjanowski, P. and Hromada, M. (2004) Do males of the great
0 grey shrike Lanius excubitor, trade food for extra-pair
Birds Voles Lizards Insects Without gift copulations? Animal Behaviour 69, 529–33.
no net change in length (this was done as an experi-

Key reference mental control). Another group had a 25 cm long
Valera F., Hoi, H., and Krištín, A. (2003) Male shrikes section of their tail removed and the tip was re-
punish unfaithful females. Behavioural Ecology 14(3),
joined to the base—thereby shortening the tail.
403–8.
These 25 cm long removed sections were inserted
into the cut tails of the final experimental group,
thereby lengthening their tails. Andersson then
5.3.2 Ornaments and displays released the birds back into their territories and
Male Long-tailed Widowbirds Euplectes progne recorded the number of additional nests that each
have, as their name suggests, an extremely long tail. bird built (a measure of the number of additional
In fact this 15–20 cm long bird can have a tail around females attracted to him). The results (Figure 5.5A)
50 cm long during the breeding season. We saw in show clearly that males with the longest tails attract
chapter 2 that feathers can be expensive and there the most mates.
must surely be an aerodynamic cost to be paid However, the results of another tail lengthening
when towing a streamer this long. So why do these experiment carried out by Sarah Pryke and Staffan
males have such a long tail? It seems to have Andersson (Figure 5.5B) provide an intriguing
evolved as a result of sexual selection because there insight into the basis of the evolution of this court-
is good experimental evidence of a link between tail ship signal. They manipulated the tails of a relatively
length, male reproductive success, and female short-tailed species, the Red-shouldered Widowbird
choice. Simply put, females want males with long Euplectes axillaries. Males of this species are slightly
tails. The evidence for this comes from a particularly smaller than male Long tailed Widowbirds but they
elegant experiment carried out by ornithologist Malte have very much shorter tails (around 7 cm long).
Andersson who captured males and artificially When these tails were artificially lengthened (in
elongated or shortened their tails and then observed some cases to 22 cm long) males attracted as many
the effect that this had upon their subsequent repro- as six females; three times as many as the longest
ductive success. Long-tailed Widowbirds are polyg- tailed unmanipulated individual. So it seems that
amous. Males defend an area of grassland from female widow birds have a generalized preference
other males and advertise their presence to females for longer tails, and that this sensory bias has driven
by means of a conspicuous, bouncing display the evolution of the extraordinarily long tails of
flight—showing off their tails to good effect. Each some species.
male attempts to attract a harem of females to his
territory, all of whom will rear his young (assuming
5.3.3 Sharing a mate
no EPCs take place of course) without his assist-
ance. Andersson trapped male birds and assigned Both male and female Dunnock Prunella modularis
them randomly to three groups. One set of birds seem content to share their mates under some cir-
had their tail feathers cut in half and re-joined with cumstances (see Box 5.4). Female widowbirds seem
(A)
2
Mean number of new

nests per male
1
0
Shortened Control Elongated
Tail treatment
(B) 7
120
Natural tail frequency
6
80
Mean number of active nests
5
40
4
0
3
0 2 4 6 7 8 10 12 14 16 18 20 22
Manipulated tail length (cm)
Figure 5.5 The relationship between male tail length and reproductive success in the Long-tailed Widowbird (A) and the short-tailed
Red-shouldered Widowbird (B). From (A) Andersson M (1982) Female choice selects for extreme tail length in a widowbird. Nature 299, 818–20;
(B) Pryke, S.R. and Andersson, S. (2002) A generalized female bias for long tails in the short-tailed widowbird. Proceedings of the Royal Society
B: Biological Sciences 269, 2146.
content to share their male with others in his harem. monogamous one. This model assumes that females
This is probably because all they require of him are should prefer monogamy because there will be a
his genes and access to the resources available in his cost to polygamy and that females should only
territory. They rear their young without his assistance. accept polygamy when the benefits of that relation-
In some species however polygyny appears to result ship outweigh its costs relative to monogamy with
in reduced reproductive success for at least some of an available unmated male. The point at which this
the females involved. So why do they accept it? economic decision is made is the polygamy thresh-
In 1969 Gordon Orians published a very influen- old (see Figure 5.6).
tial paper in which he proposed a mathematical
model to explain female acceptance of polygyny. In Key reference
his polygyny threshold model (PTM) Orians envi- Orians, G.H. (1960) On the evolution of mating
sioned a situation in which females would sample systems in birds and mammals. American Naturalist
and compare the territories of available males and 104, 589–603.
then using the information that they have gathered,
elect to join an already mated male in a polygamous Do female birds really behave in a manner consist-
relationship, or to settle with an unmated male in a ent with the PTM? Stanislav Pribil and William
REPRODUCTION 103
Box 5.3 Turning the tables: reproductive role reversal in the Spotted Sandpiper
In the vast majority of bird species males compete with one with the emergence of a superabundance of insect food and
another for the attentions of choosier females and females because newly hatched sandpipers are precocial (able to
are able to make the most of good males and favourable thermoregulate and fend for themselves from hatching).
breeding conditions by varying the numbers of eggs that are Furthermore, the system works because males are slightly
laid in a clutch. The Spotted Sandpiper Actitis macularis is an more common in the population than females and so after
interesting exception to this rule. Female Spotted Sandpipers abandoning their first mate, females are able to secure a
always lay four eggs in a clutch. Unable to vary their clutch second and lay a second clutch of eggs to be reared by him.
size, the only way that they could increase their output in a The first males to pair up clearly benefit because they
good year would therefore be to lay a second clutch of four have secured for their offspring the genes of the best females
eggs. However, the sandpiper breeding season is a short one and because the best that they can do is secure for them-
and it is doubtful that a female could manage to rear one selves a clutch of four eggs. But do the females compromise
brood of chicks to fledging and then have time to rear a the quality of their offspring when they take a second male?
second before migrating. After all these are the males that were ‘left on the shelf’ first
Faced with these difficulties female Spotted Sandpipers time around and so are presumably inferior in some way. In
employ an interesting strategy—they act like males. Females fact DNA paternity analysis has revealed that second brood
arrive on the summer breeding grounds first and compete chicks are often fertilized by first male sperm that have been
with one another to secure territories. When the males do stored by the female, in this way females are able to make
arrive the females actively court them and the ‘best’ females the most of the genetic resources available to them.
secure mates quickly and lay a clutch of four eggs.
When resources allow it the females of some populations Further reading
then abandon their newly laid eggs leaving their mate to Oring, L.W., Fleischer, R.C., Reed, J.M., and Marsden, K.E.
incubate and rear the brood alone. Males are only able to do (1992) Cuckoldry through stored sperm in the sequen-
this because the sandpipers time their breeding to coincide tially polyandrous spotted sandpiper. Nature 359, 631–3.
(A) (B) Monogamous

Female reproductive success
c
2nd
A polygyny Figure 5.6 The polygyny threshold model. The model
presumes that females have choice and can choose to pair
PT
? with already mated or unmated males (A). Female
reproductive success varies according to the quality of the
B territory of the male chosen. If a female can gain more by
choosing an already mated male than she can by choosing a
single bird, then she should choose polygamy over
monogamy (B). From Scott G.W. (2005) Essential Animal
B A Behavior. Blackwell Science, Oxford; adapted from Orians,
Territory quality G.H. (1969) On the evolution of mating systems in birds and
or quantity of breeding situation mammals. American Naturalist 104, 589–603.
Searcy have demonstrated experimentally that in ritory of the male, and, iii) that faced with a choice
the case of at least one species, the Red-winged between a low quality monogamous male/territory
Blackbird Aegaius phoecniceus, they do. The PTM and a high quality polygamous male/territory,
makes a number of testable assumptions: i) that females will choose polygamy (if the cost of polyg-
polygamy is costly to females, so they prefer amy is lower than the cost of choosing monogamy
monogamy, ii) that females choose males on the in this situation). Through their observations and
basis of either male quality or the quality of the ter- experiments Pribil and Searcy have shown that all
three of these assumptions are met in the case of field-based experiment in which they manipulated
their Red-winged Blackbird study populations. the choices available to females. In it they compared
the attractiveness to females of males whose terri-
Key references tories were manipulated such that one in each pair
Pribil, S. (2000) Experimental evidence for the cost of offered an unmated male with no over-water nest
polygyny in the red-winged blackbird Agelaius site while the other offered a high quality nest
phoeniceus. Behaviour 137, 1153–73. (over-water, see Figure 5.7) that was occupied by an
Pribil, S. and Searcy, W.A. (2001) Experimental already mated male. In almost all cases newly arriv-
confirmation of the polygyny threshold model for
ing females chose polygyny rather than monogamy,
red-winged blackbirds. Proceedings of the Royal
exactly as would be predicted by the PTM.
Society of London B 268, 1643–6.
Pribil began by confirming the first prediction of the (A)

model when he demonstrated that female Red-
winged Blackbirds suffered a reproductive cost if they
chose to mate with an already mated male; he found
that they fledged fewer and lighter young. This obser-
vation is important because survival to maturity in
this and many species is significantly correlated with
fledging weight; heavier birds survive better. As
(B)
would be predicted from these results he also showed
that when offered the choice of two males, one with a
mate and one without, experimental females invari-
ably chose to enter into a monogamous relationship.
When they have the choice, female Red-winged
Blackbirds also discriminate between males on the
basis of territory quality (the second of the model’s
predictions). They will preferentially mate with an
unmated male controlling a territory that offers the
opportunity to build a nest overhanging water (pre-
sumably because such nests offer enhanced protec-
tion from predators).
To test the model’s third and perhaps most sig-
nificant prediction; that faced with a choice between
a low quality monogamous male/territory and a
high quality polygamous male/territory, females
Figure 5.7 (a) Male Red-winged Blackbird Aegaius phoecniceus
will choose polygamy (if the cost of polygamy is (© Ian Robinson). (b) This Red-winged Blackbird nest was built on a
lower than the cost of choosing monogamy in this platform designed by Searcy and Pribil to provide females with high
situation) Pribil and Searcy designed an elegant quality over-water nest sites (© Stanislav Pribil).
Box 5.4 The Dunnock: a case study in sexual conflict
Within a single population of the Dunnock it is possible Cambridge University colleagues is quite possibly one of
to recognize genetic monogamy, social monogamy, the best, and best-known, case studies of bird breeding
polygyny, polyandry, and even polygynandry. As a conse- behaviour.
quence, the study of the reproductive behaviour of this Central to the system is sexual conflict, the conflict of
otherwise unobtrusive bird by Nick Davies and his interests of males and females. Figure 5.8 summarizes the
REPRODUCTION 105
benefits and costs of each system (in terms of chicks pro- average. Primary males therefore attempt to drive away
duced) to both males and females. secondary males.
Taking monogamy as a starting point, males and females A similar state of affairs exists in the case of males in that they
both benefit equally—raising 5 young each (assuming that can do considerably better if they persuade a second female to
this is genetic and social monogamy). But note that a join them in a polgynous group, and if polyandry is inevitable
female can improve upon this situation if she persuades a then by attracting another female to change a polyandrous
secondary male to join a polyandrous group—she will raise group into a polygynandrous one he can at least not lose out.
6.7 chicks, and the secondary male benefits because rather The actual system that is established will represent a
than have none he will have sired 3 chicks. Female Dunnocks compromise on the part of one or all of the parties involved
regularly court males in an attempt to benefit in this way. and of course through EPCs and EPC counter measures the
However, this arrangement clearly does not benefit the pri- actual genetic composition of broods may be even more
mary male, rather than siring 5 chicks he sires just 3.7 on complicated than even Figure 5.8 would suggest.
Monogamy
=5
=5
= 7.6
= 3.8 = 3.8 b = 3.0 = 6.7 a = 3.7
Polygyny Polyandry
a
a =5 Figure 5.8 The complex mating system of the

Dunnock. Several scenarios are illustrated and in each
= 3.6 case the average number of young produced per
b = 2.2 = 3.6
individual is given. See text for detailed explanation.
From Davies, N.B. (1992) Dunnock Behaviour and Social
Polygynandry Evolution. Oxford University Press, Oxford.
Bird song is produced when air passes through

5.4 Song
the syrinx, the avian equivalent of the human
Male birds of a number of species sing a courtship voice box. The variations in song that we hear are
song to attract a mate and as a form of resource a result of the carefully controlled contraction of
defence (Figure 5.9). We will consider both of these the muscles and membranes of the syrinx, which
functions of song below, but first we should con- are in turn controlled by nervous signals originat-
sider the song and singing behaviour itself. We ing in a clearly defined area of the hindbrain,
should also note that only three groups of birds termed the tracheosyringeal motor nucleus (often
(the songbirds, the hummingbirds, and the parrots) referred to as nXIIts). Singing is triggered by a
have the capacity to learn and reproduce new wide range of environmental stimuli (by environ-
sounds. The vocalizations of all other birds groups ment here I mean both the environment external to
are innate and inherited from their parents. the bird—the physical and social environment,
effect has yet to be confirmed). As the male HVC

develops, it forms two major projections, one of
which connects it to an area of the hindbrain termed
RA (the Robust nucleus of the Arcopallium) that is
involved in the production of learned sounds and is
part of the same control pathway as nXIIts. In female
brains, the HVC-RA pathway does not develop. The
other projection is to the enigmatically labelled fore-
brain Area X, which is associated with song learning
and to which I will return later in this chapter.
Key references
Figure 5.9 This male Whitethroat Sylvia communis is in full song,
Chen, X., Agate, R.J., Itoh, Y., and Arnold, A.P. (2005)
proclaiming ownership of a territory and availability to mate (© Ian
Sexually dimorphic expression of trkB, a Z-linked gene,
Robinson).
in early posthatch zebra finch brain. Proceedings of
the National Academy of Sciences of the USA
and the bird’s internal environment—the particular 102(21), 7730–5.
Marler, P. and Slabbekoorn, H. (2004) Nature’s Music:
hormones in its bloodstream etc.). However, song
The Science of Birdsong. Elsevier, San Diego.
production is under the control of a specific cluster
of brain cells termed the High Vocal Centre (HVC)
from which neuronal signals propagate through a
5.4.1 Song learning
pathway involving specific areas of the fore, mid,
and hindbrain, ultimately connecting with nXIIts Song production is innate in that males reared in
and the syrinx. The details of this pathway are isolation will sing at maturity. However, singing the
beyond the scope of an introductory text such as right song seems to largely depend upon a male
this, but if interested readers did want to know learning from an appropriate tutor. (Although it
more the excellent book Nature’s Music by Peter has been recently shown that in the Reed Warbler
Marler and Hans Slabbekoorn would be a very Acrocephalus schoenobaenus birds reared in isolation
good place to start. can mature to sing normally). Birds learn songs in a
The HVC of male songbirds is significantly more variety of ways. Some such as the White-crowned
developed than that of female birds and this differ- Sparrow Zonotrichia leucophrys can only learn their
ence is initiated at an early stage in the development songs during a very short period of their early lives
of the brain. But what exactly triggers this sexual dif- (often referred to as a sensitive period). In the
ference in the neurological basis of song has been a Chaffinch Fringilla coelebs this sensitive period is
mystery. Recently however Xuqi Chen and col- longer (lasting for the whole of the first year of a
leagues have reported that HVC development in the bird’s life). Such birds are termed closed-ended
brain of the male Zebra Finch Taeniopygia guttata is learners or age-limited learners. On the other hand
temporally linked to the expression of a Z-linked males of some species such as the Willow Warbler
gene which codes for the protein tyrosine kinase Phylloscopus trochilus are able to learn new songs
receptor B (trkB) which acts as a receptor for a neuro- and add to their repertoires throughout their lives.
transmitter termed BDNF. BDNF in turn is known to The various mechanisms by which song learn-
be involved in the differentiation of brain cells and in ing takes place are proving to be more variable
the development on the HVC in particular. As we than was originally thought to be the case and I would
might reasonably expect male birds have far higher recommend that the interested reader consult the
trkB levels, having twice as many trkB Z-linked excellent review of the topic by Beecher and Brenowitz.
genes than females. Thus a direct link between a sex- However, the basic model of learning seems to include
linked gene and a sex-specific behaviour has been three steps: a preliminary sensory acquisition phase, a
established (although the exact mechanism for its silent phase, and finally a sensorimotor phase.
REPRODUCTION 107
be perfect but it will be a very close approximation of

Key references the song typical of the species. Through time (and
Beecher, M.D. and Brenowitz, E.A. (2005) Functional actually very quickly) the song is refined until it is
aspects of song learning in songbirds. Trends in perfected or crystallized. It seems that hearing one-
Ecology and Evolution 20(3), 143–9.
self is crucial at this time and that birds match the
Wheelwright, N., Swett, M.B., Levin, I.I., et al. (2008)
songs that they produce against their now completed
The influence of different tutor types on song learning
in a natural bird population. Animal Behaviour 75, internal template. But how does the bird know that it
1479–93. is getting it right? Jesse Goldberg, Vikram Gadagkar,
and their colleagues have demonstrated that Area X,
Young birds seem to have an innate template that that part of the forebrain that is connected to the
can be modified to some degree by a process of HVC is crucial to the development of the correct
learning. During the first phase of song develop- song. As a ‘practising’ bird develops its song it can
ment (the sensory acquisition phase which equates essentially sing two types of note—the right ones
to the sensitive period) a young bird will hear a wide and the wrong ones. By recording the activity of the
range of noises but evidence suggests that they are neurons of a the ventral tegmental area (VTA), which
most sensitive to the song that most closely matches project to Area X, the Goldberg group determined
their own innate template—the song of a suitable that VTA neurons had an inhibitory effect on brain
conspecific tutor. In some cases such as the Zebra activity when the bird produced an incorrect note,
Finch Taenoipygia guttata and galapagos finches but when the right note was produced they stimu-
Geospizidae the tutors are always, or almost always, lated a dopamine response. In essence the bird was
the rearing male parent. In others however the song rewarded, and when it eventually perfected a note
that a bird learns is not a complete copy of that of its that it had struggled with for some time, the level of
father. In a study of a wild population of Savannah the dopamine reward was larger. It would seem
Sparrow Passerculus sandwichensis Nathaniel Wheel- therefore that the VTA neurons act as a sort of internal
wright and colleagues have shown that males in critic, using a reward to reinforce success.
their study population developed a song similar to
(but not the same as) that of their social father in Key reference
only 12 per cent of cases, the majority of the popula- Gadagkar, V., Puzerey, P.A., Chen, R., et al. (2016)
tion learning a song more similar to that of their Dopamine neurons encode performance error in
singing birds. Neuroscience 35, 12–82.
neighbours. Their results also suggest that in this
population individuals incorporate elements of
song from a number of tutors into their repertoire.
5.4.2 Functions of song
During this learning phase it appears that a bird
memorizes aspects of tutor song and uses them to Bird song has two primary functions. It is used pri-
refine its original innate template thereby producing marily by male birds as both a courtship signal to
a more exact one that conforms to the specific song attract mates and as a signal to other males that a
pattern of its species. Some birds in isolation will territory is occupied (see Box 5.5). Artificially muted
learn from a recording but learning does appear to be male birds in a number of studies have been shown
enhanced when a live tutor is present and in some to be unable to either gain territories or attract
cases, such as the Zebra Finch, a live tutor is essen- mates. Recently, experimental evidence has been
tial. After song acquisition there follows a silent provided suggesting that male birds evaluate their
phase when singing is not taking place but during rivals based upon the songs they sing. Samuel
which the components of song that the bird has Hill and his co-workers have carried out playback
learned are stored for future use. Prior to the onset of experiments to explore the responses of territorial
the breeding season (when the testes regenerate) tes- male Tui Prosthemadera novaeseelandaie (a New
tosterone triggers singing and the final phase of song Zealand endemic) to recordings of songs of increas-
acquisition, the sensorimotor phase, occurs. Now the ing complexity. Their results demonstrate that males
bird sings. Initially the song that is produced will not approach, and respond to, more complex songs
Box 5.5 What’s in a song?
European Starlings Sturnus vulgaris have been described as 90 per cent of the males were attracted to the simple song. So
being amongst the most accomplished of singers. Males it would seem that a complex song would benefit a male
have extremely varied repertoires and sing for prolonged because it would attract females and deter male rivals.
periods during their breeding season. To demonstrate that Further evidence that female starlings consider males
their song has both a female attractant and male deterrent with a complex song to be higher quality comes from
function, James Mountjoy and Robert Lemon studied a wild another piece of research carried out by Mountjoy and
population of starlings (breeding readily in nest-boxes). To Lemon. They made further detailed observations of their
see if the birds would be attracted to it, starling song was study population, this time recording the complexity of the
played from some of the boxes. As a control, and for com- song of individual males during the courtship period and
parison, each box was paired with a second, from which no then noting the date at which the first egg was laid in the
song was broadcast. Throughout their observation period boxes occupied by each of these males. Their prediction was
the team saw no female starlings at silent boxes, but they that the males with the most complex songs would be in
saw 12 investigating the boxes from which song was being the best condition and would therefore be the most attract-
broadcast. The song was evidently attractive to them. We ive to the females. The females should therefore be pre-
might have expected male starlings to behave differently— pared to commit to pair with and lay eggs with these males
given that we assume song to serve as a deterrent to rivals preferentially.
but in fact of 20 birds seen at boxes, 17 were investigating From Figure 5.10A it is clear that a positive relationship
the ones with a playback. So is song a deterrent to rival between song complexity and body condition (in this case
males in this species? A further refinement of the experiment an expression of size and mass) exists—fitter birds are bet-
showed that it is. ter singers. As would be predicted Figure 5.10B shows that
In a second experiment they paired boxes with a playback females paired to males with the biggest repertoires lay eggs
of a very simple starling song with boxes playing a very com- sooner than those that pair to poorer males. Research car-
plex one. This time the sexes did behave differently. All of the ried out by Deborah Duffy and Gregory Ball has revealed
females observed were attracted to the complex song whereas another potentially important indication that song could be
(A) 55 (B) 30
50
24
Delay until first egg (days)
45
Repertoire size
40
18
35
30
11
25
20 5
–0.06 –0.04 –0.02 0.00 0.02 0.04 0.06 20 26 32 38 43 49 55
Condition Repertoire size
Figure 5.10 A The relationship between male starling song repertoire size and body condition of male; and, Figure 5.10B The relationship
between male starling song repertoire size and delay until the laying of the first egg. From Mountjoy, D.J. and Lemon, R.E. (1996) Female
choice for complex song in the European Starling: a field experiment. Behavioural Ecology and Sociobiology 38, 65–71, by permission of
Oxford University Press.
REPRODUCTION 109
used by female starlings to assess the quality of potential In both cases their results demonstrated clearly that better
mates (and presumably therefore to influence the potential singers had the most robust immune system.
quality of their eventual offspring). They have demonstrated
a correlation between the male song variables bout length References
(the mean length of a single song) and singing rate (the Duffy, L.D., and Ball, G.F. (2001) Song predicts immunocom-
mean number of times a bird sings in an hour) and two petence in male European starlings (Sturnus vulgaris).
measures of the strength of the immune system of the birds. Proceedings of the Royal Society Series B. 269, 847–52.
more quickly and more aggressively in comparison singing rate. Presumably he is attempting to replace
to their responses to simple songs. This suggests his ‘lost’ mate. Similarly males may increase their
that these males perceive a complex song (and pre- singing behaviour while their mate incubates their
sumably therefore a bird that sings it) as being more clutch of eggs. Presumably these birds are attempt-
of a threat and the researchers have speculated that ing to attract a second mate or to secure EPCs. Dag
song complexity may therefore communicate infor- Eriksson and Lars Wallin have demonstrated very
mation about the quality, attractiveness to females, clearly that male song attracts females in the case of
and/or territorial intentions of an individual. both the Collared Flycatcher Ficedula hypoleuca and
Although reports of female song are rare, some the Pied Flycatcher Ficedula albicollis. These birds
female birds have been observed singing in behav- nest readily in nest-boxes and the boxes can be used
ioural contexts that suggest they too use song to to trap birds that enter them (trapped birds are
defend territories and mates. For example Dustin released unharmed very quickly). The researchers
Reichard and his colleagues have recorded female arranged 28 nest-boxes throughout their study
Dark-eyed Junco Hyemalis thurberi in a Californian population, each box having a model flycatcher
urban population singing a male-like song (but about 1 m from it on a prominent perch (live fly-
across a narrower frequency range) when they and catcher males usually sing from such perches pre-
their male partner are exposed to the presence of a sumably to attract females to them). From half of
potential female rival. the boxes they played the song of the same species
as the male model perched outside. The other half
Key references of the boxes were silent. The results of this study
Reichard, D.G., Brothers, D.E., George, S.E., et al. clearly show that females were far more likely to
(2018) Female Dark-eyed Juncos (Junco Hyemalis inspect the boxes of singing males and song can
thurberi) produce male-like song in a territorial therefore be presumed to have attracted them to the
context during the early breeding season. Journal of
territory and persuaded them that the nest-box
Avian Biology 49(2), 1–6.
might make a suitable home. Of the female flycatch-
Hill, S.D., Brunton, D.H., Anderson, M.G., and Ji, W.
(2018) Fighting talk: complex song elicits more ers trapped whilst inspecting nest-boxes, 90 per
aggressive responses in a vocally complex songbird. cent were attracted to those boxes having both a
Ibis 160, 257–68. model male and a recording of his song.
The temporal coincidence of male singing behav- Key reference

