VERTEBRATE MATING SYSTEMS, ALLEE EFFECTS AND

CONSERVATION

PHILIP A. STEPHENS and WILLIAM J. SUTHERLAND

School of Biological Sciences, University of East Anglia
Norwich, NR4 7TJ, UK

ABSTRACT

Recent interest has focused increasingly on the role of behavioural research in

conservation. Within this field, the study of mating systems can make a highly
important contribution. Mating systems both affect, and are affected by, interactions
between conspecifics. Of particular importance are Allee effects, which arise as a
result of the benefits of conspecific presence. Recognition of the consequences of
Allee effects for mating systems, conservation, and behaviour, has also increased
recently. The inter-relationship between these areas is highly complex, and both
mating systems and Allee effects have consequences for each other, as well as for
conservation. In this way, both have direct and indirect consequences for
conservation. We discuss these in the light of current, and potential, contributions
of the study of mating systems to conservation.

Introduction

In recent years, increasing emphasis has been placed on the potential

contributions of behavioural science to conservation1-4. A key area is the study of
mating systems. Different mating systems may explain differential susceptibilities of
species to certain conservation risks, and a thorough understanding of mating systems
is essential for many aspects of conservation intervention and management. Recently,
attention has also focused on the role of Allee effects in both behaviour and
conservation5-7. Allee effects, named after the pioneering work of W.C. Allee8-10,
arise as a result of the benefits of conspecific presence, and manifest as reductions in
individual fitness as populations become smaller and these benefits are lost11. The
types of Allee effect to which a species is susceptible may both affect, and be affected
by, the species' mating system. The inter-relationship between mating systems, Allee
effects and conservation is illustrated in Figure 1.
In this chapter, we discuss the relationships between mating systems and Allee
effects, and we explore the consequences of these relationships for conservation. We
discuss each of the four links shown in Figure 1, although inevitably, there is some
overlap between these. We begin with an assessment of how Allee effects can affect
mating systems (and thus can have indirect consequences for conservation), and how
mating systems may affect a species' vulnerability to Allee effects (also with indirect
consequences for conservation). We go on to look at the more direct consequences of
both Allee effects and mating systems for conservation.

In: Apollonio, M., Festa-Bianchet, M. and Mainardi, D. Vertebrate Mating Systems. London, World Scientific
Publishing. (2000): Chapter 9.

1
 Mating
systems

Conservation

Allee
effects

Fig. 1. The inter-relationship between mating systems, Allee effects and conservation. Both mating
systems and Allee effects have a direct bearing on many conservation issues. However, Allee effects
are important factors underlying the mating system of a species, whilst mating systems can also affect
the types of Allee effects to which a species is vulnerable. In this way, both mating systems and Allee
effects can also have indirect implications for conservation.

1. Allee effects and their consequences for mating systems

At their most basic, Allee effects arise because self-incompatible species

require conspecifics with which to mate. As population densities or sizes decrease,
availability of potential mates is reduced. This type of mate limitation is perhaps the
most widely cited mechanism of the Allee effect but many others are also recognised.
Examples of these have been divided into seven categories, presented in Table 1. For
completeness, the table lists examples from a range of taxa, both plant and animal.
Recent evidence suggests that the factors underlying mating systems are
considerably more complex than was thought previously12. We believe that Allee
effects form an important factor in this complex relationship (Fig. 2). Allee effects
are important determinants of the spatial distribution of a species (Fig. 3), and hence
are significant factors underlying the type of mating system that a species adopts. For
example, African wild dogs (Lycaon pictus) are among the smallest members of the
large carnivore guild of sub-Saharan Africa. The resultant susceptibility of this
species to intraguild kleptoparasitism leads to an Allee effect at small group sizes
which is an important determinant of group living in this species. This Allee effect
can therefore be said to underlie the 'obligate communal breeding'13 seen in the
African wild dog. Similar arguments can be made for many other species of obligate
cooperators.
As a second example, the relatively low metabolic rate of large antelope might
account for the lack of selectivity in their diet, which in turn allows them to survive
on the open grasslands14. However, it is likely that within this extensive habitat, it is
Allee effects, due to antipredatory behaviours, that promote herding behaviour among
many of these species. Those same Allee effects may therefore be responsible for the
ease with which single males can monopolise large groups of females, leading to the
polygynous, harem systems, typical of such species.