iour and the onset of reproductive behaviour is in Eriksson, D. and Wallin, L. (1986) Male bird song
itself highly suggestive that singing has a courtship attracts females—a field experiment. Behavioural
function and evidence that this is the case comes Ecology and Sociobiology 19, 297–9.
from a range of field and laboratory studies. Singing
rates of territorial males have been shown to be Females are able to discriminate between males on
higher before a female joins a male on his territory the basis of their songs, preferring some song types
than they are once the pair is established. However, over others. Female dunnocks for example have
if a female is temporarily removed from the terri- been shown to pay more attention to a recording of
tory, the resident male responds by increasing his the song of their mate when he has been removed
than to the song of a neighbour. Furthermore this is one another and identify vacant territories. Tobias
particularly the case during the female’s fertile Roth and his colleagues have radio tracked female
period suggesting that she uses her mate’s song as a nightingales and recorded male singing behaviour.
way of finding him to seek out copulations. They found that during the early part of the breeding
season (before females migrate into their breeding
areas) males sing most at dawn (although famously
5.4.3 Synchronized singing they do of course sing all night) (Figure 5.11A). Once
Although the songs of individuals of a species do the females arrive, paired males continue to be most
vary, often markedly, a consequence of birds learn- vocal towards the end of the night and at dawn
ing from those around them may be that all of the (Figure 5.11B), but bachelor males increase their sing-
birds in an area develop a broadly similar reper- ing throughout the night. Radio tracked females
toire. This seems to be an advantage in some cases (released into the area by the researchers to simulate
and males are known to match their repertoires dur- new arrivals) were found to be most mobile at night
ing singing contests. In some situations it appears (Figure 5.11C). Roth and his co-workers interpret
that singing a similar song to that of a rival can these observations as follows. They suggest that
reveal to him that you are a familiar neighbour and newly arrived females visit several males over the
may therefore be tolerated. On the other hand, a course of a night, listening to the song of each of
song repertoire that is different is more likely to be them prior to choosing a mate (this is why bachelors
responded to aggressively because it reveals the rather than paired males sing at this time). At dawn
singer to be an unknown intruder and therefore to the females become inactive and the function of
be a greater potential threat. singing switches from mate attraction to territorial
Song matching however, the singing of the same defence (all male territory holders sing at this time).
song as a rival at the same time as a rival, and the A further advantage of synchronized singing may
overlapping of singing bouts between rivals does be that it helps the birds of an area to synchronize the
appear to be a particularly aggressive signal in some rest of their reproductive behaviour. Doing so could
species, even between neighbours. Birds matching or be an advantage in that synchronized production of
overlapping in this way are more likely to escalate young may swamp local predator populations with
their contest to a full-blown fight. Perhaps not sur- prey and thereby ensure survival of a greater propor-
prisingly these contests are more common between tion of young birds and increase individual survival
strangers or between neighbouring birds that are probability of each chick. It may also enable sharing
establishing territories at the start of a breeding sea- of nest/chick defence activity and improve the effi-
son than between established territorial neighbours. ciency of foraging parents (if they are able to feed as
Perhaps to facilitate comparison, the males of flock mates with other foraging parents). In the case
many populations of birds synchronize their singing of Zebra Finch Taeniopygia guttata Joseph Wass and
behaviour; the dawn chorus being perhaps the his colleagues have shown that exposure to the
most familiar example of this phenomenon. The still, sounds of a breeding colony of finches (including
dawn air enhances sound transmission, and it has male courtship song) caused male Zebra Finches to
been suggested that low light levels and low air increase their own singing rate (particularly if the
temperatures at dawn make other behaviours less sounds were recorded from their own colony). They
possible (feeding on insects for example). There also found that females were more synchronous in
may also be less interference from noise pollution at their egg laying when they were played colony
dawn (see Box 5.6). Perhaps overnight mortality is sounds and they produced larger clutches of eggs.
high and singing at dawn allows males to identify
gaps between territories? Or perhaps a synchronized
Key reference
chorus simply makes it easier for males to compete
Wass, J.R., Colgan, P.W., and Boag, P.T. (2005) Playback
with one another and for females to compare them.
of colony sound alters the breeding schedule and
Evidence from radio tracking has revealed that in the
clutch size in zebra finch (Taeniopygia guttata) colonies.
Nightingale Luscinia megarhynchos at least, the dawn Proceedings of the Royal Society B 272, 383–8.
chorus is a means by which males can compete with
REPRODUCTION 111
(A) (B)
0.8
Singing activity (%)
0.6
0.4
0.2
0
Dusk N1 N2 N3 N4 N5 N6 N7 Dawn Dusk N1 N2 N3 N4 N5 N6 N7 Dawn
20:20 21:30 22:40 23:50 01:00 02:10 03:20 04:30 05:40 20:36 21:41 22:46 23:51 00:56 02:01 03:06 04:11 05:16
Time of day Time of day
(C)
10101010 9 9 9 9 1010 8 8 8 7 8 7 7 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 5 6 6 6 5 5 5 5
Distance covered per hour (km)
2.0
1.5
1.0
0.5
0
12 14 16 18 20 22 24 02 04 06 08 10 12 14 16 18 20 22 24 02 04 06
Time of day
Figure 5.11 Female movement and male singing behaviour of Nightingales; (A) prior to female arrival, birds that will eventually find a mate
(closed circles) and those that will not (open circles) both increase their singing activity as dawn approaches, (B) after female arrival, paired birds
and birds that will eventually find a mate (closed circles) sing most at dusk and as dawn approaches, and (C) females searching for prospective
mates are most active at night. From Roth, T., Sprau, P., Schmidt, R., et al. (2009) Sex specific timing of mate searching and territory prospecting in
the nightingale: nocturnal life of females. Proceedings of the Royal Society B, 276, 2045–50.
Box 5.6 Bird song and noise pollution
In 2003 Frank Rheindt censused the birds breeding along attention grabbing title Cities Change the Songs of Birds. In
woodland transects moving away from a busy German this thought-provoking article they made the chilling claim
motorway and found that species with low frequency songs that worldwide urbanisation and the on-going rise of urban
such as the Chiffchaff Phylloscopus collybita and Great noise levels form a major threat to living conditions in and
Spotted Woodpecker Dendrocopos major were 60–75 per around cities. Specifically they, like Rheindt, were highlight-
cent less common closer to the road. Because birds with ing the problem faced by songbirds having to compete with
higher frequency songs were not similarly affected, he con- urban noise pollution to make themselves heard. In their
cluded that birds were probably avoiding areas close to study Slabbekoorn and den Boer-Visser compared the songs
roads because ambient low frequency traffic noise drowned of Great Tits Parus major breeding in ten major European
out their song. Since then numerous studies have suggested cities with woodland populations close to each of them.
an impact of urban noise pollution from traffic and from They too concluded that low frequency urban noise pollution
industry, on birds and particularly upon aspects of birds’ masks low frequency bird song. But in this case they also
breeding behaviour. For example in 2006, Hans Slabbekoorn found that by altering their songs, the birds were fighting
and Ardie den Boer-Visser co-authored a report with the back. Analyses of the songs of the Great Tits in their study
continued
Box 5.6 Continued

populations revealed a frequency shift in urban birds. They levels of noise pollution, potentially impacting upon their
were no longer singing the lower notes of their song at a ability to adequately refuel for their onward journey.
low frequency. Although the upper frequency of their song Recently Allison Injaian and co-workers at the University
remained unchanged, the lower notes were now higher in of California have conducted a particularly elegant field-
urban than rural settings and so the frequency range of their based experiment involving a population of nest-box breed-
song was narrower. This ability to respond and adapt might ing Tree Swallows Tachycineta bicolor to better understand
seem like good news, and in the context of Great Tits being how exposure to noise pollution, and an associated reduc-
able to hear one another it probably is. More recently how- tion in perceived habitat quality, can affect bird territorial
ever a range of experiments involving manipulations of settlement patterns and reproductive success. To measure
ambient noise levels in both the laboratory and the field sug- the impact of noise pollution, the researchers assigned some
gest that increased exposure to noise has a much broader clusters of nest-boxes to an experimental group where they
range of impacts upon birds than just making their songs played loud recordings of traffic noise from a few days prior
difficult to hear. Noise pollution can in fact have physio- to the return of any swallows from their migration grounds
logical impacts upon adults and nestlings. It has also been until after all of the boxes in the study had been occupied
demonstrated by Alizée Meillère and colleagues that expos- (no eggs or chicks were exposed to elevated noise levels).
ure to noise results in reduced telomere length in House The other clusters of boxes were used as controls for com-
Sparrow Passer domesticus nestlings, which may affect their parison and no recordings of traffic noise were played there.
survival in the longer term. Also, birds exposed to noise often By recording the occupancy of experimental and control
have a reduced immune response and associated higher nest-boxes, and by monitoring the reproductive success of
blood concentrations of stress indicators. Migrating birds the swallows, the team were able to demonstrate the impact
have been shown to avoid stop-over sites that have higher of increased noise levels upon both settlement rates and
(A) (B)
15 20
Female Settlement Rank
Male Settlement Rank
15
10
10
5
5
Figure 5.12 shows the order in which
nest-boxes were occupied in relation to the
45 50 55 60 45 50 55 60 level of ambient noise (amplitude in dBA)
Amplitude (dBA) Amplitude (dBA) at each of them for male (A) and female
(C) (D) (B) tree swallows. Quieter boxes were
1.5 settled first. Female swallows laid their first
egg sooner in quiet nest-boxes than in
Mean nestling BCI per nest
1.0
noisy nest-boxes (C), and that nestlings in
Apr 24
0.5
Egg-laying date
noisier boxes had poorer body condition

(D) (body condition index (BCI) measured
0.0
as mass/wing length). From Injaian, A.S.,
Apr 20
–0.5 Poon, L.Y., and Patricelli, G.L. (2018) Effects

of experimental anthropogenic noise on
–1.0
avian settlement patterns and reproductive
–1.5 success. Behavioural Ecology 29(5),
Apr 16
1181–9, by permission of Oxford

Control Noise Control Noise University Press.
REPRODUCTION 113
aspects of reproductive success. Specifically they found that females because through EPCs males can ensure that some
control (quiet) nest-boxes were occupied more quickly by of their offspring develop in quieter nest-boxes.
returning birds than noisy experimental nest-boxes, an indi- It seems clear that noise pollution in the form of traffic
cation that the birds prefer the quiet nest-boxes. They also noise has a detrimental impact upon birds, but what can we
found that females were more likely to lay eggs sooner in do about it? Where appropriate, roadside barriers could be
quiet boxes (on average 3.8 days sooner) and that clutches erected, or vegetation managed to reduce noise transmis-
of eggs laid in noisy nest-boxes were on average 0.58 eggs sion. However, research suggests that much of the noise
smaller than those in quiet boxes. In addition, although sur- produced by traffic is related to the speed vehicles travel and
vival to fledging was not related to noise levels, nestlings the interaction of tyres and road surfaces. So one strategy
in noisy nest-boxes did have poorer body condition, even might be to impose speed limits and to use noise dampening
though they had not been directly exposed to the noise as road surfaces (such as porous asphalt) in areas that are of
either eggs or chicks. These findings suggest that birds particular conservation significance.
perceive noise polluted areas to be poorer quality territories
and confirm that noise pollution has a negative impact References
upon important aspects of reproductive success. From Meillère, A., Brischoux, F., Ribout, C., and Angelier, F. (2015)
Figures 5.12A and 5.12B though it is apparent that the Traffic noise exposure affects telomere length in nestling
impact of noise on settlement rates is stronger for females house sparrows. Biology Letters 11(9), 1–5.
than it is for males, something that the researchers suggest Rheindt, F.E. (2003) The impact of roads on birds: Does song
might be explained by the fact that extra-pair copulation frequency play a role in determining susceptibility to noise
rates are particularly high in Tree Swallows (50 per cent of all pollution? Journal für Ornithologie 144, 295–306.
broods have extra-pair offspring) and that the fitness costs Slabbekoorn, H. and den Boer-Visser, A. (2006) Cities change
for males occupying noisy territories may be lower than for the songs of birds. Current Biology 16, 2326–31.
time birds often have a diet that differs from that

Flight path: Swamping predators can reduce
of adults of their species to enable them to obtain
individual vulnerability to predation. page 137.
higher than usual amounts of protein, fat, and cal-
cium for muscle and bone development. Most pas-
5.5 Raising a family
serine chicks for example are raised on a diet of
You will recall from chapter 4 that most young birds soft-bodied insects, snails, and fragments of egg
require some degree of parental care; the exception shell even if as an adult their diet would be
being the fully independent super-precocial chicks restricted to grains and fruits. Some specialists such
of some megapode species. The degree of care as pigeons and penguins regurgitate a nutritious
required varies from a relatively low level of protec- mixture of fats and protein to facilitate very rapid
tion and tuition (precocial chicks) to that required chick growth. The ‘milk’ regurgitated by pigeons
by the altricial passerines that are blind, deaf, and is composed largely of sloughed off oesophageal
completely helpless at hatching. During the post- epithelial cells.
hatching period chicks are not efficient thermoregu-
lators and rely to a large extent upon their parents
5.5.1 Begging
for warmth or for shade (when the problem is an
inability to stay cool). Both precocial and altricial Chicks solicit food from their parents by begging, a
chicks develop quickly though, and after about a behaviour that typically involves a screaming call, a
week most are largely able to control their own wide gape, and exaggerated head movements. In
body temperature. To do this they rely upon their the case of some birds, and particularly those in
insulating down and growing contour feathers to darker nests, the flanges of the gape and the palate
regulate heat loss and upon the heat-generating are often brightly coloured to make them a more
shivering of their developed leg and breast muscles. conspicuous stimulus (Figure 5.13). Initially most
Rapid growth requires a lot of energy and so young birds are indiscriminate in their begging
chicks typically have prodigious appetites. At this behaviour. For example, the very young chicks of
Amount of pecking
0 5 10
Days in nest
Figure 5.14 Although equally likely to beg from (peck) models of

both Herring Gulls (open symbols, broken line) and Laughing Gulls
(filled symbols, solid line) when newly hatched, Herring Gull chicks
learn to focus their attention on a model of their parent. From
Hailman, J.P. (1969) How an instinct is learned. Scientific American
221(6), 106.
Figure 5.13 The bright yellow gapes of these begging Barn
Swallow Hirundo rustica are an effective signal of hunger to their hard Laughing Gull model waned. Why? Well because
working parents (© Bill Scott).
these chicks were of course being fed by their par-
ents and so learned to associate a Herring Gull head
cavity nesting passerines will beg at any shadow pass- and beak with food and to ignore the inappropriate
ing in front of the nest entrance be it friend or foe. As stimulus of a Laughing Gull head; a process termed
they mature, their behaviour becomes more refined perceptual sharpening.
and eventually they become more discriminating; Recently further subtleties of the begging rela-
directing their begging only towards their parents and tionship have been explored. Clearly chicks beg to
responding to other shadows with silence and a be fed and parents should respond to begging by
crouch. This ability to discriminate and beg only when feeding chicks, but do the needs of the parents and
it is appropriate to do so is essential because begging chicks and of siblings in the nest always coincide?
calls have been shown to attract predators.
In a set of experiments now quite properly regarded Key reference
as being ‘classics’ Jack Hailman demonstrated this Moreno-Rueda, G., Soler, M., Soler, J.J., et al. (2007)
phenomenon in the case of the Herring Gull Larus Rules of food allocation between nestlings of the
argentatus. These chicks had been previously shown, Black-billed Magpie Pica pica, a species showing
by Niko Tinbergen, to instinctively peck at any brood reduction. Ardea 54(1), 15–25.
beak-like stimulus just so long as it was vaguely
similar to a real beak (long, thin, and with a con- Gregorio Moreno-Rueda and his colleagues have
trasting mark towards its tip). Herring Gull beaks demonstrated that Black-billed Magpie Pica pica
are yellow with a red spot towards the tip of the parents respond to the differing needs of their
lower mandible. Chicks peck at the spot instinct- brood by feeding the chick that begs with the high-
ively and the pecking stimulates the adult bird to est intensity. As begging intensity is known to cor-
regurgitate food—so pecking is a begging behav- relate strongly with hunger in this and other species
iour. Prior to Hailman’s work it had been assumed this does seem to be a sensible strategy on the part
that instinctive behaviours such as this one were of the adult birds. What would happen though if
inflexible, but by presenting wild Herring Gull insufficient food was available and the whole brood
chicks in their own nests with models of Herring could not be successfully fledged? (In most birds
Gull heads and beaks and Laughing Gull Larus atri- there is a strong relationship between size/mass
cilla heads and beaks (all red) he showed that this at fledging and subsequent survival rates.) By
was not in fact the case. As the data presented in always feeding the hungriest chick the parents may
Figure 5.14 show, the chicks did initially peck at disadvantage the strongest and therefore reduce
both stimuli, but through time their interest in the their own reproductive success. Moreno-Rueda’s
REPRODUCTION 115
observations suggest that a further refinement of lay. In effect they give favoured offspring a head
the behaviour of the parent birds allows them to start. We have also seen that this kind of differential
avoid this problem. parental investment persists after eggs have hatched,
with some chicks receiving more food than others.
Flight path: Page 78. Magpie broods suffer losses at It has been recently shown that this phenomenon
the nestling stage.
can be more sophisticated than we might have
thought. Male Spotless Starlings Sturnus unicolor
Although the parent magpies do preferentially feed
have been shown to provide more food for chicks
chicks that beg intensely, they also preferentially
that hatch from darker shelled eggs. By doing this
feed larger chicks, and because magpie eggs hatch
the males are thought to favour the chicks that have
asynchronously there is often quite a size range
hatched from the highest quality eggs. It is also the
amongst chicks within a brood. In a poor season
case that by some, as yet undetermined means,
therefore smaller chicks will in effect be allowed to
male birds are able to assess the likelihood that the
starve so that their siblings can survive.
chicks in their brood are unrelated to them and
Key reference therefore the result of extra-pair copulations. Having
Porkert, J. and Špinka, M. (2006) Begging in Common done so they allocate their feeding accordingly and
Redstart nestlings: scramble competition or signalling preferentially feed those chicks most likely to have
of need? Ethology 112, 398–410. been sired by them. Sometimes of course this
kind of differential allocation of feeding effort may
Brood reduction of this type is not an uncommon not be a means of increasing individual fitness by
response to resource limitations and in many cases favouring those chicks that are themselves pre-
such as some of the herons, raptors, and parasitic sumed to be fit, it may simply be a means by which
cuckoos it is the norm. It is often more brutal and a pair of birds can make the process of raising a
competitor chicks are ejected from the nest, killed family more efficient.
and/or cannibalized by their siblings. However, it
is not the case that all brood mates compete in this Key reference
cutthroat way. For example Jiři Porkert and Marek Draganoiu, T.I., Nagel, L., Musseau, R., and Kreutzer,
Špinka have shown that in the Common Redstart M. (2006) In a songbird, the Black Redstart, parents
Phoenicurus phoenicurus begging intensity is an hon- use acoustic cues to discriminate between their
est signal of need (hungrier chicks beg more) and different fledglings. Animal Behaviour 71, 1039–46.
that like magpies, adult redstarts do preferentially
feed the hungriest chicks. In this species chicks In the case of redstarts, and specifically the Black
within a brood vary very little in weight at fledging Redstart Phoenicurus ochruros, Tudor Draganoiu
suggesting that there is little competition between and his colleagues have shown that the members of
them. So do the parent redstarts have other feeding a breeding pair each preferentially feed some mem-
preferences? Yes they do. They preferentially feed bers of the brood while paying little if any attention
those chicks that beg most closely to the entrance of to the others. Often they observed males to feed
the nest cavity. So does this mean that some chicks fewer of the chicks than females and in some cases
are fed more than others as was the case in the mag- the division of the labour was such that the female
pie? Through observation of the behaviour of the parents fed three times as many chicks as the males.
nestlings within broods, Porkert and Špinka found Although the reason for this behaviour has not
that once it had been fed to satiation a chick typic- been determined in this species, Draganoiu and his
ally moved to the back of the nest, allowing its hun- team have demonstrated that birds are able to rec-
gry nest-mates to take their turn at the front. ognize the chicks that they will feed. By observing
This may not mean however that redstart parents the response of adults to recordings of chick
feed all chicks equally. You may recall that in chap- begging calls, they have shown that adults are
ter 4 I mentioned that female birds vary the invest- able to discriminate between the begging calls of
ment that they make in each of the eggs that they individual chicks.
Box 5.7 Helpers at the nest
Raising a family can be a chore and evidence that two In the mid 1960s this species was on the verge of extinc-
parents are better able than one to do the job is com- tion with a population of just 26 pairs and was confined to
monly cited in the scientific literature. However there are Cousin Island in the Seychelles archipelago. Effective conser-
cases when even two parents are not sufficient and in vation interventions by the International Council for Bird
these situations it is common for bands of birds to work Preservation (ICBP) have included the removal of predators,
together to cooperatively raise a brood. In some cases a the planting of trees that support an abundance of the insect
number of pairs will breed close to one another in a col- food the birds rely upon, and the translocation of birds to
ony, sharing the roles of food finding and defence. But in other islands in the archipelago. As a result the most recent
some species it is common for a territorial pair of birds to IUCN assessment of the warbler population (2016) esti-
be assisted in rearing their brood by non-breeding helpers. mates that there are at least 3000 individuals across the
One of the cooperative breeding species that we know archipelago (Cousin, Frégate, Denis, and Aride Islands) and
most about is the Seychelles Warbler Acrocephalus sechel- that the population continues to grow. As a result the
lensis (Figure 5.15). Seychelles Warbler is no longer considered to be in danger of
extinction and is classified by the IUCN as Near Threatened,
this is an excellent example of a conservation success story.
During the initial period of population growth of Cousin
Island pairs of warblers defended their territories, incubated
their eggs, and raised their families alone. But then as the
population grew it became more common for breeding pairs
of birds to be helped by non-breeding conspecifics. Jan
Komdeur and his colleagues monitored the breeding warblers
throughout this period and Figure 5.16 highlights two key
points. First, the number of occupied territories plateaus in
the early 1980s at about 120, which is thought to be the
carrying capacity of the island. This means that as the popu-
lation of birds grew, a point was reached where there were
many more breeding age birds than there were territories
available. Secondly, at about that time when the island
became effectively saturated, some birds stopped dispersing
Figure 5.15 Seychelles Warbler Acrocephalus sechellensis (© when they became independent and chose instead to remain
Daniel Wade). on their natal territory as helpers. Confirmation of the
Birds
Territorios
400 200
160
300
Territorios
120
Birds
200
Cooperative 80
breeding
100 Figure 5.16 The growth of the population of
40
Cousin Island Seychelles Warblers. From Komdeur,
J. (1992) Importance of habitat saturation and terri-
0 0 tory quality for evolution of cooperative breeding in
55 60 65 70 75 80 85 90 the Seychelles Warbler. Nature 358, 493–495.
Year Reprinted by permission.
REPRODUCTION 117
(A) (B)
1.0 69 31 7 4 1.0 33
99 89 42 9
530 592
0.8 0.8
435
211 97 388 190
61 104
Annual survival
Annual survival
0.6 91 0.6
0.4 0.4
31
34
0.2 0.2
Without helper Without helper
With helper With helper
0.0 2 0.0 3
2 4 6 8 10 12 14 16 18 2 4 6 8 10 12 14 16 18
Age of female dominant (years) Age of male dominant (years)
Figure 5.17 Age dependent survival of female (A) and male (B) Seychelles Warblers who were (solid lines) and were not (dashed lines)
assisted by helpers at the nest. The lines show model predicted slopes derived from the available data. From Hammers, M., Kingma, S.A.,
Spurgin, L.G., et al. (2019) Breeders that receive help age more slowly in a cooperatively breeding bird. Nature Communications 10(1301),
1–10. Reprinted by permission.
generality of this sequence of helper behaviour develop- It isn’t just young birds that help, research by Komdeur
ment has come from ongoing conservation efforts that have and his co-workers has also revealed that grandparents are
introduced small numbers of the warblers to adjacent Aride, helpers too! Over a 24-year observation period almost 14
Frégate, and Denis Islands. In the case of Aride no helping per cent of breeding females were deposed by one of their
was recorded until the island had reached its carrying younger relatives. Rather than disperse and become non-
capacity. breeding floaters (birds without a territory), 68 per cent of
These helpers assist their parents in incubation (females these grandmothers stayed on and assisted their offspring
only), chick feeding, territory defence, and predator mob- in the raising of the next generation. Recent research suggests
bing. They are most often found on higher quality territories; that grandparents are able to help in this species because
the ones that are particularly rich in insect food and so able they themselves were helped as breeders. Martijn Hammers
to support a larger population of birds. As territories become and colleagues have shown that although survival rates
available helpers have a choice—stay on at home or move of breeding male and female warblers with and without
out to occupy the vacant space. Researchers have found that helpers are similar, late-life decline in survival is signifi-
in many ways they act in a manner similar to that predicted cantly lower among older females when a helper is present
by the Polygyny Threshold Model: When the first vacancy to (Figure 5.17) and a similar non-significant trend is apparent
arise is in a poor quality territory they stay home and wait among older males. Intriguingly the researchers have also
until something better ‘comes to market’. If a high quality found that the telomeres of older females without helpers
territory becomes available first they moved onto it. Essentially are shorter than those of birds with helpers. Telomere short-
this seems to be because, considered over a reproductive ening is associated with age-related senescence and so this
lifetime, the immediate term benefit of taking up a low qual- suggests that a benefit of having helpers is that they help
ity opportunity and then staying on that territory for the breeding females to maintain their body condition, and in
remainder of one’s life is less than the benefits to be gained effect to delay the impact of ageing.
by waiting until the high quality territories come along.
Remember all of the time that a helper is assisting in the Further reading
raising of its siblings or grandchildren it is in effect helping to Richardson, D.S., Burke, T., and Komdeur, J. (2007) Grandparent
propagate genes that it shares with them. In this way a bird helpers: The adaptive significance of older, post dominant
that delays dispersal and breeding is still making an indirect helpers in the Seychelles Warbler. Evolution 61(12),
contribution to its own genetic fitness. 2790–800.
5.5.2 Imprinting and independence have been hand-reared specifically to imprint them
upon a human trainer and can be encouraged to
During the nestling and post fledging stage, before
mate and ejaculate with their trainer’s gloved hand
they become fully independent, young birds imprint
to facilitate the collection of semen to be used in
upon their parents. This very specific learning pro-
artificial insemination programmes.
cess serves to ‘fix’ the species identity of the indi-
Eventually, if a chick has survived the competi-
vidual and set it on a behavioural path that will
tion with its siblings, the vulnerable period in the
persist into adulthood. As we saw in the case of the
nest and the risky business of fledging into a hostile
sensitive period of song acquisition, the imprinting
environment there comes a time when it must
period is a short and discrete period in the young
become independent. In some cases birds remain in
bird’s life. As an example of the significance of
extended family groups (see Box 5.7) but in most
imprinting consider the mating preferences of adult
cases they drift away from, or are chased away by,
birds that were imprinted upon a ‘parent’ of a spe-
their parents to disperse and begin their adult life.
cies other than their own. If Zebra Finch Taeniopygia
Marion Germain and co-workers have explored
guttata eggs are cross-fostered to be hatched and
the potential impact of dispersing to an unfamiliar
reared by the domesticated Bengalese Finch Lonchura
area by capturing and translocating members of a
striata parents, the resulting male Zebra Finches
population of Collared Flycatcher Ficedula albicollis
will preferentially court female Bengalese Finches
shortly after they arrived on their Swedish summer
and ignore females of their own species. For this
breeding grounds. Some of the birds were simply
reason birds that are hand-reared as part of a con-
captured and released, while others were captured
servation programme must be maintained in a care-
and moved to a new area. This was done to separate
fully controlled environment and provided with
the effects of capture per se from the effects of dis-
suitable specific stimuli to ensure normal develop-
placement. Some of the translocated birds found
ment. Sometimes though there is occasionally an
their way back to their capture site and bred there,
advantage to inappropriate imprinting. Male raptors
others bred at their release site. By comparing the
14.6
N = 203
14.4
N = 1210
Predicted nestling body mass (g)
14.2 N = 640
14
13.8 N = 140
13.6
13.4
13.2
Non Control Displaced- Displaced-
experimental returned not returned
Figure 5.18 Although birds that were displaced from their breeding area reared lighter nestlings than birds that had not been displaced, those
that did find their way back to their initial breeding site reared heavier nestlings than those that did not. From Germain, M., Part, T., Doligez, B.,
et al. (2017) Lower settlement following a forced displacement experiment: nonbreeding as a dispersal cost in a wild bird? Animal Behaviour 133,
109–21. Reprinted with permission from Elsevier.
REPRODUCTION 119
reproductive success of these experimental birds Summary

with the control birds, and birds that had not been
captured at all, the researchers have provided evi- As a result of anisogamy the priorities of males and
dence that there is a cost associated with breeding females differ—although of course both are primar-
in a novel area. Figure 5.18 shows that birds that ily driven to pass on their genes. Consequently
bred in a novel area reared lighter nestlings than a wide range of mating/breeding strategies has
birds that found their way back to their initial cap- evolved. Females choose males on the basis of song,
ture site and birds that were not moved. As we saw display, resource provision or genetic quality, and
earlier in the chapter, nestling size is a measure of males compete for access to mates. Chicks manipu-
reproductive success because smaller fledglings are late their parents but mothers and fathers may also
less likely to survive than heavier ones. manipulate the care that they provide.
C H A PT ER 6
Foraging and avoiding predators
‘A curious bird is the Pelican, its beak can hold more than its belly can!’
D.L. Merritt, Nashville Banner (1913)
Birds need to eat and drink. The basic principles of

Flight path: Foraging can involve navigation and
foraging for food and water are common to all spe-
spatial memory. page 66.
cies be they a predatory owl, an herbivorous goose,
a generalist omnivore like the crows, or a highly Birds have highly developed eyes and high visual
specialized feeder like the nectivorous humming- acuity, so it should come as no surprise that many of
birds. Food or water has to be found, captured or them rely upon sight to locate prey. Some such as the
obtained, and then processed and ingested. At the hawks and owls have forward-pointing eyes that
same time a foraging individual has to make deci- facilitate binocular vision—essential for a bird that
sions about food quality, perhaps choosing one item grabs moving prey. Others have eyes more towards
over another, make decisions about how much to the sides of their heads, a compromise between bin-
eat and in some cases how much to store, and make ocular vision for prey capture and something closer
decisions about when to share with flock-mates and to monocular vision, with a wider field of view, for
when to defend the resource. Think about this next predator avoidance. These birds often have to cock
time you watch a feeding bird—their behaviour their head from side to side to get an accurate fix on
may not be as simple as it appears! their target prior to pecking. Of course there are occa-
sions when sight is not sufficient. Nocturnal owls can
see by moonlight, but they rely to a greater extent
Chapter overview upon their hearing to locate prey. Similarly it has been
demonstrated experimentally by Robert Montgomerie
6.1 Finding food and capturing prey and Patrick Weatherhead that American Robin Turdus
6.2 Optimal foraging migratorius listen out for their prey too. Although for-
6.3 Risk and foraging aging robins do use visual cues when hunting for
6.4 Predator avoidance worms in leaf litter and soil, they are less able to locate
their prey when it is immobile or if the sounds made
by crawling worms are masked by white noise. This
6.1 Finding food and capturing prey suggests that robins use auditory cues to find worms.
In chapter 3 we saw that birds such as the chicka- Key reference

dees and titmice are able to relocate previously Montgomerie, R. and Weatherhead, P.J. (1997) How
stored food by impressive acts of memory. In many robins find worms. Animal Behaviour 54, 143–51.
cases, however, foraging involves the location and
acquisition of previously unidentified food sources Wading birds feeding on soft sediments are able
and involves the use of the full range of senses. to see prey and visual cues to the presence of prey
DOI: 10.1093/oso/9780198804741.003.0006
F O R A G I N G A N D AV O I D I N G P R E D ATO R S 121
(worm casts and burrow mouths) during the day or long billed waders. In this case however smell rather
under a bright moon. However, the pressures of than touch seems to be the important sense. Whereas
feeding between the tides mean that these birds the nostrils of most birds are situated at the base of
often have to feed when they are unable to see well, the beak, those of the kiwi are close to the tip. It seems
and of course long billed birds like curlews cannot that they find their prey by sniffing out burrows.
see the prey that they seek when they probe deep Similarly it has recently been shown that some of the
into soft mud. In such cases waders feel for their oceanic albatrosses and petrels are stimulated to fol-
food. The tip of the wader beak is sensitive to touch low the scent of pyrazine. This is a chemical com-
and able to discriminate prey from non-prey. Smaller pound that is released when plankton and krill are
billed waders, sandpipers, and plovers, use a simi- eaten by fish or other birds. This might explain how
lar tactic when searching for surface prey in the some species are able to home in on patchily distrib-
dark. By day they can see their prey and dart across uted but locally super-abundant swarms of krill.
the sand to snatch it up with a single, well aimed Unfortunately many species of seabird hunting krill,
peck. At night they hunt by ‘stitching’ repeated, squid, and jellyfish accidentally consume marine
rapid jabs at the sand/mud as they walk across it plastic pollution with fatal results (see Box 6.1).
(like the stabbing of a sewing machine needle—
hence the term stitching), occasionally swallowing Key reference
food that they encounter. Nevitt, G., Reid, K., and Trathan, P. (2004) Testing
Nocturnal kiwi feed largely on burrowing earth- olfactory foraging strategies in an Antarctic seabird
worms that they capture by probing into soft earth assemblage. Journal of Experimental Biology 207,
3537–44.
with their long beak in much the same way as the
Box 6.1 Plastic pollution
Plastic pollution is a global problem, and marine plastic pol- the bodies of more than 1,700 birds of 51 Procellariiform
lution is known to impact seabirds in particular. In fact more species from sites around Western Australia, Tasmania, and
than half of the world’s seabird species have been reported New Zealand, and examined them to determine cause of
to have ingested potentially harmful plastic fragments. It is death and to record the amount and type of plastic that
currently estimated that between 15 and 51 trillion pieces of they had ingested. They recorded plastic ingestion by indi-
plastic, or 250,000 tonnes, are currently floating in the seas viduals of all of the species encountered, but as Figure 6.1A
and oceans of the world. In spite of an increasing global shows, the level of plastic ingestion varied and so it seems
awareness of this issue it is likely that the scale of the prob- likely that not all species are equally at risk of consuming
lem will continue to increase for at least the medium-term plastic. So why the variation? Based upon their analyses
future. Marine plastics are ubiquitous but tend to concen- the researchers believe that the foraging strategy employed
trate in hot-spots such as the Southern Ocean boundary of by a species determines the likelihood that it will encoun-
the Australasian Tasman Sea, which is coincidentally one of ter and ingest floating plastic debris. The albatrosses for
the sites of greatest seabird biodiversity on the planet. example, hunt for fish below the water surface and as a
Plastic ingestion by seabirds is not a new phenomenon, it consequence encounter and consume less plastic than say
was first reported in the 1960s. I remember vividly my initial the storm petrels who flutter across the surface picking up
surprise when finding small plastic pellets in the regurgi- shallow swimming crustacean (which bear a more than
tated stomach contents of the young Scottish Fulmars that I superficial resemblance to fragments of floating plastic).
ringed as part of a monitoring programme in the 1990s Species that consume squid are also thought to be particu-
(regurgitation is a highly effective defence strategy employed larly at risk because balloon fragments and some other
by the immobile chicks). The potential scale of the problem, marine plastics look very like squid. In this study all of
and growing public outrage at the environmental impact of the species found to have ingested balloons typically
plastic pollution have, however, intensified in recent years. hunt squid.
To better understand the impact of plastic pollution
upon seabirds, Lauren Roman and her colleagues collected continued
Box 6.1 Continued

(B)
40
(A)
Albatrosses
Giant petrels 30
Procellarine petrels
Fulmarine petrels
Sum of Debris
Gadfly petrels
Shearwaters 20
Prions
Storm petrels
Diving petrels
10
0 10 20 30 40
Number debris of items ingested
KND Ind KD
Figure 6.1 (A) The numbers of items of plastic that had been ingested by birds in each of the Procellariiforme taxonomic groups, and
(B) the quantity of marine debris that had been ingested by birds that have died as a result of debris ingestion (KD), where death was not
related to debris (KND), and where the ingestion of debris may have played some part (Ind). From (A) Roman, L., Bell, E., Wilcox, C., et al. (2019)
Ecological drivers of marine debris ingestion in Procellariiform seabirds. Nature Scientific Reports January. (B) Roman, L., Hardesty, B.D., Hindell,
M.A., and Wilcox, C. (2019) A quantitative analysis linking seabird mortality and marine debris ingestion. Nature Scientific Reports March.
But how much of a problem is plastic ingestion? Of the 27 per cent of their sample (459 birds). The more plastic a bird
birds examined 32 per cent had ingested between 1 and 40 had ingested, the higher the mortality risk (Figure 6.1B). The
pieces of plastic, typically hard plastic fragments and pellets 13 birds that were known to have died directly as a result of
(92 per cent of pieces). Less commonly ingested items included plastic ingestion did so because their gut wall had been per-
balloon fragments, rubber pieces, fishing debris, and soft forated by hard plastic, or because their gastrointestinal tract
packaging. Although the researchers were only able to attri- had been blocked by plastic. Although balloon fragments were
bute plastic ingestion as the cause of death in a small number relatively rare (just 2 per cent of all fragments recovered) birds
of cases (13 birds), they were able to determine that plastic that has swallowed balloon pieces were 32 per cent more
ingestion probably played a significant role in the mortality of likely to die than birds that had ingested hard plastic.
frenzy is likely to be a very strong cue to any bird in