2
 Table 1. Summary of mechanisms which may give rise to a component Allee effect
Mechanism
1. Predator/parasite avoidance
1.1 vigilance and survival
1.2 vigilance and foraging rate
1.3 anti-predator aggression
1.4 activity budgets
1.5 dilution of predators or parasites
1.6 developmental synchrony and predator satiation
Examples References
Predators detected at greater distance (and hence earlier) by larger flocks of woodpigeon (Columba palumbis); 15
mortality thus reduced.
Larger groups of long-tailed macaques (Macaca fascicularis) detect predators earlier than smaller groups. 16
Individuals in larger flocks of starlings (Sturnus vulgaris) spend less time in vigilance and consequently more time 17
foraging, than individuals in smaller flocks.
Less time spent vigilant and more time spent foraging in larger groups of pronghorn (Antilocapra americana). 18
Groups of 11-20 grey herons (Ardea cinerea) consume more fish per capita than smaller groups, due to the increase 19
in collective vigilance in the larger groups.
Risk of nest predation increases linearly with distance from active lapwing (Vanellus vanellus) nest; lapwing 20-23
colonies thus have a protected zone around them of a size related to the number of lapwing present.
Colonial male bluegill sunfish (Lepomis macrochirus) spend less time pursuing predators than solitary males, and 24
hence have more time to aerate the nest, leading to reduced incidence of fungal disease.
Individual "domains of danger" are reduced by aggregation. 25
Groups of the marine insect, Halobates robustus, form flotillas; individuals in larger flotillas suffer lower predation 26
due to dilution and confusion of predators (primarily clupeid fish).
Groups of the stream-dwelling trichopteran Rhyacophila vao suffer higher encounter rates with the planarian 27
predator Polycelis coronata than do individuals but this is more than compensated for by predator dilution effects.
Large groups are associated with decreased individual loads of mobile parasites across many taxa. 28,29
Synchronous breeding is an important mechanism by which colonial guillemots (Uria aalge) increase reproductive 30,31
success, principally as a result of predator swamping.
Synchronous mast-seeding in cycads (Encephalartos spp.) reduces pre-dispersal seed predation. 32
(Continued
overleaf)
Mechanism
2. Overcoming hosts or prey
2.1 parasitism
2.2 predation
3. Resource defence or acquisition
3.1 intraspecific territorial defence
3.2 interspecific competition
3.3 interspecific kleptoparasitism
4. Amelioration of environment
4.1 thermoregulation
4.2 soil characteristics
Examples References
High densities of bark beetles (Dendroctonus ponderosae) are required to overwhelm the defences of pines (Pinus 33
contorta) and cause host mortality (on which the beetles depend).
Individuals in larger clusters of larvae of the bordered patch butterfly (Chlosyne lacinia) have higher survival and 34
more rapid development, partly due to greater potential to initiate feeding on tough host sunflower (Helianthus
annuus) leaves.
Many carnivore species are better able to capture large prey by cooperative hunting; group living may thus be 35
favoured in areas with abundant large prey.
Large groups of red colobus (Colobus badius) may be necessary to defend territories encompassing enough 36
temporally-asynchronous resources to ensure a mixed diet year-round.
Larger packs of African wild dog (Lycaon pictus) won inter-pack clashes on ten of ten occasions. 37
Larger groups of blue tang surgeonfish (Acanthurus coeruleus) are able to overcome territorial defence of dusky 38,39
damselfish (Stegastes dorsopunicans) and thus feed in areas of higher algal turf biomass.
Larger packs of African wild dog are better able to defend kills from intraguild kleptoparasitism by spotted 40,41
hyaenas (Crocuta crocuta).
Alpine marmots (Marmota marmota), which experience high over-winter mortality due to harsh environmental 42
conditions, reduce over-winter energy consumption by social thermoregulation within groups in shared
hibernacula.
Mass incubation by the Brazilian stingless bee (Scaptotrigona postica) allows maintenance of high temperatures in 43
the brood chamber, even when ambient temperatures are low.
At low densities, hemlock (Tsuga heterophylla) is less able to acidify soil and sequester water in the upper soil 44
horizons, and production increases with density. (Continued
overleaf)
Mechanism Examples References