6.1.1 Sharing information
the area as to the whereabouts of that food patch.
Although petrels may follow pyrazine slicks to The idea that birds might use the sight of the suc-
locate food, if the krill are under attack by other sur- cess of other foraging birds as a cue to the hunt is
face feeding birds the visual stimulus of a feeding encapsulated in the ‘information transfer hypothesis’
Number of departures from colony
No No Winter Alewife Pollock Smelt

information fish flounder
Figure 6.2 Departures from an Osprey colony are more common when birds have observed a successful colony-mate returning with a shoaling
fish. From Greene, E. (1987) Individuals in an osprey colony discriminate between high and low quality information. Nature 329, 239–41.
Reprinted by permission.
which simply predicts that animals should act upon the shoaling Alewife, Pollock and Smelt, Winter
information from others for their own benefit. In the Flounder is a solitary fish.
case of a petrel flying towards a mob of feeding birds
there is of course no suggestion that the cue is an
6.1.2 Foraging flocks
intentional signal designed to recruit others, but in
some cases intentional communication does seem to Sharing information and working together can
be used to recruit flock-mates to good feeding areas. enable birds to forage more efficiently as a flock and
During observations of a colony of Osprey Pandion to have a higher level of success than they would
haliaetus, Erik Greene noted that whilst birds return- were they to forage alone. For example, experi-
ing to the colony after an unsuccessful fishing trip ments with captive flocks of fishing Black-headed
flew directly to their nest or favoured perch, birds Gull Larus ridibundus have shown that as flock size
that had been successful (they were carrying a fish) increases, the likelihood of an individual catching a
did not. Instead successful birds performed an elab- fish also increases (Figure 6.3). This is probably
orate undulating display flight accompanied by a because fish fleeing from lots of predators are likely,
persistent call. Greene hypothesized that if these in their confusion, to blunder into the beak of one of
birds were intentionally advertising their success them rather than because the birds are actively
then their colony-mates should take advantage of working together.
the information provided to them and fly out to In the case of the Harris Hawk Parabuteo unicinc-
hunt more often when they are ‘told’ that fish are tus however, real cooperation is the order of the day.
available, and fly most often in the direction from Groups of hawks gather in the early morning and
which the successful hunter approached the colony. then spend the day actively searching for prey in an
This is exactly what he recorded happening. extended flock. Individual hawks leap-frog over
There is an added sophistication to this behaviour. one another as they search for rabbits and other
From Figure 6.2 it is clear that when the returning small mammals (see Figure 6.4).
hunter carries an Alewife, Pollock or Smelt into the Once one hawk has found a prey animal the
colony there is an increase in the number of birds others in the group converge upon it and then they
setting out on a hunting trip (compared to the num- work together to move it into a position from which
ber setting out with no information or with nega- one or more of them can launch an attack. Sometimes
tive information). The figure also shows that when they drive the animal into the open and then several
the hunter returned with a Winter Flounder colony birds pounce upon it from different directions. If
mates did not respond. This is because unlike the prey takes to cover, one bird will follow it to
40
Flock of 6 birds
Flock of 3 birds
Single bird
Average number of fish eater

30
20
10
0 1 5 10
Trial number
Figure 6.3 Birds in larger flocks are more successful when hunting than are solitary birds. From Göttmark, F., Winkler, D., and Andersson,
M. (1986) Flock-feeding on fish schools increases success in gulls. Nature 319, 589–91. Reprinted by permission.
Cottontail kill
14.28 14.31
Five hawks
Fed until 15:50
12.40
13.17
Unsuccessful
strike at prey
13:47
14:21 12:27
Start monitoring
13:48 14:05
13:51
13:58
14:01
0 500 m
Figure 6.4 Sequence of movements of Harris Hawks during an ultimately successful hunt. Perched hawks indicate the number of birds recorded
in the group at that time and location. From Bednarz, J.C. (1988) Cooperative hunting in Harris' Hawks (Parabuteo unicinctus). Science 239,
1525–7. Reprinted with permission from AAAS.
flush it out towards the others who are waiting in return a little too early to beat their competitors.
ambush. When a kill is made all members of the Observations of grazing geese made by Herbert
group share in the meal and it would appear that a Prins and his co-workers have shown that on Dutch
single rabbit is sufficient to satiate several hawks. saltmarshes Brent Geese do cooperate to re-crop
Solitary Harris Hawks are rarely seen hunting and areas on a four-day rotation. They have also shown
so cooperative hunting would appear to be the (by experimentally clipping the plants) that four
norm in this species. Indeed Bednarz suggested that days is the optimal time to return to maximize the
on the basis of his observations it is probably the only amount of new growth material available to them.
way that Harris Hawks can survive in the harsh So it would seem that cooperation is as much of an
desert environment of southeastern New Mexico. advantage to herbivores as it is to predators.
6.1.3 Do herbivores cooperate? 6.2 Optimal foraging

It is easy to see how, by confusing prey or cooperat- The geese that we have just considered are behav-
ing to overcome it, gulls and hawks are coordinating ing as ‘intelligent foragers’ in an optimal fashion.
their behaviour to maximize their individual suc- That is to say their behaviour is exactly what we
cess. But can the same ever be said of herbivores? would predict if they are attempting to maximize
Plants do not need to be overcome, nor do they try to the benefits (food intake) of their activity at the
escape (although of course it would be wrong to same time as minimizing the costs.
think that they were defenceless—just grasp a net- Many species of coastal bird feed upon intertidal
tle!). Later in this chapter we will see that flock for- molluscs. Some like the Eurasian Oystercatcher
mation in herbivorous birds may be a predator Haematopus ostralegus use their beaks to open their
avoidance strategy but here I would like to consider prey, and as an aside they have evolved two distinct
the possibility that it is also a means by which birds morphologies and behaviours to do this. Some oyster-
can maximize their individual success in terms of the catchers have sharp pointed beaks that they use to
quality of the food that they have available to them. stab between the valves (shells) of their prey and then
prise or twist the shells apart to access the flesh. Others
Key reference have a heavy, blunt ended beak that they use as a
Prins, H.H.T., Ydenberg, R.C., and Drent, R.H. (1980) hammer or chisel to smash open the shells of their
The interaction of Brent Geese Branta bernicla and prey. Gulls and crows however use a different strat-
Sea Plantain Plantago maritime during spring staging: egy. Having selected a potential prey item they carry it
Field observations and experiments. Acta Bot Neerl into the air and drop it to shatter on the rocks below.
29, 585–96. During a study of the whelk dropping behaviour
of Northwestern Crows Corvus caurinus Reto Zach
In Europe, Brent Geese Branta bernicla spend the noted that birds were very selective when choosing
winter on temperate estuaries and salt-marshes a whelk to drop. Although whelks ranging from
where they feed on coastal vegetation, and in par- around 1.5 cm to 5 cm were available in the environ-
ticular on Sea Plantain Platago maritima. The plants ment, the crows preferentially selected larger whelks
that they eat are not particularly nutritious but they for dropping (see Figure 6.5A). He also noted that
are abundant and supplies are replenished through they consistently dropped whelks from a height of
re-growth within a few days of grazing. New shoots around 5 m and tended to have preferred drop-zones
are more nutritious than old growth. So we would (which were littered with broken shells).
predict that the best strategy for a bird is to feed on a Through a series of experiments Zach ruled out
patch and then to stay away from it until re-growth the possibility that smaller whelks were unpalat-
has occurred—but not to stay away so long that the able (crows were equally likely to consume the flesh
growth becomes old and tough. Of course this can of smaller and larger whelks when presented with a
only work if all of the members of a flock coordinate choice). He also found that larger whelks broke more
the way that they re-graze particular patches. If they easily than smaller ones when dropped (Figure 6.5B)
do not then birds would probably always attempt to and unsurprisingly provided the greatest reward
(A)
30
PER CENT FREQUENCIES

20
10
0
1.4 2.0 2.6 3.2 3.8 4.4 5.0
LENGTH (cm)
(B)
60
SMALL
MEDIUM
NUMBER OF DROPS
40 LARGE
PER WHELK
20
0
1 3 5 7 9 11 13 15
HEIGHT OF DROP (M)
Figure 6.5 (A) Although whelks ranging in size from 1.4 cm to 5 cm in length were available (white bars) crows preferentially selected rarer,
larger whelks (black bars). (B) Large whelks require fewer drops to break their shells than do smaller whelks. From Zach R (1979) Shell dropping:
Decision-making and optimal foraging in Northwestern Crows. Behaviour 68, 106–17.
(having most flesh). He also found that shells were same area as the breeding territory and it is likely
more likely to break if he dropped them in the that they are retained between years to facilitate
crows’ preferred drop-zones than if he dropped breeding. Others are only held outside of the breed-
them elsewhere. But most significantly, he calcu- ing season and so their prime function seems to be
lated that by making multiple drops from 5 m to provide the holder with access to sufficient food.
(rather than fewer from a higher height) the birds In this respect some territories may be quite small
maximized their net energy return when they ate the and persist for a very short period.
whelk (net energy return remember is the amount of For example Sanderling Calidris alba congregate
energy obtained from the food minus that spent find- on beaches in feeding flocks and large numbers of
ing it and making the flights to break it). He showed birds can often be seen feeding alongside one
that the birds were foraging in an optimal fashion. another. However, these diminutive waders may,
under certain conditions, defend small feeding ter-
ritories. Myers and co-workers made observations
6.2.1 Feeding territories
of the flocking and territorial behaviour of Sander-
As we saw in chapter 5 one of the functions of a ter- ling feeding on the isopod Exirolana linguifrons
ritory is to provide the resources a bird or a pair or on a sandy beach. Their results (Figure 6.6)
group of birds need to raise their young. But many indicate that the decision to defend a territory
birds retain their territories (or acquire new ones) depends upon the amount of food available. They
outside of the breeding season. In some cases these found that when prey were scarce birds fed alongside
non-breeding territories occupy all or most of the one another, presumably it would be impossible for
100 during an eight-hour observation period, whereas

those birds without a territory spent around 32 kJ.
% of area defended by sanderlings
80 Sunbirds generally feed on nectar whilst perched

on flowers but recently the invasion of parts of
60 South Africa by a new world plant, Nicotina glauca,
which is usually pollinated by hovering humming-
40
birds, has resulted in a startling behavioural devel-
opment. Sjirk Geets and Anton Pauw have reported
that the members of a community of Double-collared
20
Sunbirds Cinnyris afer and Malachite Sunbirds
Nectarinia famosa (Figure 6.7) have started to hover
0 200 400 600 800 1000 1200 to obtain nectar from Nicotina glauca (and to pollin-
Density of prey (animals/m2) ate the flowers in the process). The effects of this has
been that areas with Nicotina glauca support larger
Figure 6.6 Sanderling defend feeding territories only at numbers of sunbirds than do areas with only native
intermediate prey densities. From Myers, J.P., Connor, P.G., and Pitelka,
flower species present, and sunbirds delay their sea-
F.A. (1979) Territory size in wintering sanderlings: the effects of prey
abundance and intruder density. Auk 96, 551–61. Reprinted by sonal migration spending longer in Nicotina-rich
permission of Oxford University Press. areas than would previously have been the case.
Recent advances in technology are providing
ornithologists with unprecedented insights into the
an individual to defend an area large enough to
foraging behaviours of difficult to observe species.
provide sufficient food. Similarly, when food is
Take for example the Thick-billed Murre Uria lom-
super-abundant there is presumably no need to
via, a generalist fish-eater that spends most of its
defend the resource and birds do not have territor-
foraging time at sea. Until recently the only way
ies. However, at intermediate prey densities (and
that we could have studied their diet would have be
the thresholds involved are quite narrow) the birds
to record the food items that they brought back to
do become territorial. Here the costs of defence are
their breeding colonies to provision their chicks.
outweighed by the benefits of controlling access to
But by attaching an array of data collection devices
the available food.
(biologgers) to murres (see Figure 6.8) Émile
Brisson-Curadeau and Kyle Elliott have gained a
Key references
far more detailed understanding of murre behav-
Gill, F.B. and Wolf, L.L. (1975) Economics of feeding
territoriality in the Golden-winged Sunbird. Ecology iour. They attached camera loggers, GPS locators,
56, 333–45. and depth recorders to birds and with them were
Geerts, S. and Pauw A. (2009) African sunbirds hover able to record where birds travelled to catch their
to pollinate an invasive hummingbird-pollinated plant. prey, how deep they dived when hunting it, how
Oikos 118, 573–9. long it took them to handle it, and what it was.
These data enabled the researchers to test predic-
The actual energetics of the trade-off involved in tions about foraging behaviour made by the Central
this kind of territorial defence have been investi- Place Foraging Theory (CPFT) proposed by Orions
gated in the case of the old world sunbirds and new and Pearson. The CPFT predicts that when foraging
world hummingbirds. Both rely to a great extent from a central place (such as a breeding colony)
upon energy rich nectar and nectar availability is birds should select larger prey if they travel a long
a key determinant of territory size. For example way to hunt (and smaller prey when hunting close
in a now classic study of the foraging energetics to the colony). It also suggests that adults should
of Golden-winged Sunbird Nectarinia reichenowi, select larger prey when hunting to provision their
Frank Gill and Larry Wolf showed that in defended chick than they do when they are self-feeding.
patches of flowers nectar levels were higher than in The data collected confirmed the predictions of the
undefended patches. They calculated that birds CPFT. On average murres travelled further and dived
defending patches expended around 26 kJ of energy deeper when provisioning chicks than they did when
Figure 6.7 A hovering Malachite Sunbird taking nectar from Nicotina (© Sjirk Geerts).
incubating and self-feeding. In fact provisioning

phase dives were on average 47 m deep whilst incuba-
tion phase dives reached only 27 m. Furthermore the
rate of capture of larger prey (cod for example) was six
times higher when chicks were being fed than when
birds were self-feeding and the diet of adult birds
was almost entirely composed of small amphipods
(shrimps, etc.). GPS data revealed that larger prey like
cod were typically caught some 35–45 km from the
colony, whereas trips to catch the smaller amphipod
prey were generally shorter than 10 km. Interestingly
however, the data also revealed that individual
birds tended to specialize in particular prey types
and to hunt for their prey in particular areas.
Key references
Brisson-Curadeau, É. and Elliott, K.H. (2019) Prey
capture and selection throughout the breeding season
Figure 6.8 This Thick-billed Murre Uria lomvia is wearing a data in a deep-diving generalist seabird, the thick-billed
logger, in this case a depth-temperature-accelerometer, on its back. murre. Journal of Avian Biology 2019, e01930.
The bird hasn’t been injured—the red mark on its breast is a dab of Orians, G.H. and Pearson, N.E. (1979) On the theory
paint used by the researchers to quickly re-find the bird in its colony of central place foraging. Annual Review of Ecology
when they need to retrieve their hardware (© Kyle Elliott). and Systematics 157–77.
Box 6.2 City living
City living birds can get something of a reputation for being UK, Goldfinch Carduelis carduelis only really became com-
a nuisance when it comes to the dietary shift that often mon garden birds in the late 1990s when people started to
accompanies urbanization. In my hometown for example, put out the niger seed that they particularly like.
Herring Gulls Larus argentatus are viewed by some as being Globally garden bird feeding is a multi-billion dollar
a real pest because of their habit of stealing food from the industry and one that an estimated 50 per cent of all house-
hands of incautious tourists. The local council do warn holds in the UK and the USA enjoy. In the UK it has been
visitors—there are posters all over the place explaining that estimated that homeowners supply enough additional food
the gulls will steal food, that we can all do our bit by taking to support 196 million garden birds (more than twice the
sensible precautions when eating out of doors, and, by not actual number). I am fifty years old and can remember feed-
encouraging gulls to see people as a provider of food. ing birds in my own garden from a very early age. Back then
Despite these warnings many of the same people that will in the UK we mostly fed birds peanuts and kitchen scraps,
cry foul when robbed of their chips can be seen throwing today we provide an amazing array of foods specifically
their food scraps to the gulls because we do all like to feed ‘formulated’ to attract particular species to the garden and
the birds! delivered via an equally amazing variety of bird feeders.
So what characterizes a successful city living bird? Through Across Europe and North America garden bird feeding has
a comparison of urban and non-urban species Facundo modified local food abundance, particularly during the win-
Xavier Palacio has shown that those species of bird that ter months (we tend to feed birds when we perceive them to
thrive in an urban setting tend to have features in common. be suffering from a resource shortage or as having a particu-
They tend to be larger than non-urban congeners and to larly hard time). As a result it is likely that we have had, and
have a broader diet, typically feeding on the ground or continue to have, a significant impact upon the health and
aerially, traits that enable them to exploit the diversity of composition of bird communities. Using 40 years’ worth of
resources available (seeds, carrion, and human waste). Non- data collected by the British Trust for Ornithology, Kate
urban comparison species on the other hand feed more Plummer and her colleagues have described increased use of
often in the mid strata and canopy of wooded areas, they are garden feeders by a number species of bird and have shown
more likely to include fruit in their diet and they are more that as a result of the range of food types that are offered,
likely to be specialist insectivores or granivores. But when I the garden bird community is more diverse today than it has
think about the birds I see in urban gardens I do see special- ever been and that in fact more than half of the species of
ists some of the time and that is probably because supple- birds known to breed or winter in the UK can now be seen
mentary garden bird feeding directly supports species with in urban gardens. Moreover the populations of urban birds
quite specific dietary needs (Figure 6.9). As an example in the that use garden feeders are increasing (those that do not are
not) probably due to a combination of increased survival,
enhanced physiological fitness, and increased productivity.
Experimental evidence to support this has also been pro-
vided by Kate Plummer and her colleagues in a related study
of non-urban birds. In this work the researchers explored the
impact of supplementary winter feeding on populations of
Blue Tits Cyanistes caeruleus resident in British woodlands.
Before their experiment the team assessed the body condi-
tion of the birds by measuring the carotenoid concentration
of their feathers, taking advantage of the fact that Blue Tits
moult before winter when the feeding would take place.
Over the winter period they provided some populations of
birds with no additional food, some received fat-rich food-
stuffs, and others were given a fat-rich diet enriched with
vitamin E. During the subsequent breeding season, the team
assessed the body condition of birds and recorded their
Figure 6.9 This Marsh Tit Poecile palustris is taking advantage breeding success. Their results showed that whilst a fat-rich
of a garden bird feeder filled with shelled sunflower seeds
(© Margaret Boyd). continued
Box 6.2 Continued
diet actually led to poorer breeding season body condition, a and disease state of captive house finches in experimental
fat-rich diet with added vitamin E did improve the overwin- conditions. The researchers inoculated individual House Finches
ter survival and breeding condition of birds, particularly those Haemorhous mexicanus with a common bacterial low viru-
who started the winter in poorer shape. These results suggest lence pathogen Mycoplasma gallisepticum and then allo-
that it is the type of food that is provided rather than the provi- cated them each to flocks that had access to different
sion of food per se and that dietary balance rather than sheer numbers of feeders, simulating different feeding densities.
volume is key. So we should think carefully about the quality of Although overall rates of disease transmission were low,
the food that we put out for the birds in our own gardens. they were significantly higher in flocks with higher feeding
Poor diet is only one of a number of potential drawbacks to densities demonstrating that feeding in close proximity to
supplementary garden feeding. As birds are concentrated in one another, or at sites frequented by more birds increases
gardens the risk they face from domestic cats and other preda- disease transmission risk. So if you are going to feed the
tors also increases and it has been estimated that domestic birds make sure that you have a number of feeders in your
cats kill billions of birds annually. There is also evidence that a garden rather than just one, and clean them regularly.
concentration of birds at bird feeders presents an increased risk
of disease transmission, particularly if our feeder hygiene is References
poor. In the UK during the early years of this century the num- Lawson, B., Robinson, R.R., Colvile, K.M., et al. (2012) The
bers of Greenfinch Carduelis chloris and Chaffinch Fringilla emergence and spread of finch trichomonosis in the British
coelebs declined markedly as a result of trichomonosis, a dis- Isles. Philosophical Transactions of the Royal SocietyB
ease caused by the protozoal parasite Trichomonas gallinae. It 367, 2852–63.
is suggested that the disease jumped from pigeons to doves Moyers, S.C., Adelman, J.S., Farine, D.R., et al. (2018) Feeder
and finches when these species were brought into close prox- density enhances house finch disease transmission in
imity at bird feeders (the incidence of the disease began to experimental epidemics. Philosophical Transactions of the
increase shortly after pigeons became markedly more common Royal Society B 373, 20170090.
in gardens), and then spread quickly at feeders where birds fed Palacio, F.X. (2019) Urban exploiters have broader dietary
in close, possibly artificially close, proximity to one another. niches than urban avoiders. Ibis.
Some 50 per cent or 2.5 million greenfinches are thought to Plummer, K.E., Risley, K., Toms, M.P., and Siriwardena, G.
have died between 2005 when the disease reached epidemic (2019) The composition of British bird communities is
level and 2009. In my own garden a Greenfinch is now some- associated with long-term garden bird feeding. Nature
thing remarked upon, a bird that once I took for granted. Communications 10, 2088.
Confirmation that crowded feeds are sites of disease Plummer, K.E., Bearhop S., Leech, D.I., et al. (2018) Effects of
transmission has been reported by Sahnzi Moyers and her winter food provisioning on the phenotypes of breeding
co-workers who carefully monitored the feeding behaviour blue tits. Ecology and Evolution 8, 5059–68.
6.3 Risk and foraging risks of not doing so (which might ultimately be
starvation). For example many birds are reluctant to
Flight path: Mixed species flocks divide up a resource forage far from cover. Titmice, sparrows, and juncos
to minimize competition. page 147. have all been shown to prefer to feed closer to cover
into which they might flee when disturbed or
So far we have considered foraging as an isolated attacked and evidence exists that birds are able to
behaviour but of course in reality finding food is modify their behaviour in response to changing
just one of a number of concurrent activities under- levels of risk. For example Jukka Suhonen found
taken by an individual. The individual doesn’t just that during periods of relatively low predation
have to decide what to eat it also has to decide when risk Crested Tits Parus cristatus, foraging in trees,
to eat it. This might involve storing food during a utilize both high and low branches and feed close to
glut as a way to survive a future shortage, like the trunk and outwards to branch tips. However
the Coal Tits discussed in chapter 3. It might also during years when small mammal populations were
involve weighing up the risks of feeding against the particularly low and Pygmy Owls Glaucidium
passerinum changed their behaviour to hunt birds, which they are exposed. In this section I would like
the tits responded by concentrating their own for- to consider predator avoidance in more detail.
aging closer to tree trunks where they would be less
likely to be attacked.
6.4.1 Camouflage
Key reference
Suhonen, J. (1993) Predation risk influences the use of Concept
foraging sites by tits. Ecology 74, 1197–1203. Camouflage
Lima, S.L., Wiebe, K.L., and Dill, L.M. (1987) Protective When we find it difficult to see a bird because its
cover and the use of space by finches: is closer better? colouration blends with that of its environment
Oikos 50, 225–30.
we think of it as being camouflaged. However, it is
Lima, S.L. (1988) Initiation and termination of daily
important to remember that what one animal sees as
feeding in dark-eyed juncos: influences of predation
being camouflaged another may not. Birds are able to
risk and energy reserves. Oikos 53, 3–11.
see reflected UV light and species that look dull to us
may therefore be very bright to other birds.
On the other hand there are situations in which
birds will take risks, or at least appear to do so. For Many birds are difficult to see. Some simply skulk
example Stephen Lima and his colleagues have and remain inconspicuous, others have evolved
shown that towhees and song sparrows feed further plumage that is camouflaged. My personal experi-
from cover than would be expected if they were ence of camouflage is one of frustration and amaze-
behaving in a way that would minimize the time ment. I know first hand how difficult it can be to
taken to flee to safety. This is possibly because cover find an inconspicuous leaf-warbler amongst a can-
is paradoxically also a risk—many predators make opy of leaves or a straw-coloured bittern on the
ambush attacks from cover and in such cases feeding fringes of a reed bed, and on countless occasions I
in the open might be an advantage. Lima’s observa- have almost trodden on a Ringed Plover Charadrius
tions suggest that the finches he studied optimize hiaticula chick as it crouches pebble-like on a rocky
their behaviour by arriving at a compromise between beach (Figure 6.10). But what evidence is there that
the costs and benefits of proximity to cover. camouflage benefits birds by protecting them from
It has also been shown that when resources are predators rather than from the gaze of a curious
scarce, or competition close to cover is high, subor- birder?
dinate birds (presumed to be those least able to
compete) will take increased risks and feed in the
open. In another study Lima has shown that those
Dark-eyed Juncos Junco hyemalis starting their day
with the lowest energy reserves (stored fat) are more
likely to start feeding in low light when predators
are more difficult to locate and both nocturnal and
diurnal predators may be active. Birds with sufficient
fat stores are more likely to wait until light levels
and therefore relative safety from predators increase.
6.4 Predator avoidance

It is likely that some level of risk is inevitable and
that at some stage of their life-cycle all birds face the
threat of predation. In the preceding section of this
chapter however we saw that by adjusting their Figure 6.10 When immobile this Ringed Plover chick is almost
behaviour birds are able to adjust the level of risk to indistinguishable from the pebbles around it (© Graham Scott).
N = 308
Tits recovered at hawk nests (%)

Key reference 6
Hutta, E., Rytkönen, S., and Solonen, T. (2003) N = 365
Plumage brightness of prey increases predation risk: N = 445
4 N = 537
an among-species comparison. Ecology 84, 1793–9.
Esa Hutta and co-workers have approached this

2
question from an unusual angle. Rather than
attempting to show that camouflage reduces preda-
tion risk they have demonstrated that the inverse is 0
true, i.e. that brightness increases predation risk. To Red Control Red Control
assess vulnerability to predation they looked at the 1994 1995
relative proportions of the remains of bright and
Figure 6.11 The percentages of conspicuous red-painted and
dull plumaged passerine remains found in and inconspicuous yellow-painted Great Tits recovered from the nests of
around Sparrowhawk Accipiter nisus nests and Sparrowhawks during two seasons. N indicates the total number of
known plucking posts over a 30-year period. Their each class of tits painted in each season. From Götmark, F. and
analysis revealed that as they predicted, brightly Olsson, J. (1997) Artificial colour mutation: do red-painted tits
experience increased or decreased predation? Animal Behaviour 53,
plumaged species were overrepresented in the
83–91. Reprinted by permission from Elsevier.
hawks’ diet and were presumably therefore easier
for hunting hawks to catch than were dull plum-
aged, camouflaged, species.
6.4.2 Predator distraction displays
In another study involving Sparrowhawks and
their prey, Götmark and Olsson have dramatically Plovers and other ground nesting birds are gener-
demonstrated the cost of increased conspicuous- ally well camouflaged, as are their eggs and mobile
ness. To do this they manipulated the plumage of young (see Figure 6.10). However in terms of avoid-
young Great Tits while they were still in the nest. ing predation the plovers are better known for their
Great Tits have striking yellow, black, white, and unusually conspicuous behaviour and habit of
greenish plumage which might sound quite con- drawing attention to themselves, behaviour which
spicuous, but is in fact relatively inconspicuous might at first seem paradoxical in the face of a pre-
against the mottled light and shade of a woodland dation threat.
canopy. Some of the birds were made less conspicu- Plover nests are typically on open ground and a
ous by having the white feathers on their cheeks, vigilant bird will detect a threat (a fox or mustelid
wings, and tails painted yellow. Others were made typically) when it is still some distance away.
more conspicuous by having their white feathers Having identified a predator the plover discreetly
painted red. All of the chicks were fitted with num- leaves its nest and walks a little distance from it.
bered metal rings to facilitate individual recogni- The bird will then employ one or more of a number
tion and then allowed to fledge normally. of anti-predator strategies. Plovers that have been
The main predators of fledgling Great Tits are incubating eggs often sit and pretend to incubate,
Sparrowhawks which time the hatching of their allowing the predator to find and flush them. The
own eggs to coincide with the annual titmouse bird then flies to safety leaving the hapless predator
glut. Two weeks after the tits fledged the to search in vain for non-existent eggs.
researchers used a metal detector to search for In other cases if the plover is in long grass and
their rings in the area of Sparrowhawk nests and cannot be easily seen by the hunter, it will scurry
plucking posts. The results of their searches away uttering a high pitched squeaking sound
(Figure 6.11) revealed that red-painted birds were effectively impersonating a small rodent. Typically
38 per cent more likely to be predated then yellow- the predator will give chase and when it has moved
painted birds, evidence that conspicuousness a sufficient distance from the nest or young the
increases predation risk and that inconspicuous- plover will fly to safety. If the predator seems not to
ness (camouflage) decreases it. want to follow it the plover will often run towards
Figure 6.12 This bundle of feathers is a perfectly healthy adult Ringed Plover feigning extreme injury to lure me away from its chicks. Seconds
later it took flight and uttered what I can only describe as a mocking call! (© Graham Scott).
it calling loudly and then at the last moment darting nest, the plover utters an almost mocking call and
away, usually followed by the predator which is by flies to safety.
now well and truly hooked.
There is however another behaviour for which
6.4.3 Tonic immobility
the plovers are renowned, and that I can confirm is
highly effective having fallen for it myself on If these strategies fail and chicks are found, they too
numerous occasions. This is the broken-wing dis- have a ruse by which to effect their escape. When
play. Having identified a threat the plover will they are picked up by a predator the chicks of
stand in a conspicuous position and draw attention ground nesting birds exhibit what is referred to as
to itself with a repetitive pipping call. At the same tonic immobility—basically they become limp and
time it will lower one wing (feigning an injury) and play dead. Because such chicks tend to come in
start to slowly ‘limp’ away. Presented with such an groups, predators often drop ‘dead’ chicks in the
easy target the predator gives chase and the plover hope that they will find another. Of course when
following an irregular path leads it away from its they subsequently return to reclaim their prize they
nest or chicks (chicks crouch immobile in response find it gone. Tonic immobility can be induced if a
to an alarm call from their parent). If the predator chick is presented with a stimulus mimicking two
appears to lose interest the plover exaggerates its forward pointing eyes (like those of a predator) and
plight even more, often falling to the ground and can be sustained for up to 30 minutes if the stimulus
flailing an apparently useless wing (see Figure 6.12). is not removed. During this time the chicks will
But as soon as the predator comes close to grabbing regularly open one eye a little just to check that the
its prey or has moved a sufficient distance from the danger is still present.
6.4.4 Alarm calls researchers found that they varied their call, pri-
marily by adding in more repeats of the terminal dee
When they detect a predator, individuals of most, if
note, in response to increasing predator size (see
not all, bird species produce an alarm call. One of
Figure 6.14A). Furthermore, by playing back a range
the functions of such calls, and indeed of other
of chickadee alarm calls they also showed that con-
forms of alarm behaviour, is probably to inform the
specifics vary their responses to different alarm calls,
predator that it has been detected and that having
taking note of the content of the call and decoding
lost the element of surprise an attack is unlikely to
the potential risk that the predator poses. So for
succeed. In this way alarm calls could act as a
example they respond most strongly to smaller
predator deterrent. The other main function of
predators, which are themselves more likely to attack
alarm calls is to provide flock-mates with the vital
chickadees than are larger predators (Figure 6.14B).
information that a predator has been detected and
Templeton and Greene have also shown that
to stimulate them to take appropriate anti-predator
members of other species in the forest community
actions. Such responses might include becoming
are able to decode the messages transmitted between
silent and inconspicuous (particularly in the case of
alarm calling chickadees. For example Red-breasted
nestlings and dependent young birds), fleeing, or
Nuthatches Sitta canadensis respond to the alarm
somewhat paradoxically making one’s presence
calls of neighbouring Black-capped Chickadees and
known to the predator and even attacking it as we
take note of more than the presence of a threat. In
shall see later in this chapter when we consider
response to chickadee alarm calls stimulated by the
mobbing behaviour.
presence of a Northern Pygmy Owl Glaucidium
Walking in English woodland one of the most
gnoma, a species which also predates nuthatches,
common calls that I hear is a high pitched seet.
they responded with high intensity alarming and
Usually this is the alarm call of a European Robin
mobbing. But when the chickadees’ alarm calls
Erithacus rubecula that has been disturbed by my
were a response to the presence of a Great Horned
presence. Through this call the Robin shares with
Owl Bubo virginianus, a species which is not known
the wider community of woodland birds the infor-
to hunt nuthatches, their anti-predator response
mation that I am there and that I am a potential
was far less strong.
threat (of course I’m not really!). This multi-species
sharing of information is enhanced because the
Key references
alarm calls of most, if not all, of the members of the
Templeton, C.N. and Greene, E. (2007) Nuthatches
community have evolved to become very similar
eavesdrop on variations in heterospecific chickadee
indeed (see Figure 6.13). Typically they are rela- mobbing alarm calls. Proceedings of the National
tively drawn out calls with a rather narrow fre- Academy of Science 104(13), 5479–82.
quency range making them very difficult for a Ridley, A.R., Child, M.F., and Bell, M.B.V. (2007)
predator to locate accurately. This of course is an Interspecific audience effects on the alarm-calling
advantage to the birds in that a predator cannot behaviour of a kleptoparasitic bird. Biology Letters 3,
attack a target that it is unable to locate. 589–91.
At first glance the alarm call system would there-
fore appear to be a relatively simple one. However
Concept
recent research has revealed that in fact it is often
Sentinels
used in quite a sophisticated way. For example it
Single and mixed-species flocks often include individ-
has been shown by Christopher Templeton and his
uals who take on the role of sentinel. These individuals
co-workers that Black-capped Chickadees Poecile
act as a lookout for the flock, devoting more time to
atricapillus vary their alarm call in response to the vigilance and therefore less time to foraging than their
identity of the predator that they have detected. The flock-mates.
chickadees are named for their chick-a-dee-dee call
which is used as an alarm/mobbing call when There is however evidence that heeding the warn-
predators are detected. By exposing chickadees to ings of others may sometimes be a costly behaviour.
models of a range of potential predators, the Fork-tailed Drongo Dicrurus adsimilis are insectivorous
(A)
9 Blackbird
Kilocycles\s
7
5
9 Great Tit
Kilocycles\s
7
5
9 Blue Titmouse
Kilocycles\s
5
9 Chaffinch
Kilocycles\s
Stonechat
(B)
Blackbird
Warber
Garden
Thrush
Mistle
Robin
Wren
8
6
Kilocycles\s
0 1s
Time (s)
Figure 6.13 Sonograms of alarm calls (A) and mobbing calls (B) of a range of coexisting European woodland birds. Note that whereas alarm
calls typically have a narrow frequency range, making them difficult to pinpoint, mobbing calls have a wide frequency range and are easily locked
onto by predators. Note also the convergence in the evolution of both types of call. From Marler, P. (1959) Developments in the study of animal
communication. In Darwin’s Biological Work. Bell, P.R. (ed.) Cambridge University Press, Cambridge.
and tend to take prey by hawking it from the air. However, when in the company of ground-foraging
They will however also take prey from the ground, Pied Babblers Turdoides bicolor, the Drongos take on
particularly when it has been disturbed by a a sentinel role and will alarm in response to both
ground-foraging bird, a form of kleptoparasitism. aerial and terrestrial predators. This of course bene-
When foraging alone Drongos will alarm call in fits the Babblers who, relying upon their Drongo
response to the threat posed by an aerial predator, lookouts, reduce the level of their own vigilance
but they rarely call in response to a terrestrial one. (spending more time foraging) and respond to the
(B)
(A)
40
4.5
Saw-whet
4.0
Number of “chick-a-dee” calls

Number of D notes per call
Pygmy-owl 30
3.5
merlin Cooper’s 20
3.0 Peregrine
kestrel
red tail
2.5 short-eared great-horned 10
gyrfalcon
praine great
2.0 grey
0
bobwhite
1.5 rough-leg
1.0 Control Large Small

20 40 60 80 100 120 140
predator predator
Predator wingspan (cm)
Alarm call treatment
Figure 6.14 (A) Intensity of alarm call (number of dee (D) notes in the call) clearly increases as predator size decreases and chickadees clearly
respond most strongly to hearing alarm calls that are a response to the greater threat posed by the presence of a smaller predator (B). Each
taxonomic group of raptors is represented by a different symbol (⚫ owl; ▲, falcon; ◼, hawk). A bobwhite quail (♢) was used as the procedural
control. The dashed line displays the mean number of D notes per control trial without any stimulus. Adapted from Templeton, C.N., Greene, E., and
Davis, K. (2005) Allometry of alarm calls: Black-capped chickadees encode information about predator size. Science 308, 1935–7. Reprinted with
permission from AAAS.
Drongo alarm by fleeing to the safety of deep cover. birds are recruited and very quickly a small flock of
The intriguing question of course is why do the birds will form, all harassing the unfortunate hunter.
Drongos go to this effort? Amanda Ridley and her Typically, having lost the element of surprise or
colleagues have shown that in some cases they use because it just cannot take any more, the predator
this relationship to their own advantage. Occasionally will move on to hunt elsewhere. Numerous studies
they will alarm dishonestly (i.e. when there is no have demonstrated that mobbing is a successful
predator present) causing the fleeing Babblers to strategy, and most birders will have seen it at work.
drop or leave their own prey which is quickly In fact learning to recognize mobbing behaviour
snapped up by the hungry Drongo. This dishonesty can be a great way to detect predators that you
can persist because it is a strategy that the Drongo might otherwise have overlooked!
uses sparingly and the Babbler is unable to call its Mobbing does however have a potential cost and
bluff. there are reports of predators taking a mobbing bird
that came too close. This is perhaps why birds
tend to cooperate and mob in flocks. Brown and
6.4.5 Mobbing
Hoogland, in a comparative study involving the
Whilst alarm calls appear to have evolved to have a mobbing behaviour of solitary and colonial species
frequency range which reduces the chances that a of swallow, have shown that solitary mobbers are
predator will be able to locate the caller, mobbing forced to take greater risks (coming closer to the
calls in contrast have evolved to be easily located predator) than are mobbers in flocks (Figure 6.15).
(Figure 6.13B). As a strategy, mobbing depends
upon the predator knowing that it has been detected
6.4.6 Flocks and colonies
and that an attempt to hunt will probably result in
failure. Mobbing is most commonly observed when Lowering individual risk and increasing the chance
passerine birds respond to the presence of an aerial of success in mobbing birds is just one of the anti-
predator. It may begin with a single mobbing bird, predator advantages of group living and/or colo-
calling and diving at the predator repeatedly, perhaps nial breeding. Whilst being part of a large and
even striking it. As the behaviour continues other conspicuous group might on the face of it seem to
make a bird more obvious to predators, there is in birds are able to increase the effectiveness of their
fact safety in numbers. By breeding in huge colonies, mobbing behaviour to deter predators, and to
and synchronizing the hatching of their young, sea- simply swamp them with food. There are so many
eggs and chicks available that even the hungriest
of predator populations will make relatively little
(A) (B)
4% impact upon the prey population as a whole.
Conservationists can take advantage of this prin-
ciple by providing food to divert the attention of
predators away from the species that they are trying
35% to protect (see Box 6.3).
At a very simple level a phenomenon known as
Colonial species Solitary species the dilution effect comes into play as group size
increases. If a bird in a flock of one is attacked by
Figure 6.15 The percentage of mobbing actions that are high risk a predator it has a 100 per cent chance of being the
(shaded segments) are lower for colonial swallows mobbing as part of target of the hunter. A bird in a flock of 2 has a 50
a flock (A) than they are for solitary birds (B). From Scott, G.W. (2005) percent chance, and one in a flock of 100 has only
Essential Animal Behavior, Blackwell Publishing, Oxford adapted from
Brown, C. and Hoogland, J.L. (1986) Risk in mobbing for solitary and
a 1 per cent chance (all things being equal) (see for
colonial swallows. Animal Behaviour 34, 1319–23. Reprinted by example Figure 6.16). This effect is clearly at work
permission from Elsevier. in the large seabird colonies described previously
(A)
Probability of attack on individuals
0.14
0.11
0.08
0.06
0.03
0 2–5 6–10 11–20 21–3031–40 41–50 51–6061–100

Flock size class
(B)
30
Mean interscan interval (s)
20
10
0
1–5 6–10 11–15 16–20 21–25 26–30 31–40 41+
Flock size class
Figure 6.16 Increasing flock size results in a decreasing probability that any individual Redshank will be the target of a predator (A), and allows
individuals to forage for longer between bouts of vigilance (scans) (B). From Cresswell, W. (1994) Flocking is an effective anti-predator strategy in
redshanks, Tringa totanus. Animal Behaviour 47, 433–42. Reprinted by permission from Elsevier.
Box 6.3 Feeding predators to protect prey
The Little Tern Sternula albifrons is one of the least common foxes out of their colonies. But in spite of all of this, terns
seabirds breeding in the UK. These terns breed in colonies on remain at risk from aerial predators, in particular from rap-
sandy beaches, just above the strandline and are therefore tors such as the Kestrel Falco tinninculus. So what to do?
at risk of inundation, disturbance and sadly, persecution Although predators are controlled in some conservation
from people—their eggs and chicks are particularly vulner- situations (think of the example of rat eradication pro-
able to predation. Conservation efforts are intensive and grammes on seabird islands) lethal control of one threat-
include 24/7 observation by dedicated volunteers and nature ened species to protect another poses something of an
reserve wardens as well as fencing to keep people, dogs, and ethical dilemma to put it mildly. One innovative solution is to
feed the predator. This diversionary feeding as it is known
0.8 operates under the assumption that a well fed predator
poses a lesser threat. But does it work? Jennifer Smart and
Kestrel predation (LT chicks
0.7
0.6 Arjun Amar have shown that it does.
hour–1 ±95%Cl)
Taking advantage of the fact that Little Tern colonies are