5. Reproduction
5.1 mate finding The frequency of reproductive encounters between male and female flour beetles (Tribolium confusum) increases 8
with increasing density.
The fraction of mated females of the Glanville fritillary butterfly (Melitaea cinxia) decreases with decreasing local 45
density.
5.2 pollination Many plant species, particularly those that are self-incompatible, show reduced viability at low densities or in 46-53
fragmented populations, due to reductions in incidence of aerial pollination, or reductions in pollinator activity.
5.3 fertilisation Both lower density and lower numbers of sea urchins (Strongylocentrus franciscanus) lead to lower rates of 54
fertilisation.
5.4 conspecific enhancement of mating Captive females of the black lemur (E. macaco) and mongoose lemur (E. mongoz) housed with additional 55
conspecifics have higher reproductive rates than those maintained as part of an isolated pair.
It is likely that females of several Callitrichid species would be energetically unable to forage efficiently, lactate 56
and carry young, and thus would be unable to reproduce without the presence of helpers who participate in
transport of young.
5.5 mate choice Female moorhens (Gallinula chloropus) of equal competitive ability secure better mates when sampling males in 57
larger flocks than when fewer males are available for sampling.
6. Demographic stochasticity
6.1. Skewed sex ratios Sex ratios in small populations of the grassland campion Silene otites vary greatly as a result of demographic 58
stochasticity and may be crucial for population survival.

7. Genetics
7.1 inbreeding Seed production and viability are reduced by decreased genetic variation in small populations of the flowering 59
plant Gentianella germanica.
7.2 genetic drift Small, scattered populations of the European brown bear (Ursus arctos) are monomorphic and fixed for different 60
mitochondrial haplotypes in different parts of western Europe, owing to several centuries of geographic isolation.
7.3 hybridization Small populations of many species are vulnerable to 'genetic extinction' by hybridisation with more abundant 61
species.
 Mate
choice

Mating
systems

Parental
care

Allee Spatial
effects distribution

Environment

Fig. 2. Mating systems and Allee effects. Both Allee effects and environmental factors may affect the spatial
distribution of a species. Allee effects may also affect the requirement for parental care, as may the spatial
distribution of the species. Spatial distribution, parental care and mate choice are all factors influencing the
mating system adopted by a species. Mating systems can, in turn, influence the nature of the Allee effects to
which a species is subject.

Finally, in pukeko (Porphyrio porphyrio), territorial defence has been postulated as

a major factor promoting polyandry62. Males that do not ally with extra male defenders
risk losing their territory to those that do, and consequently risk losing the opportunity to
breed. Thus Allee effects arising from inadequate territorial defence by individuals appear
to promote polyandry in this species.
From the above examples, it is clear that Allee effects can have major implications
for the type of mating system adopted by a species. Understanding the relationship
between Allee effects and mating systems is therefore an important element in
understanding both the social and breeding behaviour of the species. In particular, this is
important for understanding how social dysfunction can result from rarity and impair a
species' chances of recovery. It can also be relevant to successful captive breeding. In
helping to shape the mating system of a species, Allee effects may also have indirect
implications for conservation, as outlined in section 4.
 Average individual fitness

F0
A0

Degree of aggregation

Component Allee effect (1)

Component Allee effect (2)
Cumulative fitness
Negative density dependence

Fig. 3. Several component Allee effects may act on a species simultaneously. The relationship between these
and any negative density dependent factors will be important in determining the degree of aggregation and
thus the spatial distribution. Component Allee effects 1 and 2 may represent, for example, ease of mate
finding and benefits of "safety in numbers". These have the effect of increasing fitness from its basic level in
the absence of conspecifics (F0), up to some point where increased aggregation brings no further benefit
through these mechanisms. Negative density dependence by contrast, may result from increased competition
for food or mates, or increased depletion of resources. This will tend to decrease fitness from F0 as degree of
aggregation increases. The cumulative fitness represents the relationship between all the density dependent
factors, and dictates an optimal degree of aggregation A0.