0.5
under intense scrutiny and every predator attempt made by
0.4 a Kestrel can be observed, they compared predator success
0.3 (and tern success) during years when no diversionary feed-
0.2 ing took place and during years when the local Kestrel popu-
0.1 lation was able to feed on dead chicks and mice that were
surplus to the needs of an animal breeding programme. Their
0
noDF DF results (Figure 6.17) demonstrate the effectiveness of this
conservation strategy. Not only were significantly fewer tern
Figure 6.17 The average hourly rate of Kestrel predation on Little chicks taken by Kestrels during years when diversionary
Tern chicks with (grey bar) and without (white bar) diversionary feeding was in place, the predators took fewer items of other
feeding. From Smart, J. and Amar, A. (2018) Diversionary feeding as wild prey species. The researchers estimate that this strategy
a means of reducing raptor predation at seabird breeding colonies.
reduced chick predation from around 275 birds per year to
Journal for Nature Conservation 46, 48–55. Reprinted by permission
around 30, a real success story.
from Elsevier.
and it probably also explains the flocking behav- Cresswell has demonstrated that the larger a
iour of female sea duck such as the Eider Somateria Redshank flock, the lower the probability that a
mollissima who bring together their chicks into given individual will be attacked by predators
often quite large crèches during their first vulner- (Figure 6.16A). The Redshank in the winter popula-
able days at sea. During this period the chicks are tion that he observed faced two basic pressures
easy prey for hungry gulls and there is little that each day—the need to avoid being eaten and the
either mother or chick can do to deter an attacking need to gain enough energy themselves. To an
bird. Instead they rely upon the dilution effect extent the two are in part difficult to reconcile
and the ability of a number of females working because a feeding Redshank often has its head
together to spot danger and respond to it (by div- down and so when actively foraging is far less able
ing and encouraging the chicks to dive) sooner to see approaching predators. However, through
than a mother on her own would. group membership, individual birds are able to
Further evidence that flocking is an effective anti- increase the interval between bouts of vigilance
predator strategy has been provided by Will behaviour and so maximize feeding time
Cresswell who has carried out an exhaustive study (Figure 6.16B). This is because in a sufficiently large
of the relationship between hunting Sparrowhawks group there will by chance always be some individ-
Accipiter nisus and Peregrine Falcons Falco peregri- uals on the lookout. There is an additional level of
nus, and their Redshank Tringa totanus prey. flexibility in this system in that all members of the
flock increase their vigilance levels in response to a I will mention it briefly to round off this discus-
heightened perception of risk—immediately after a sion. Remember that the Redshank Cresswell
predator has been seen in the area for example. observed were attacked by two different predators,
One might expect Redshank that have spotted Sparrowhawk and Peregrine Falcon, both of which
a predator to use an alarm call, and some do. use very different strategies to capture their prey.
Others however do not. How can this be explained? Sparrowhawk are a stealth hunter—typically break-
Cresswell observed that Redshank did call more ing low from dense cover and hoping to snatch sur-
often when escaping from an obvious threat (a raptor prised prey from the ground. Peregrines on the
attack) than they did when the cause of their alarm other hand are pursuit hunters, stooping (a diving
was not apparent (flocks often simply spook them- flight) towards prey from a height and at great speed
selves). Furthermore he also noted more alarm calls and preferring to take airborne prey. Cresswell
by fleeing birds that had been feeding in a habitat noted that the Redshank consistently responded to
that was visually obstructive (i.e. fellow flock mem- these predators in different ways. When attacked
bers were not easy to see) than on an open mud-flat. by a Sparrowhawk they bolt and escape with a low
In the latter habitat they were much more likely to zigzag flight pattern. In response to a Peregrine
escape with a silent and direct fast flight to safety. they freeze and crouch low to the ground. So in just
Both escape behaviours had the same effect on the fractions of a second birds are able to identify a
rest of the flock—causing all of the Redshank in the potential threat, recognize the predator, evaluate its
area to take to the air. So as was suggested previously likely mode of attack and take appropriate evasive
in the chapter, one function of the alarm call does action. An impressive feat, but an essential one—
seem to be to coordinate an escape. Birds that do making a mistake would be fatal.
alarm call, potentially drawing attention to them-
selves, were no more likely than non-callers to be
Summary
targeted by the raptor, so calling in itself is not a
high risk strategy in this case. It is a highly effective Foraging birds utilize a wide range of behavioural
strategy though because a coordinated escape pres- strategies when feeding and that behaviour continues
ents a hunter with a mass of moving targets making to evolve to take advantage of new food resources.
it impossible for it to pick out one to chase—this is Essentially however they forage in an optimal fash-
often referred to as the confusion effect, another ion. The anti-predator behaviour of birds is simi-
anti-predator benefit of flocking. larly diverse. Some species rely upon camouflage;
Will Cresswell made a number of other important some cooperate to confuse a predator. Some take
observations about the behavioural relationship risks, exposing themselves to danger when mob-
between avian predators and their avian prey and bing hunters. The provision of supplementary food
I would recommend that any interested reader take can be an important conservation strategy, but pro-
the time to read his numerous papers. But one of viding the right food and maintaining good feeder
his observations I find particularly intriguing and station hygiene is essential.
C H A PT ER 7
Populations, communities,
and conservation
‘Man, however much he may like to pretend the contrary, is part of nature’
Rachel Carson (1962)
Although birds can be found in almost every corner very often act in concert. In addition the relation-
of the globe it is apparent to even the most casual ships between populations of species which form
observer that they are not distributed evenly. communities (see section 7.2) will mean that a shift
Some places have more species of bird than others. in one population may have consequences for
Furthermore, whilst some individual species have others and so have an impact at the community and
very broad distributions, others are often found ecological network level.
only in a particular type of place or even in just one
Concept
very restricted area. To explain these patterns we
have to consider some of the characteristics of bird Populations can be defined as those members of
a species which interact and have the potential to
populations and communities, particularly if essen-
interbreed.
tial conservation efforts are to be a success.
Chapter overview 7.1.1 Life history strategies influence

population growth
7.1 Populations
7.2 Communities Some species have a naturally low capacity for
7.3 Extinction and conservation population growth because of their particular
life history strategy. Populations of larger birds
with delayed maturation and small or infrequent
7.1 Populations clutches are typically slow to grow. For example
Bird populations vary in size dramatically. Pop- although considerable conservation efforts have been
ulations of some species, such as the African Red- made on their behalf the recovery of the Californian
Billed Quelea Quelea quelea are counted in their Condor Gymnogyps californianus (Figure 7.1) has
millions whilst populations of island endemics been painfully slow. These birds have a life span of
might include only a handful of individuals. some 50 years and take at least six to reach sexual
Some populations appear to be stable (but fluctuate maturity. When they have found a mate and do
around a mean from year to year), others are grow- begin to breed their natural rate of productivity is
ing, but many are a shrinking at such a rate that very low. In 1987 only 22 of these magnificent birds
they are of immediate conservation concern. The remained and all of them were captured and taken
factors governing both population size per se and into captivity as the basis of a captive breeding
trends in population size change are numerous and programme. Eventually birds were returned to the
DOI: 10.1093/oso/9780198804741.003.0007
P O P U L AT I O N S, C O M M U N I T I E S, A N D C O N S E R VAT I O N 141
Figure 7.1 This wing-tagged Californian Condor soaring above the Big Sur is the living embodiment of a conservation success story
© Peter Dunn.
wild and the conservation programme is a success, 2.0

but the total population remains small. By 2017 it
had only grown to 463 birds (290 in the wild and 1.5
the remainder in captivity).
CBC Index
Small passerines on the other hand have a much

1.0
higher capacity for population growth. A pair of
European Starling for example can reproduce at one
year old and can produce 10 chicks per year (from 0.5
two clutches of five eggs) for several years. As a
dramatic example of the kind of population growth 0.0
that can result from such a life history strategy con- 1960 1970 1980 1990 2000
sider the fact that in 1890 Eugene Scheifflen intro- Year
duced a founder population of between 60 and 110
Figure 7.2 The population of Starlings in the UK declined
(estimates vary) European Starling into New York’s dramatically over the period 1960 to 2000 (solid line and 95 per cent
Central Park and that in 2009 they were estimated C.I.—dotted lines). The decline in the index used (derived from the
to be the most numerous bird in the USA (there British Trust for Ornithology Common Birds Census) equates to a loss
were estimated to be more than 200 million of of more than 50 per cent of the UK population. Robinson, R.A,
Siriwardena, G.M., and Crick, H.Q.P. (2005) Status and population
them). It took them around 50 years to colonize the
trends of Starling Sturnus vulgaris in Great Britain. Bird Study 52,
USA from east to west and as they did so they 252–60. Reproduced with permission from the British Trust for
wreaked ecological havoc out-competing native Ornithology.
species for access to nest cavities. Today in the USA
these starlings are considered a pest species, spread- Starling is a bird of conservation concern. Although
ing zoonotic disease and causing significant agri- not uncommon, the UK population has declined
cultural losses. Where necessary their numbers are rapidly in recent years (Figure 7.2), possibly as a
controlled through culling by the application of a result of changes in agricultural practice that have
bird-specific pesticide (DRC1339) which is adminis- reduced food availability and as a result of a loss
tered as poisoned bait. Paradoxically in the UK the of suitable nest sites as building regulations and
standards reduce the number of cavities available will go on to consider some of the ways in which
in domestic roof spaces. population changes are involved in the structuring
of bird communities.
Concept Populations grow as a result of increased product-
Zoonoses are diseases which can potentially be ivity and/or decreased mortality. This may be pos-
transmitted from animals to humans, several are known sible because resources become more abundant as a
to be transmitted from birds to man directly and others result of a climate shift, a human intervention or
involve birds as an intermediate host or vector. See for even the misfortunes of another species. Or it could
example Abulreesh, H., Goulder, R., and Scott, G.W. (2007) be a result of a decrease in predator pressure, or in
Wild birds and human pathogens in the context of ringing a conservation context because of an increase in pro-
and migration. Ringing and Migration 23(4),193–200. tection. On the other hand populations decline when
productivity falls and/or mortality increases, per-
haps because predator pressure increases, or a
parasite or disease invades a population. It could be a
7.1.2 Population change
result of increased competition as a result of a species
In spite of their intrinsic capacity for growth some introduction or a range expansion. Alternatively it
populations are in decline or have their growth could be the result of a shortage in resources because
limited in some way. Throughout the remainder of of poor weather or habitat loss. It could simply be that
this chapter we will largely focus upon examples of an extreme weather event kills lots of birds. Box 7.1
such populations. We will consider a range of illustrates the impact of species introductions, com-
factors that check population growth and then we petition, and disease upon bird populations.
Box 7.1 Aliens, pathogens, and competition
During the second half of the nineteenth century House sites traditionally occupied by sparrows. It certainly looked
Sparrows Passer domesticus were introduced to several sites like the finches were competitively dominant with respect to
across the USA. Today this successful generalist is one of the the sparrows.
most common birds in the USA. It is a pest in many contexts Evidence to support this hypothesis came as a result of an
and is held responsible for preventing the expansion of unusual natural experiment, one which in itself provides an
populations of native species because it out-competes them excellent example of the impact of pathogens as a cause of
for resources. However, in the second half of the twenti- density dependent population decline. In the 1990s the
eth century things started to go badly for the sparrow, it eastern House Finch population was still growing strongly
lost ground to another alien invader—the House Finch and expanding its range but then in the winter of 1993–
Carpodacus mexicanus. 1994 birders in the state of Maryland began to report cases
House Finches were translocated from their native west- of a House Finch specific conjunctivitis. Dubbed ‘House Finch
ern USA to Long Island in the east in 1940. This new eastern disease’ this was found to be caused by a bacterium,
population struggled to get a foot-hold initially but eventu- Mycoplasma gallisepticum, a pathogen previously restricted
ally it did establish itself and then quickly spread throughout to domestic poultry (the same pathogen discussed in Box
the eastern states. As the finches spread it was noted that 6.2). Subsequent research revealed that the disease was
where they coexisted, sparrow numbers seemed to be fall- highly contagious and highly pathogenic—as Figure 7.3
ing. Was this more than a coincidence? The diets of the two shows, as many as 60 per cent of the birds in infected popu-
species are very similar (both eat mainly seeds and vegeta- lations died within five years of the disease emerging. It also
tion); they are known to fight over resources when they spread very quickly, having reached Texas, Missouri, and
meet; and, there were reports that finches were breeding at Minesota by 1997.
It seems likely that this pathogen was able to spread so

Population size (% of expected) 120 quickly precisely because of the ecological traits that made
100 the finches such a successful species in the first place—their
ability to tolerate one another and feed in large compact
80 flocks (sites of infection) and their ability to rapidly disperse
and colonize new areas (enhancing the geographical spread
60
of the disease).
40 What about the sparrows? Remember that as the
House Finch population increased a decrease in sparrow
20 numbers was recorded. If the population dynamics of the
two species are inter-linked such that finch numbers are
–1 0 1 2 3 4 5
the check on the sparrow population, we should expect to
Years since epizootic began
see the sparrows, being immune to Mycoplasma gallisep-
Figure 7.3 Changes in House Finch abundance following the ticum, to bounce back once the competitive pressure was
emergence of Mycoplasma gallisepticum in a population. The data released. This is exactly what has been recorded by the
are expressed as changes relative to 100 per cent (year -1, or one veritable army of professional and amateur ornithologists
year prior to pathogen emergence). From Hochachka, W.M. and in the USA who take part in the annual Christmas Bird
Dhondt A.A. (2000) Density-dependent decline of host abundance Count (Figure 7.4).
resulting from a new infectious disease. Proceedings of the
National Academy of Science 97(10), 5303–6. Copyright National
Academy of Sciences, USA.
2.5
2.0 Figure 7.4 Abundance (log transformed) of House
In(counts/party-hour)
1.5 Sparrows (solid line and dotted line) and House Finches
1.0 (points) recorded in the Christmas Bird Count (1970–2005).
The shift from a solid to dotted line in the case of the
0.5
sparrows indicates the change in the direction of their
0
population trend coincident with the emergence of
–0.5 Mycoplasma gallisepticum in 1993/4. From Cooper, C.B.,
–1.0 Hochachka, W.M., and Dhondt, A.A. (2007) Contrasting
–1.5 natural experiments confirm competition between House
1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 Finches and House Sparrows. Ecology 88, 864–70.
have on occasion resulted in local hirundine popu-

Key reference lation reductions of as much as 90 per cent.
Newton, I. (2007) Weather-related mass mortality
events in migrants. Ibis 149, 453–67.
Key reference
Kluijver, H.N. (1966) Regulation of a bird population.
So, for example it is not unusual for populations of
Ostrich (supplement) 6, 389–96.
small passerines to crash during a very cold winter.
Similarly populations of migrants are often dramat-
ically reduced as a result of extreme climate events Populations that have suffered these crashes often
either during their migration or shortly after arrival rebound during the following years (assuming that
at their breeding grounds. In his excellent review of mass mortality events are not repeated) because this
this phenomenon, Ian Newton reports that in 1993 a mortality event may have lessened competition for
single tornado/storm event off the Louisiana coast nest sites/territories and food resources during the
resulted in the death of more than 40,000 migrating following spring, allowing a productivity increase
birds, and that unseasonal cold snaps in Europe for those birds fortunate enough to have survived.
Natural experiments like this have been dupli- breed (I put out nest boxes and birds nest in shrubs,
cated under controlled conditions and similar trees, and under my eaves and roof tiles). Life for
effects measured. For example Hans Kluijver has birds in my garden is not however without risk;
simulated an increase in breeding season mortality local cats no doubt take their share of fledglings.
in Great Tit populations isolated on a Dutch island. Just 3 km from home is my local nature reserve
He found that by removing a little over half of which although small supports very many more
the breeding season population (adult birds and birds. This site, which is also on the edge of a vil-
eggs/chicks) he was able to stimulate a significant lage, consists of patches of reed- and rush-fringed
increase in the survival of the remaining population open water, a small woodland, wet grassland, and
(adults and birds in their first year) over the follow- muddy flashes. I regularly record more than 30
ing winter, presumably because competition for species in a visit and more than 60 species over the
winter food had been reduced. In this situation it course of a year. Here I record flocks of 20 or 30 Tree
seems that winter food availability (or possibly Sparrows Passer montanus and of 50 to 100 Starlings
access to winter roost sites) is the factor that limits regularly. So why are these two bird communi-
growth of this tit population. But populations may ties so different? Essentially the nature reserve
be limited by a range of factors. In one of the Scottish provides birds with the same resources as my
Blue Tit populations with which I am familiar, the garden—food, water, and nest sites—but of course
population was not limited by food availability it does it on a different scale. It provides a wider
during the winter (I personally provided more than range of seeds and fruits, insects, small mammals,
was required at feeding stations), but was limited fishes, and amphibians as potential food. There are
by competition for nest sites—by putting out large nest-boxes, shrubs, trees, scrub, ditches, and banks
numbers of nest boxes I was able to record a signifi- for nests; islands for safe roosting by gulls; mud
cant increase in the local population. You may recall and wet grassland for feeding waders, shallow
from Box 5.7 that Jan Komdeur and colleagues were water and submerged vegetation for dabbling
able to increase the world population of Seychelles duck, and deep water for diving duck and grebes.
Warbler by increasing the number of potential The nature reserve is both larger than my garden
breeding territories for the birds. We will consider and more complex ecologically. It provides a
competition and population regulation again later greater number of potential niches and as we will
in this chapter when we consider its impact upon see in section 7.2, it therefore has the potential to
bird community structure. support a community that includes a greater num-
ber of species.
Flight path: Space to breed, availability of nest Populations of species of birds (those members of
sites and/or territories can limit productivity and drive
a species living and interbreeding in a particular
changes in mating systems. page 116.
area) do not generally exist in isolation. They each
live alongside populations of several other species
7.2 Communities forming multi-species communities. In some cases
the member species of a community may initially
In my garden, on the edge of a small village in the appear to have little to do with one another, simply
north of England, I might record as many as ten existing in the same place. In others however the
species of bird in a day and as many as 15 over the relationship between species is very clear. For
course of a year, the biggest flocks I record are of example, in Scandinavian woodlands Coal Tits
between six and ten House Sparrows Passer domesti- Periparus ater and Pygmy Owls Glaucidium passer-
cus. My garden is not particularly rich in birds but it nium are members of the same bird community, and
does provide the requirements of the particular one (the tit) is the food of the other. The Pygmy Owl
community found there. It provides water (I have a has the same relationship with Willow Tits Poecile
small pond), food (I put out seeds, I tolerate some montanus in the community, and as we will see later
weeds, and the plants that I cultivate support a in this chapter the ecologies of the two tit species
bewildering array of insect pests), and places to interact such that the density of one has an effect
upon the population of the other (but this is not a of ecological theories developed as a result of stud-
predator/prey relationship). ies that have been made of island systems and are
Typically a bird community will consist of a small often collectively referred to as island biogeography.
number of species that are very numerous, and
smaller numbers of less common species. Each of Key references
these will have a particular ecological role and will be MacArthur, R.H. and Wilson, E.O. (1967) The theory
an intrinsic part of the ecological network of which the of island biogeography. Princeton University Press,
community is a constituent part. As we have already Princeton.
Tzung-Su, D., Hsiao-Wei, Y., Shu, G., et al. (2006)
seen some species will be the food of others, some will
Macro-scale bird species richness patterns of the East
prey upon non-avian animal members of the net- Asian mainland and islands: energy, area and
work’s food web, others will be plant ‘predators’, but isolation. Journal of Biogeography 33, 683–93.
some will also be pollinators and seed dispersers.
In their now classic 1967 book Robert MacArthur and
Edward O. Wilson described another general phe-
7.2.1 Communities are dynamic
nomenon of island biogeography, the fact that bigger
Although I have a pretty good idea that the commu- islands typically have more species than do those of
nity of birds in my garden will be the same tomorrow smaller islands. In fact their data suggest that each
as it was today it would be wrong to think of commu- ten-fold increase in island size is correlated with a
nities as being fixed. Fifty years ago Collared Doves ten-fold increase in species number. Research by
Streptopelia decaocto would have been unknown in our Tzung-su and colleagues who have studied the avian
village. These doves expanded their range north- communities of East Asian islands provides part of
wards to colonize most of Europe over the course of the explanation for this phenomenon. As would be
the twentieth century. Ten years ago they woke me up expected Tzung-Su and colleagues found that there
in the morning with their cooing call. Sadly today they were more species of birds on larger East Asian
are a relative rarity probably as a result of the tricho- islands, but they have shown that species richness is
monosis epidemic that I discussed in Box 6.2. also positively related to a measure of habitat hetero-
Communities change as a result of the immigra- geneity, in this case an index of vegetation productiv-
tion of new species and the extinction of old ones ity. We will return to this link between species
and community stability is presumed to be achieved diversity and habitat diversity later in this chapter.
when immigration and extinction rates are bal- In the case of the results described by Tzung-su,
anced (see Figure 7.5). the islands concerned are real oceanic islands, i.e.
This apparent community stability is the basis of a land surrounded by sea, but if we were to think of
concept termed equilibrium theory, one of a group islands as being one habitat surrounded by another,
Immigration rate
Extinction rate
R2 Figure 7.5 The number of species (species richness) on an island of

a given size represents a balance between rates of immigration and
R1 R3
extinction. The equilibrium point (number of species present) will vary
R2 in relation to both the size of the island and to its proximity to a
mainland. In the figure a distant, small island has R1 species, a
closer, small island and a larger, distant island both have R2, and a
Island Species Richness large, close island has R3.
we can shift our thinking to consider woodland The second point that I want to draw from the
fragments as islands in a ‘sea’ of grassland for theory of island biogeography concerns island iso-
example, and as Figure 7.6 shows, the species–area lation. You will recall (from Figure 7.5) that islands
relationship still applies. When Robyn Wethered closer to one another, or to a mainland (or in the
and Michael Lawes surveyed the bird communities case of habitat islands—those that are part of a
of fragmented montane forests in South Africa matrix of similar habitats or close to a significant
they found a very strong relationship between for- contiguous area of that habitat), have a greater
est fragment area and the number of bird species potential for colonization by new species. This means
that fragments supported. that in addition to island size, island connectivity
1.69
1.64
Log15Species richness
1.59
1.54
Figure 7.6 The number of species of bird present in a
1.49
natural montane forest fragment increases with the area of
the fragment. This relationship is apparent when the natural
1.44
forest is surrounded by natural grassland (closed symbols,
solid line) and when it is surrounded by a habitat matrix that
1.39
includes artificial forest plantations (open symbols, solid line).
From Wethered, R. and Lawes, M.J. (2003) Matrix effects on
1.34 bird assemblages in fragmented Afromontane forests in South
–0.50 0.00 0.50 1.00 1.50 2.00 2.50 3.00 Africa. Biological Conservation 114, 327–340. With
Log10Area (ha) permission from Elsevier.
0.9
(corrected for area and habitat effects)
0.6
0.3
Species richness
0.0
–0.3
–0.6
Figure 7.7 The density of wooded banks (a measure of