2. Mating systems and their consequences for Allee effects

In section 1, we discussed how Allee effects can affect the spatial distribution and,
hence, the mating system of a species. However, many other factors, including
environment, mate choice and parental care systems also dictate the mating system of a
species. These can, in turn, influence the nature of associations between individuals and
groups, and can thus affect the type of Allee effects to which a species is susceptible. For
example, more solitary, monogamous species might be more vulnerable to certain Allee
effects than are aggregative or polygamous species. In particular, these might include mate
finding Allee effects when at low densities63, and problems due to skewed sex ratios when
population sizes become small. Polygamous breeding systems might also be more
susceptible to certain Allee effects. Most notably, these include some of the genetic
problems associated with small population sizes.

7
 As observed in section 1, mate limitation is an important mechanism of the Allee
effect. In small populations, or populations at low density, this may arise simply as a result
of infrequent encounters with potential mates, as has been demonstrated for some insect
species (see Table 1, 5.1-5.3). Similarly, unequal sex ratios which arise stochastically in
small populations, may also lead to mate limitation11. As an example, chance differences
in the numbers of males and females in a small population of reintroduced sea eagles
(Haliaeetus albicilla), in Scotland, led to a significant number of individuals failing to form
pairs64. A further, less obvious form of mate limitation results in species in which sexual
selection plays an important role in the mating system. Females have been shown to have
higher reproductive success when breeding with males of perceived high quality, even
where differential male quality is based entirely on nonfunctional ornaments65. The
differential-allocation hypothesis suggests that females may allocate more reproductive
effort to offspring sired by higher quality mates65,66. It follows from this, that if mate
choice is restricted in small or low density populations, then low parental investment and
low reproductive output may result. Such a phenomenon would certainly correlate with
low repoductive rates and success in many species of zoo animals, where forced matings
with apparently suitable mates are conducted without regard for mate choice67. Leks
provide a forum for mate choice in a variety of species68. It would be interesting to know
whether species which rely on such communal displays are particularly susceptible to small
population extinctions. Finally, mate limitation may also arise where individuals are highly
related, and animals avoid breeding in preference to breeding with a close relative. This
has been shown for acorn woodpeckers (Melanerpes formicivorus)69 (see further below)
and is also thought to be a feature of the meerkat (Suricata suricatta) mating system70.
For polygamous species, genetic issues may be of particular concern. Genetic
mechanisms are perhaps the most widely discussed mechanisms of the Allee effect
(although rarely by that name), but their importance to declines in survival and fecundity is
still widely debated71,72. Three genetic mechanisms of the Allee effect are given in Table
1: inbreeding, genetic drift, and hybridization. Hybridization is discussed in greater detail
in section 4; in the current section we will concentrate more fully on inbreeding and drift.
Both inbreeding and genetic drift lead to a reduction in heterozygosity and allelic
diversity. Of considerable concern is inbreeding depression, the increased expression of
deleterious, recessive alleles that can result from reduced heterozygosity. The negative
effects of inbreeding depression have rarely been documented in natural populations of
vertebrates, but potentially costly behavioural mechanisms aimed at avoiding inbreeding in
natural populations, suggest that its consequences may be severe69. Given that genetic
mechanisms are dependent on effective population size, Ne, it may be expected that
polygamous mating systems will increase rates of inbreeding and loss of genetic variation,
and experimental data support this prediction73. Frankham72 calculated that genetic
management could potentially increase the ratio of Ne/N almost 20-fold, and discussed
several methods by which this could be achieved. These included: equalising family size;
reducing reproductive skew by decreasing polygamous mating strategies; minimising
population fluctuations; and minimising kinship between breeding individuals. All of these
strategies are clearly far more easily implemented in captivity than in the wild, whilst such
intensive manipulation of natural breeding strategies and, potentially, disproportionate
selection for less fit phenotypes, remain contentious. In particular, as discussed above,