–0.9
habitat connectivity) is a key determinant of species richness
in both the eastern Netherlands (top line) and the central/
–1.2 southern Netherlands (bottom line). van Dorp, D. and
Opdam, P.F.M. (1987) Effects of patch size, isolation and
2 3 5 10 15 20 25 30 regional abundance on forest bird communities. Landscape
Density of wooded banks (m/ha) Ecology 1, 59–73. Reprinted by permission from Springer.
is also a key determinant of observed species

Flight path: Adaptive radiations facilitate niche
richness.
divergence and specialization. page 10.
Whilst carrying out a study of the woodland bird
communities of the Netherlands, van Dorp and 7.2.2 Niche divergence
Opdam have also confirmed woodland patch size is
the single most significant determinant of bird com- You will recall that in chapter 1 I discussed the
munity size, but they have also demonstrated the mechanisms of natural selection and adaptive radi-
importance of habitat connectivity and the proxim- ation by which individual species within communi-
ity of patches to one another (Figure 7.7). In 1987, ties evolve to coexist by specializing in their ecology
when they conducted their work, only 8 per cent of in some way so as to avoid or at least minimize
the Netherlands were wooded and all of the wood- inter-specific competition. We saw for example that
land fragments were scattered throughout an agri- through beak specialization the Charidriiform
cultural landscape. However, in some parts of the waders are able to feed alongside one another in
country the density of small woodland fragments multi-species flocks on estuarine mud-flats and
was greater than in others (i.e. fragments were Box 7.2 illustrates niche separation in a community
closer to one another) and were to some extent con- of river birds. The Geospizid finches of the Galapagos
nected to one another by wooded ditches. Van Dorp islands have evolved beak morphologies which
and Opdam found that those woodlands that were allow them to co-exist and exploit the full range of
part of a matrix of similar habitats interconnected feeding opportunities available to them. This is pos-
by wooded ditches supported a richer bird commu- sible because faced with an array of different feed-
nity than did very isolated woodlands. ing opportunities at a single site the birds are able to
Box 7.2 Niche segregation in a riparian community
The fast-flowing mountain streams of the Himalaya are Plumbeous Water Redstarts foraged along stream edges
thought to be home to more species of specialist riparian and in stream centres where they tended to fly-catch above
birds than any other river system. However, until Sebastian dry boulders and occasionally pick between them. In con-
Buckton and Steve Ormerod made detailed observations of trast White-capped Water Redstarts favoured stream mar-
the behaviour of these birds and compared their body meas- gins where they foraged amongst dry boulders, only
urements, no ecologist had attempted to explain the mech- occasionally fly-catching or picking food from the splash
anisms by which they coexist. Working in four valleys in zone. The two forktails also exhibited micro-habitat based
central Nepal, the researchers studied five species of segregation; the Spotted Forktails preferring dry areas and
insectivore: the Spotted Forktail Enicurus maculates, Little litter and the Little Forktails utilizing the splash zone where
Forktail Enicurus scouleri, White-capped Water Redstart they fed on wet boulders and submerged gravels. Faecal
Chiamorrornis leucocephalus, Plumbeous Water Redstart, analysis revealed that by using the available micro-habitats
Rhyacornis fuliginosus, and Brown Dipper Cinclus pallasii. in this way the five species were able to some degree to
They captured and measured examples of each species, col- avoid competition and specialize to some extent in their
lected their faeces (to determine diet), and recorded how diets (see Figure 7.8). Although it is clear from Figure 7.8
each of them used riverine microhabitats whilst foraging. that there is considerable overlap in prey taken, it is also
They found that the birds spent between 50 per cent clear that the two more aquatic species, Brown Dipper and
(Brown Dipper) and more than 80 per cent (Forktails) of Plumbeous Water Redstart, show least overlap and the
their time foraging, but that the species foraged in different three less aquatic species are also separated from one
ways and in different places from one another, presumably another. Furthermore the sizes of individual prey items
therefore minimizing competition. The Brown Dipper was selected was also found to further contribute to dietary
the only species to forage underwater (a behaviour charac- separation. For example although both Brown Dipper and
teristic of dippers the world over), and was observed at
both the edges of streams and in their centres. Similarly continued
Box 7.2 Continued
Plecoptera
Simuliidae
4
3.5
2.5 LF
SF
Axis 2
2 PWR
WWR
1.5
BD
1
0.5
Chironomidae 0
Terrestrial prey 0 1 2 3 4 5 6
Axis 1
Ephemeroptera
Coleoptera Trichoptera
Terrestrial prey Diptera
Aquatic prey
Figure 7.8 Prey selection as an indicator of niche segregation in Little Forktail (LF), Spotted Forktail (SF), Plumbeous Water Redstart
(PWR), White-capped Water Redstart (WWR), and Brown Dipper (BD). From Buckton, S.T. and Ormerod, S.J. (2008) Niche segregation of
Himalayan river birds. Journal of Field Ornithology 79(2), 176–85.
Little Forktails fed on Ephemeroptera, those individuals iour. In this particular example the researchers did not
eaten by dippers were considerable larger. observe inter-specific aggression and so it seems likely that
It is clear therefore that the members of this particular the species have evolved to complement one another rather
community of birds are able to coexist because they each than having achieved resource partitioning as a result of
specialize to some extent in aspects of their foraging behav- intense competition.
specialize and each therefore occupies a different what it eats etc.). However when we consider the
feeding niche. The kind of adaptive radiation exem- ecology of birds as members of particular ecological
plified by the Galapagos finches is possible because networks and avian communities we most com-
the ancestral finch colonized an island system that monly record a sub-set of the fundamental niche
contained an array of vacant niches and this is a termed the realized niche. This is that part of the
fundamental part of the explanation for the species fundamental niche that the bird can actually use at
area relationship previously discussed—quite sim- that time—being effectively squeezed as it is between
ply larger islands have more potential niches and so other competing species.
can support a greater number of species.
Although we often focus on feeding behaviour
7.2.3 Niche shifts, ecological release,
when we discuss the niche it is in fact a far broader
concept. Each species of bird has a fundamental
and competition
niche that can be described as being the ecological The competitive exclusion principle dictates that no
space in which it can exist (where it is, what it does, two species may occupy the same niche at the same
time and in the same place, and so where species two forms of inter-specific competition (exploitation
overlap in range they have evolved competitively or competition and interference competition) and the
through complementarity to each occupy a smaller actions of a predator. The communities that they have
realized niche. This is perhaps most apparent when a studied include four species: the diminutive Coal Tit
community shift occurs and competitive pressure is Periparus ater, the larger Crested Tit Lophophanes cris-
removed, with the result that a species expands its tatus, the Willow Tit Poecile montanus, and the Pygmy
ecology and moves beyond the confines of the real- Owl Glaucidium passerinum which is a tit predator.
ized niche. For example where they co-occur, Yellow-
rumped Warblers Dendroica coronata and Black- Key reference
throated Green Warblers Dendroica virens exhibit Kullberg, C. and Ekman, J. (2000) Does predation
niche segregation and both utilize different areas of maintain tit community diversity? Oikos 89, 41–5.
the spruce trees in which they forage. The Yellow-
rumped Warblers concentrate their activity in the Throughout Scandinavia these tits are found sym-
bottom six feet or so of the tree whilst the Black- patrically and when they are the birds segregate
throated Green Warblers feed in the top part of the when feeding in a manner similar to the Dendroica
tree. In fact there can be other species of Dendroica warblers that we have just discussed. The smaller
warbler using the same trees and under such condi- Coal Tits forage closer to branch tips and the larger
tions foraging area specialisms can become even Crested and Willow Tits utilize the areas of the tree
more marked. In some parts of their ranges these two closer to the trunk. But on islands where there are
species do not co-occur and when the Black-Throated only Coal Tits present they forage throughout the
Green Warbler is absent the Yellow-rumped Warbler tree having undergone an apparent niche expansion.
undergoes a niche expansion (sometimes referred to Coal Tit-only islands are occasionally colonized
as a competitive release) and forages 30 per cent by either Willow or Crested Tits but they seem to be
higher into the tree. Interestingly when the situation unable to establish stable populations. Coal Tits are
is reversed and it is the Yellow-rumped Warbler that also more efficient foragers than either Willow Tits
is absent, the Black-throated Green Warbler does not or Crested Tits and are superior in exploitation
exhibit a shift in niche. This suggests strongly that competition for food. The may also out-compete the
this is behaviourally and ecologically the dominant larger species because they are more productive,
species and that its presence dictates the realized having up to two large broods per season when
niche breadth of the Yellow-rumped Warbler. Crested and Willow Tits manage only a single,
smaller brood each year.
Flight path: Birds segregate when feeding to
minimize competition. page 10 and 127. Flight path: The presence of a predator can alter
feeding behaviour. page 130.
Key reference However the situation changes when Pygmy Owls

Morse, D.H. (1980) Foraging and coexistence of are present on an island. In these situations the
spruce-wood warblers. Living Bird 18, 7–25. larger Crested and Willow Tits exploit their social
dominance over Coal Tits and monopolize the safer
The fact that one member of the spruce warbler feeding areas close to the tree trunk through inter-
community dictates the feeding opportunities of ference competition. This forces the Coal Tits to for-
another is an excellent example of the role of age in risky areas on the outside of the tree and as a
competition in structuring bird communities. It is result they suffer disproportionately from owl pre-
often the case however that community structure is dation. Because the owls limit the Coal Tit popula-
also strongly influenced by a range of factors that tion, exploitation competition becomes irrelevant
have a cumulative effect. For example Cecilia and a stable community of the three tit species
Kullberg and Jan Ekman have shown that the becomes possible. In this situation, the Pygmy Owl
structure of the European tit community found on is clearly acting as a keystone predator and its
Scandinavian islands is a result of an interaction of actions maintain community diversity.
7.3 Extinction and conservation
Number of extinctions
100
When a population shrinks below a minimum viable 75

size it becomes effectively extinct. It no longer fulfils 50
an ecological role and it no longer has the capacity to 25
recover and grow. Without human assistance (and
in many cases even with it) such populations shrink 0
1500 1600 1700 1800 1900 2006
until there are no birds left and they become extinct Year
in the traditional sense of the word. If another popu- Extinctions observed Extinctions prevented
lation of the same species exists in another place Extinct Extinct in the Wild
there is the chance that natural re-colonization will Critically Endangered Critically Endangered
(Possibly Extinct) (Possibly Extinct in the Wild)
occur as has happened in Scotland in the case of the
Extant
Osprey. This species became extinct in Scotland in
1916 (having already been lost in England in 1840), Figure 7.9 Estimated numbers of bird extinctions and of numbers
but in 1954 a pair returned to breed. Since that time, of critically endangered bird species in the past five centuries. The
thanks to the conservation efforts of many individuals inset bird, the Atitlàn Grebe, Podiymbus gigas was found on lake
Atitlàn, Guatemala. It became extinct in 1986. From Rodrigues,
and organizations, the British population has grown
A.S. (2006) Are global conservation efforts successful? Science 313,
to around 150 pairs. 1051–52. Reprinted with permission from AAAS.
If natural re-colonization is unlikely, then conser-
vation efforts might result in the successful re- For example species with a very narrow geo-
introduction of the species, moving members of a sur- graphical or ecological range are at particular risk,
viving population into the area to be colonized. This birds found on just one oceanic island, or extreme
strategy was used to re-introduce the Osprey to south- specialists for example. Loss of habitat in such a
ern England when it became apparent that a rapid situation could be catastrophic. Conservation efforts
natural spread southwards from Scotland was unlikely. can however make a difference in such situations.
However, as we all know, there comes a point Recall that Jan Komdeur and his colleagues greatly
when a species goes the way of the Dodo Raphus cuc- increased the world population of the Seychelles
ullatus, the Passenger Pigeon Ectopistes migratorius, Warbler by trans-locating a group of birds to a sec-
and the Great Auk Penguinius impennis, when the ond island (see chapter 5).
last population shrinks to the point that the last indi-
viduals die, then the species becomes extinct and is Key reference
extinct for ever. In 2006 the IUCN (International Diamond, J.M., Bishop, K.D., and van Balen, S. (1987)
Union for the Conservation of Nature) stated that Bird survival in an isolated Javan woodland: Island or
135 bird species had become extinct since the year mirror? Conservation Biology 7, 39–52.
1500. A sobering thought, particularly when one
takes into account the rate of increase in extinction However, even though the threat to the warblers is
rate over the same time period (Figure 7.9). lessened, these small populations remain particu-
Clearly, small populations are particularly vul- larly vulnerable. There is often little scope for move-
nerable to extinction, but small numbers alone how- ment of individuals between such populations and
ever do not explain what makes a species vulnerable each is in itself vulnerable by virtue of its small size.
to extinction. After all, the Passenger Pigeon went For example Jared Diamond and co-workers have
from being one of the most numerous birds known reported that of the birds in the Bogor Bogor
to being extinct in a very short period—birds that Arboretum and Botanical Garden, Java, a green
are hunted by man, but which man makes no effort space which had been isolated from similar habitats
to harvest in a sustainable way are at particular risk. for 50 years at the time of Diamond’s work, 75 per
A number of factors make one species more likely to cent of those species with a small initial population
become extinct than another, and when a number of became extinct, whereas all of the species with an
these coincide the odds are not good. initially large population survived.
Small populations, or populations that have Warbler Vermivora bachmanii is thought to have
rapidly grown from a small founder population, become extinct in the 1960s as a result of the defor-
face another problem—reduced genetic diversity— estation of Cuban forests to make way for sugar
which may make them more susceptible to emer- cane plantations.
gent diseases because they are unable to evolve
resistance. This could for example explain the
7.3.1 Conservation can be a success
susceptibility of the House Finch to Mycoplasma
gallisepticum. Earlier in this section I cited the sobering statistics
Species with low population densities, or large provided by Ana Rodrigues which bring home the
range requirements (such as the larger birds of scale of the threat of extinction faced by birds.
prey) are particularly vulnerable, their habitats are However we should not lose hope. Throughout
susceptible to fragmentation and encounters with this chapter and elsewhere in this book I have
potential mates can become infrequent. We have described examples of monitoring programmes,
already seen that a species with a naturally low rate nest-box schemes, habitat management, breeding
of productivity is less able to expand its population; programmes, re-introductions and translocations,
similarly species with low dispersal potential are at and other practical conservation efforts. The human
risk. They simply lack the ability to spread. Island love of, and admiration for, birds is such that armies
rail species are an excellent example of this phe- of citizen scientists can be mobilized across the
nomenon. Many have lost the ability to fly (in some globe to raise funds and carry out practical work in
cases they are psychologically flightless even an effort to conserve birds and thereby conserve the
though they retain the mechanical ability). Most, if ecosystems that both we and birds are part of. But is
not all, are threatened with extinction. it working? I think that it is. Ana Rodrigues pro-
Migrants rely upon multiple locations and stop- vides evidence that the tide is turning (Figure 7.10)
ping off points between them and so are particu- and at the scale of my own experience I can see
larly susceptible to habitat loss. They are often birds in the UK today that were locally extinct in my
funnelled through geographical bottlenecks where memory and that conservation efforts have restored
predators can concentrate their effect and in some to us. As a bird ringer and birder I can see the pas-
cases, such as the North American warblers, have sion and dedication of private individuals for their
very restricted wintering grounds. A single hurri- own conservation actions and as an academic I am
cane could make a species extinct just because it aware of the advances in our understanding that
destroys the forests of a single Caribbean island. leaders in the field of ornithology are making. But
This scenario is not at all far fetched—Bachman’s good science alone will not be enough, as Box 7.3
9950
Number of bird species
9900
9850
9800
9750
1500 1600 1700 1800 1900 2006 Figure 7.10 The estimated impact of global
Year conservation actions to prevent bird extinctions. In the last
100 or so years conservation efforts have resulted in more
Expected number of species in absence of human activities
Observed number of species
than 30 species being brought back from the brink of
Predicted number of species in absence of conservation action extinction. From Rodrigues, A.S. (2006) Are global
Impact of human activities conservation efforts successful? Science 313, 1051–2.
Impact of conservation action Reprinted with permission from AAAS.
Box 7.3 How much does conservation cost?
Governments, non-governmental organizations and char- location. But Antonio Barbosa and José Tella have attempted
ities, and concerned private individuals invest huge amounts to answer the question in the case of one bird species, Lear’s
of money in conservation projects annually. But how much Macaw Anodorhynchus leari. When it was discovered in
does it actually cost to save a species from extinction? Well north-eastern Brazil Lear’s Macaw was already rare, it had
there is no single answer to that question; obviously the been hunted for food, persecuted as a crop pest, captured
costs incurred will vary from case to case and location to for the pet trade, and suffered as a result of habitat loss. In
(A)
(B) (C)
Figure 7.11 Birders visit north-eastern Brazil specifically to see the rare Lear’s Macaw Anodorhynchus leari (A; © José L. Tella). While they
are there, birders contribute to the local economy and conservation efforts by buying souvenirs like these models (B; © José L. Tella) and
baskets (C; © Simone Tenório) made from the wood and leaves of the licuri palm.
1978, when it was first recognized as a distinct species, the Ornithological tourism supports four small companies who
global population was estimated to be only 60 birds but as guide around 50 tourists per year to view the birds
a result of a mixture of in situ and ex situ conservation meas- (Figure 7.11A); generating approximately US$ 1000 to the
ures the most recent population estimate is of 1263 birds in local economy each year. Making and selling macaw-related
two subpopulations. Barbosa and Tella carried out extensive handicrafts as souvenirs for the tourists (Figures 7.11B, C)
research to determine the amounts of money that were supplements local salaries (each artisan is thought to derive
invested in the in situ conservation of the species (i.e. direct around 18 per cent of their monthly income from this work).
action to conserve the populations in the wild) by the These commercial benefits of eco-tourism could be further
Brazilian government and by a number of key NGOs and enhanced if a plan was developed to increase the number of
commercial sponsors. The activities that they considered visitors each year and to both lengthen their stay and
included the expenses associated with habitat protection encourage them to view the other endemic species of the
and species surveillance, education and outreach activities area. The birds also provide an important ecosystem service
to raise awareness with local people, the administrative because they, like other macaws, are efficient seed dispersers.
costs of coordinating multiple conservation efforts, and the In the case of Lear’s Macaw they are efficient dispersers of
costs of censusing the populations. Their synthesis of these the seeds of the licuri palm. This palm is their main food stuff,
data revealed to them that over the 25-year period between the main habitat of the other endemic species of the region,
1992 and 2017 around US$ 3,660,000 was invested. Most the main material used by artisans to create macaw-related
(51 per cent) of this money supported research work to bet- souvenirs, and has up to 537 uses for local people. By
ter understand the species’ conservation needs, 22 per cent supporting the regeneration of the palm, the macaw has an
was spent on direct protection of the endangered popula- important conservation, economic, and social impact.
tions, and 16 per cent was spent on social projects. The
remaining smaller amounts were spent on census work and Reference
administration. Barbosa, A.E.A. and Tella, J.L. (2019) How much does it cost
It is also important however that the continued survival to save a species from extinction? Costs and rewards of
(and perhaps to some degree rarity) of the macaw in the conserving the Lear’s Macaw. Royal Society Open Science
region does result in a flow of monies into the local economy. 6, 190.
shows there is a real cost to conservation and to species- and habitat-focused conservation efforts
be effective it is essential that scientists work with and the banning of DDT have had a positive impact
local communities and both governmental and here. The fact that some species of non-native intro-
non-governmental agencies. duced bird have experienced population shrinkage
might be seen as a positive too, because it could
reduce competition with native species. Overall
7.3.2 The task that faces us as ornithologists
however the picture is a very gloomy one and their
There are ornithological conservation success sto- estimates suggest that there has been a staggering
ries, and I have highlighted some of them in this cumulative loss of three billion birds during this
book, but there is still a lot of work to do. Kenneth period. Significant declines in the numbers of 303
Rosenberg and his colleagues have been able to (57 per cent) species were recorded, and some fam-
bring together data from a range of standardized ilies have suffered disproportionately; 90 per cent of
long-term surveys and from a network of 143 all of the birds lost come from just 12 families and
weather radars, capable of detecting nocturnally more than half of the loss involves the sparrows,
migrating birds, to examine changes in the abun- warblers, and blackbirds. All habitats have been
dance of 73 per cent (529 species) of the breeding affected but grassland birds have fared particularly
birds of the USA and Canada between 1970 and poorly and 74 per cent of grassland species have
2018. The positive news is that numbers of 100 spe- declined in numbers. Richard Inger and his col-
cies of breeding bird have increased, there are more leagues have reported a similar situation in Europe.
raptors, game birds, ducks, and other waterfowl Their data from 144 species over a 30-year period
that there have been in the past. Presumably (1980–2009) suggest a loss of more than 400 million
individual birds and, as is the case in North America, had become extremely rare but have benefited from
the farmland/grassland birds have suffered par- conservation efforts. These increases mask a signifi-
ticularly steep declines. Here too though there are cant decline in once common and widespread spe-
some species that have become more numerous and cies and it is estimated that some 44 million birds
the researchers have determined that these tend to have been lost from the UK. Once again it is farm-
be those species that already have small population land birds that have suffered a particularly dramatic
sizes, i.e. the birds most likely to have been the sub- decline (54 per cent) and so perhaps it is time for us
ject of direct conservation efforts. to review once more our agricultural and wider land
use practices. It is now almost 50 years since Rachel
Key references Carson brought to the attention of the world the
Carson, R. (1962) Silent Spring. Houghton Mifflin, threat of a ‘silent spring’. We may not have solved
Boston. the problem yet—but by working together we are
Rosenberg, K.V., Dokter, A.M., Blancher, P.J., et al. inching closer to doing so. That is why it is import-
(2019) Decline of North American Avifauna. Science
ant that those of us who have a love for birds, and
336(6461), 120–4.
for the wider environment, should continue to learn
Inger, R., Gregory, R., Duffy, J.P., et al. (2015)
Common European birds are declining rapidly while all that we can and to take all possible positive action
less abundant species’ numbers are rising. Ecology to ensure a bird-filled world for future generations.
Letters 18, 28–36.
State of Nature Partnership (2019) State of Nature
2019 https://nbn.org.uk/stateofnature2019/
Summary
The life history strategies of individual species
A similar situation exists in the UK where the State influence their population size, as do numerous
of Nature Partnership have recently published a environmental pressures both natural and anthropo-
sobering report suggesting that although the num- genic. Communities of birds are able to coexist
bers of birds of 171 species for which data exists because the species within them exhibit niche sep-
have increased over the longer term (the last 50 to 30 aration and competition avoidance. Many of the
years), these increases are driven by colonization world’s birds are threatened as a result primarily of
and range expansion of species from mainland human activity, but by working together species
Europe and by increases in numbers of birds that can be saved from the brink of extinction.
Index
adaptive radiation 10, 146, 148 Bustard (Otididae) community stability 145–6
accessory optic system 43 Houbara 98 competition 10–11, 115, 147–9, 153
air sacs 38–9 Little 99 competitive exclusion principle 148
alarm calls 133–5 Buzzard (Accipitridae) 36 Condor (Cathartidae),
Albatross (Diomedeidae) Californian 140–1
Gray-headed 49–50 calls Confuciusornis 6
Tasmanian Shy 48–9 alarm 133–6 confusion effect 139
Wandering 49 mobbing 136–7 Conservation 16–17, 43–4, 49–51, 113,
albatrosses calmodulin 13 116–7, 138, 150–4
and longlining 49–50 CaM 13 contact zone 14–5
conservation 49–50 camouflage 10, 131–2 contour feathers 22–26, 88, 113
foraging 121–2 eggs 81 convergence 7–8
flight 33–4 cannibalism 22 cooperative breeding 116–7
migration 48–50 carrying capacity 116–117 cooperative feeding 124–5
reproduction 77 central place foraging theory 127 copraphagy 87
albumen 74–7 Chaffinch (Fringillidae) 106 copulation 75, 95–6, 100, 113
alien species 16, 142–3 chalaza 76 retaliatory 95–6, 100
altricial development 86, 91–93, 113 character conservation 7 coracoids 34, 37
ansiodactyl feet 7–8 Charidriiformes 10, 147 in archaeopteryx 4
anisogamy 96–7 Chickadee (Paridae), Black-capped corticosterone 58–9
Anseriformes 7 66, 134, 136 courtship 21, 26, 37, 42, 99–110
anting 28 chicks 78, 83–4, 87, 91–92 133, 138 Cowbird (Icteridae)
Apodidae see Swifts begging 113–15 Brown-headed 83
Archaeopteryx 1–7, 45–6 tonic immobility 133 Shiny 84
Auk (Alcidae), Great 150 Chiffchaff (Sylviidae) 31, 111 crèches 138
chorioallantois 76 cross-fostering 53
Babbler (Timaliidae), Pied 135 classification 5 Crow (Corvidae)
BDNF 106 cloaca 74–75 Carrion 14
beaks see bills clock shift 68 Hooded 14
begging 113–14 clutch size 77–80, 99, 103 Northwestern 125–6
bills Cockatiel (Psittacidae) 41–2 crows
Darwin’s finches 12–14 collision avoidance 42–3 hybrid zone 14
diversity 10 colonial breeding 22, 70–72, 82, 86, optimal foraging 125–6
morphology 10 110, 136–8 Cuckoo (Cuclidae)
Blackbird (Turdidae) 52 see also flocks Common 82
Red-winged 102–4 colour Diederik 82
Blackcap (Sylviidae) 13, 31, 53–7, 69 of eggshells 81–2, 84 Curlew (Scolopiacidae)
BMP4 13 of feathers 26–7, 132 Eurasian 10
bone morphometric protein 13 communities 144–9
Booby (Sulidae), Masked 77 dynamics of 143 Darwin’s finches 10–14, 147
bout length, song 109 ecological network 140, 145 dawn chorus 110
broken wing display 133 extinction 145, 150–2 delayed maturation 140
brood parasites 82–84 immigration 145 diapsid reptiles 1–2
brood patch 88 patch size 146–7 Diclofenac 90
brood reduction 114–5 species richness 145–6 differential allocation 115
155
156 INDEX
dinosaurs 4, 6 equilibrium theory 145 Galapagos see Darwin’s finches

theropods 17 evolution Cactus 14
thecodonts 2 adaptive radiation 10–13 Large Cactus 14
Dipper (Cinclidae), Brown 147–8 from dinosaurs 5–10 Large Ground 14
directional selection 11–13 natural selection 11–13 Medium Ground 12–4
disease 130, 141–3 of flight and flightlessness 45–47 flight
dishonest signal 82, 136 of migration 51–6 adaptations for 34
displays evolutionary tree see phylogenies aerodynamics 29, 34, 36, 41
broken-wing 133 extinction 6, 16, 145, 150–4 respiration 38–40
courtship 98, 101 extra-pair copulation (EPC) 95–6, wing morphology 23, 30, 33–35
disruptive selection 11–12 100, 105 energetics 38–40
DNA 8–9, 11 evolution of 45–47
Dodo (Raphidae) 150 faecal pellets 87 flapping 33–8, 41, 45–6
Dove (Columbidae) Falcon (Falconidae) gliding and soaring 33–36,
Barbary 41 Eleonora’s 51 40–1, 45
Collared 145 Peregrine 89, 138–9 speeds 33, 35–7, 41–2
down, feathers 21–6, 113 fat reserves flightlessness
Drongo (Dicruridae) for migration 57–62 evolution of 45–7
Fork-tailed 134–6 fault bars 28–9 flocks 29, 40, 57, 123–4, 126, 130, 134,
Duck (Anatidae) feather tracts 24–5 136, 139, 143–4, 147
American Black 16 feather Flycatcher (Tyrannidae)
Black-headed 82 of Archaeopteryx 1 Collared 109, 118
Eider 138 colour 26 Pied 58, 84, 109
European Mallard 16 contour 22–26, 88, 113 food storage 66
Ruddy 16–17 damage 26–7 foraging 49–51, 63, 66, 120–131
White-headed 16–17 down 21–6, 113 and risk 130–1
ducks, hybridisation 16–17 filoplume 22 and spatial memory 66
Dunnock (Prunellidae) 101 follicle 25 cooperation 123–4, 125
dunnocks, mating system 104–5 growth 26, 28 flocks 123–5, 127
maintenance 27–8 optimal 125–6
ecological isolation 11 pennaceous 6, 22, 45 see also feeding
ecological network 145 plumulaceous 6, 22 Forktail (Turdidae)
ecological release 148 primary 23, 26, 29 Little 147–8
ecological role 150 secondary 23, 29 Spotted 147–8
egg dumping 82 semiplume 22 formation flying 40–1
egg recognition 82–4 structure 24 funnel cage 52,68–9
egg white see albumen wear see feather damage furcula 1, 2, 4, 34, 37
egg yolk see yolks see also moult Archaeopteryx 4
eggs 75–77 feeding
and agricultural chemicals 89–90 differential allocation 115 Galapagos Islands 10, 12
camouflage 81 niche 10, 147–8 genetic swamping 14, 16
clutch size 77–80 territory 126–7 gliding see flight
formation 73–7 see also foraging Godwit (Scolopacidae)
hatching 91 feet Bar-tailed 62
incubation 85–88 toe arrangement 5, 7–8 Goose (Anatidae)
internal structure 75–7 claw curvature 5 Brent 124
mimicry 82 female preference 98–9 Pink Footed 40
recognition 82 Finch (Estrildidae) Grassquit (Thraupodae)
quality 84–5 Bengalese 118 Dull-coloured 11
eggshells Zebra 35–6, 77, 94–6, 106–7, Grebe (Podicipedidae)
colouration and pattern 81–5 110, 118 Atitlan 150
effects of pesticides 89–90 Finch (Fringilliade) ground nesting 81, 85, 132–3
quality 84–5 Chaffinch 130 Grouse (Phasianidae)
Eider (Anatidae) Goldfinch 88, 129–30 Greater Sage 99
Common 138 Greenfinch 25, 130 Guillemot (Alcidae) 85
Steller’s 29 House 87, 130, 142–3, 151 egg recognition 82
embryo 76–77, 91 Finch (Thraupidae) Gull (Laridae)
INDEX 157
Black-headed 123 foraging 121 see also evolution

Glaucous 31 kleptoparasitism 135 directional selection 11–13
Herring 53, 114 disruptive selection 11–12
Ivory 31 last male precedence 95 stabilizing selection 11–12
Laughing 114 learning to sing 106–7 navigation 65–72
Lesser Black-backed 53 leks 98–9 visual landmarks 65
gulls life history strategy 51 celestial cues 68–9
begging 114 light pollution 64–5 magnetic-field 69–70
cannibalism 22 lungs 38–9 sun compass 68–9
migration 53 scent-based 70–2
moult strategies 31 Macaw, Lears 152–3 vector-based 67–8
magnetic field 69–70 Neornithes 4
hallux 4, 5 magneto-receptor 70 neonicotinoids 60–61
harems 101–2 Magpie (Corvidae), Black-billed 41, nests 85–7
Hatching, eggs 91–2 78, 114–5 niche 10, 147–9
Hawk (Accipitridae) Mallard (Anatidae), European 16 divergence 147–8
Harris 123–5 Manakin (Pipridae), Blue- shifts 148–9
helpers 116–17 crowned 98 bill diversity 10
herbivores 125 Manx Shearwater (Procellariidae), Nightingale (Turdidae) 110–11
Hesperornithiformes 6 flight 35 noise pollution 111–3
high vocal centre (HVC) 106–7 mate choice see courtship nuptial gift 100–1
hippocampus 65–6 mate sharing 101 Nuthatch (Sittidae), Red-breasted 134
hormones 58–9, 88, 106 mating systems 97
hot-shots 98 megapodes optimal clutch size 78–9
hot-spots 98 incubation 86 optimal foraging 125–6
Hummingbird (Trochillidae) superprecocial chicks 91 organochlorines 89–90
Anna’s 42 melanins 26–7, 33–4 Ornithomimus 1
Ruby-throated 37, 59 melatonin 58 Osprey (Pandionidae) 8, 123, 150
hummingbirds meloxicam 90 Ostrich (Struthionidae) 25
fat reserves 59 Merlin (Falconidae) 90 ovaries 74–5
feathers 26 Microraptor gui 6, 45–6 oviduct 74–5
flight 36–7, 42 migration 48–65 ovum 74–5, 94
physiology 40–1, 59 and fat reserves 58–61 Owl (Strigidae)
song 105 and stable isotopes 55–6 Great Horned 134
hybrid zone 14–5 and weather 63 Northern Pygmy 134
hybridization 14–6 control of 51–4, 58–60 Pygmy 130, 144, 149
hyperphagia 57, 62, 70 disruption 60–1, 64 Tawny 99
ecology of 51–2 Oystercatcher (Haematopodidae),
Icthyornithiformes 6 evolution of 51–7 Eurasian 10, 81, 88, 125
immunocompetence 84, 109, 112, 143 genetics 52–7
imprinting 118 navigation 68–72 parasites 87, 130
incubation 86–8, 91 stopover sites 62 Parrot (Psiticidae), Swift 50
information transfer hypothesis migratory orientation 68 partial migrant 53
122–3 migratory restlessness 52–3, 58, 68–9 passerines 7, 79–80
infundibulum 74–5 mimicry, egg 82 feather tracts 25
invasive species see alien species mobbing 136–7 pathogens 87, 130
monogamy 97, 103–5 Peafowl (Phasianidae), Indian
Jackdaw (Corvidae) 28 moult 28–32 21, 99
Jay (Corvidae), Blue 8, 23 fault-bars 28–9 pectoralis 34, 37, 41
Junco (Emberizidae), Dark-eyed 54, in gulls 31 Pelican (Pelecanidae), Great
109, 131 minimizing impact of 29–30 White 40–1
strategies 30–2 pelicans, formation flying 40–1
K/T boundary 6 movement, categories of 48 penguins (Speniscidae) 25, 47
keratin 28 Murre, thick-billed 127 incubation 87
kin selection 98–9 perceptual sharpening 114
Kittiwake (Laridae) 92 nXIIts 105 pesticides 60–61, 89–90
Kiwi (Apterygidae), Brown 75 natural selection 10–13, 30, 54, 83 photoperiod 58
158 INDEX
phylogeny 7–10, 17–20 resource provision 99–101 European 29, 37–8, 67–8, 108, 141
biomolecular 8–10 retricies, see feathers, tail Spotless 115
consensus 9 Robin (Turdidae) sternum 1, 4, 34, 37, 42
morphological 8–9 American 120 stitching 121
Pigeon (Columbidae), Passenger European 29, 70, 134–5 Strigidae 8
7, 150 sun compass 69
pigeons, navigation 65, 69–70 Sanderling (Scolopacidae) 10, 126–7 Sunbird (Nectariniidae)
piloting 65 Sandpiper (Scolopacidae) Double-collared 127
pipping, see hatching Semipalmated 65 Golden-winged 127
place cells see hippocampal cells Spotted 77, 103 Malachite 127
placode see feather follicle sensitive period 106–7 Palastine 86
plastic pollution 121–2 sensorimotor phase 106–7 superprecocial development 91
Plover (Charadriidae) sensory bias 101 supracoracoideus 34, 37
Little Ringed 10, sensory acquisition phase 106–7 Swift (Apopidae) 8, 33, 57
Ringed 131 sentinels 134–5 synapsid reptiles 2
plovers, broken wing display 132–3 sex chromosomes 73–5 Sinosauropteryx prima 6
plumage sex-linked genes 75, 82 syrinx 105–6
camouflage 30, 131–2 sexual conflict 104–5
cryptic 29 sexual selection 97, 101 tail feathers 22, 26, 28–9
eclipse 30 sexy sons hypothesis 98 tectofugal pathway 43
nuptial 30 shell dropping behaviour 125–6 Tern (Laridae), Arctic 92
polyandry 97, 104–5 shells, see eggshells Territory
polygamy 102–4 Shrike (Laniidae) and song 108–9, 111
polygynandry 97, 104–5 Great Grey 100 breeding 78–9, 99–104, 116–7
polygyny 97, 102–5, 117 Lesser Grey 101 feeding 126–7
polygyny threshold model Red-backed 69 testes 75
(PTM) 103–4, 117 silent phase 106–7 testosterone
population change 142–4 Silvereye (Zosteropidae) 69–70 and bird song 107
populations 11–13, 16, 142–144 singing rate 109–10 and incubation 88
see also communities Sinosauropteryx 1 and migration 58
porphyrins 26, Snipe (Charadriidae), Great 98 thalamofugal pathway 43
precocial 77, 82, 91–92, 103, 113 social monogamy 97 thecodonts 2
predation 77–80, 82–3, 92–3, 130–8 song 74, 105–113 theropod dinosaurs 17, 45
predator avoidance 131–8 and noise pollution 112–3 Tit (Paridae)
preen gland 7, 28 bout length 109 Blue 66, 77, 84–5, 98, 129, 144
prolactin, and incubation 88 courtship 106–7 Coal 130, 144, 149
Ptarmigan (Phasianidae) 30 functions of 107–13 Crested 130, 149
pterylae, see feather tracts learning 106–7 Great 30, 84, 91, 144
pyrazine 121–2 sonograms 135 Marsh 66, 129
Sparrow (Passerellidae) Willow 144, 149
Quelea (Ploceidae), Red-billed 140 Savannah 107 toe arrangement 4, 7–8
White-crowned 60–1 tonic immobility 133
rachis 22 Sparrow (Passeridae) trachoesyringeal motor nucleus 105
Razorbill (Alcidae) 85 House 5, 87, 106, 112–3, 142–3 trkB 106
Redpoll (Fringillidae) 22 Sparrowhawk (Accipitridae) 47, 132, turacous (Musophagidae), feather
Redshank (Scolopacidae) 10, 137–9 138–9 colour 26
Redstart (Muscicapidae) spatial memory 65–66
Black 115 speciation 10–13 uropygial gland, see preen gland
Common 27, 115 species uterus 74–5, 95
Plumbeous Water 147–8 biological concept 11
White-capped Water 147–8 richness 145 vagina 74–5, 95
Redstart (Parulidae) sperm 7, 73, 75, 94–6, 103 vector navigation 68
American 98 storage tubules 95 vigilance behaviour 134–5, 137
refuelling, during migration 52, sperm competition 95–6 Vireo (Vireonidae), yellow-green 57–8
57–62 stabilising selection 11–2 Vulture (Cathartidae)
resource availability 79 stable isotopes 55–6 Griffon 44
resource defence 105, 126 Starling (Sturnidae) White-backed 90
INDEX 159
Vultures Red-faced 79 egg recognition 84

collisions 44 Yellow 86 nest 86
pollution 90 Yellow-rumped 149 Widowbird (Ploceidae)
vision 44 Warbler (Sylviidae) Long-tailed 101–2
Aquatic 75 Red-shouldered 101–2
W sex chromosome 73, 82 Chiffchaff 31 wing 33–36
wading birds, foraging Garden 31 wishbone, see furcula
10, 121 Greenish 31
Warbler (Parulidae) Reed 106 yolk 75–7
Bachman’s 151 Sedge 51 yolk sac 76
Black-throated Green 149 Seychelles 116–17, 150
Blue-winged 14–15 Willow 31, 55–6, 106 Z sex chromosome 73
Brewsters 15 Whitethroat 26–7, 106 zoonotic disease 142
Golden-winged 14–15 weather, and migration 63 zugunrhue, see migratory
Lawrences 15 Weaver (Ploceidae), Village 82 restlessness
Prothonatory 83 weavers zygodactyl feet 7

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OUP CORRECTED PROOF – FINAL, 27/08/20, SPi

2 Feathers and flight 21

3 Movement: migration and navigation 48

4 Eggs, nests, and chicks 73

6 Foraging and avoiding predators 120

7 Populations, communities, and conservation 140

‘Creation is never over. It had a beginning but it has no ending.’

roots of birds we need to look back to the now extinct

145 130 120 100

Avialae/Aves (Birds) Keeled

Theropoda/Coelurosauria Vaned feathers

announced from the same region—that of an almost

Figure 1.2 Archaeopteryx

Grey-faced Woodpecker (Picis canus)

in a range of unrelated species and orders including

Box 1.1 Continued

Seed abundance (g/m2)

So can we see evolution by natural selection actually hap- 200

In effect what has happened here is a burst of intense direc-

Box 1.2 Hybridization and duck conservation

Gruidae Cranes Accipitriformes

Furnariidae Ovenbirds Paridae Tits and chickadees

Rhodinocichlidae Thrush-tanager Phaenicophilidae Hispaniolan tanagers

Feathers and flight

‘Birds are pilot and aircraft in one.’

‘No bird soars too high if he soars on his own wings.’

Primaries and Secondaries Auriculars

Posterior vane Longitudinal

Spinal tract, cervical region Submalar tract

the exception of the typically bare legs, and the

2.4 Feather damage

when the ultraviolet component of sunlight alters

Box 2.1 Taking advantage of feather wear

Figure 2.9 An example of wing moult in the European Starling

Box 2.2 Minimizing the impact of moult

Standardized body mass (g)

again; and montane/high latitude birds such as the

Box 2.3 Moult strategies of the old world warblers

Box 2.3 Continued

140 Post-juvenile moult extent (proportion) 0.8

0–2500 2500–5000 >5000 0–2500 2500–5000 >5000

2.7 Flight wings. They make these manoeuvres by altering

(A) Dynamic soaring wing (C) High aspect ratio wing

(B) Elliptical wing (D) High lift ratio wing

both lift and thrust are generated and there is a net

(E) Outer wings

(A) (B) (C) (D)

Figure 2.16 Skeletal movements of the European

surface area for oxygen transport. In mammalian

(B) Inhalation 5 Exhalation

Box 2.5 Formation flying saves energy

at the front of the V have a wing-beat frequency similar

sumably they were maximizing the energy savings that

170 Figure 2.19 Variation in heart beat rate (a measure of

Box 2.6 Collision avoidance

Through experiments with pigeons, the neurons that pro- Hummingbirds

Box 2.6 Continued

Movement: migration and navigation