8
interfering with free mate choice might well be detrimental to the health of captive
populations67.
Different species react in different ways to inbreeding. It has been observed that
many species have relatively high inbreeding coefficients, and yet remain unaffected74.
These differences may reflect differences in the natural abundance of the species, but will
also be dependent on their mating systems. For many vertebrates, dispersal is an important
behaviour relating to the mating system, and obviously functions to reduce inbreeding.
However, in fragmented habitats, dispersal is frequently highly risky, or indeed,
impossible. Understanding the natural behaviour of a given species may therefore have
important consequences for issues such as reserve design, corridor use, or translocation.
There is some support for the idea that repeated inbreeding of healthy individuals
can 'purge' a population of deleterious alleles and thus prevent inbreeding depression75,
although evidence for this process is limited and the method is not without considerable
risks72,75. Knowledge of the species' natural mating system may be important in
determining the merits of this process. More commonly, efforts are directed towards
maximising heterozygosity within populations of rare species. Encouraging gene flow
between subpopulations, or introducing individuals from elsewhere can improve
reproductive fitness; however, risks associated with disease transmission, dilution of
locally co-adapted genes and other costs of translocation, mean that this must be judged on
a case by case basis, and only with a sound knowledge of the mating system of the species
involved.
To summarise, mating systems can impact on the type of Allee effects to which a
species is susceptible. As a result of this, mating systems and other associated behaviours
can also affect the vulnerability of a given species to certain types of conservation risk. An
understanding of mating systems is thus an important component in assessing and treating
the causes of population declines.

3. Allee effects and their direct consequences for conservation

The major consequences of Allee effects for conservation have been reviewed
recently7. Allee effects often result in aggregative behaviour or group living, which can
render species more susceptible to certain types of conservation threat. Examples include
disease outbreaks, which models indicate can more readily establish in aggregated host
populations76, and harvesting, which may be more efficient and damaging, when the target
species is highly aggregated. Beyond these specific examples however, the principal
implications of any type of Allee effect can be inferred from incorporating Allee effects
into simple models of population dynamics (Box 1 and Fig. 4). The most important
conclusion of this simple modelling approach is that at reduced numbers or densities, Allee
effects reduce the viability of groups, populations, or species. Furthermore, where Allee
effects are strong, lower threshold group or population sizes result, below which growth is
negative, and extinction is highly likely.

9
Box 1. Allee effects and models of population dynamics

Allee effects can be described, for example, by either a negative exponential or a

rectangular hyperbola function77. Due to its mathematical tractability, the rectangular
hyperbola function is most easily incorporated into models. This function takes the form:
n
p = (1)
( + n)

where p is the fitness due to the component Allee effect, n is the population size and is
the population size at which p = 0.5. The value of allows the strength of the Allee effect
to be scaled (Fig. 4a).
The specific growth rate of populations limited by the carrying capacity of their
habitat is often given by the logistic equation:

dn rn
= r (2)
ndt k

where t is time, r is the intrinsic growth rate of the species, and k is the carrying capacity.
When n < k, the specific growth rate is positive and n increases. When n > k, growth is
negative and n decreases. Thus the population always tends towards k (Fig. 4b).
Given that equation (1) gives relative fitness under an Allee effect, the reduction
below optimal fitness which results from that effect can be derived as:

1 p = (3)
( + n)

An Allee effect can thus be incorporated into the logistic equation by subtracting a
term proportional to equation (3) from equation (2). Whilst will scale the Allee effect, a
term of proportionality, , will allow the severity of the Allee effect to be modelled.
Logistic growth subject to an Allee effect will thus be given by:

dn rn
= r (4)
ndt k ( + n)

The result of this additional term is that the specific growth rate is depressed at any
given population size, and that this reduction is most marked at low values of n (Fig. 4c).
The population will have two equilibria - a lower, unstable equilibrium and an upper, stable
equilibrium. The lower equilibrium is critical; below this, growth is negative and the
extinction of the group or population becomes highly likely.

10
 (a)
1.0

0.8
Fitness

0.6

0.4

0.2

0
0 40 80 120 160 200

(b) 0.4

0.3

0.2

0.1
n increases towards k
dn
0
ndt 40 80 120 160 200
(k)
-0.1
n decreases towards k
-0.2

-0.3

-0.4

(c) 0.2
n increases towards upper,
stable equilibrium (U)
0.1
C U
dn 0
ndt
n decreases towards upper,
-0.1 stable equilibrium (U)

-0.2
n declines to
extinction
-0.3

-0.4

-0.5
0 40 80 120 160 200
Population size (n)

Fig. 4. Allee effects and simple population dynamics. a) A function such as the rectangular hyperbola can be
used to describe Allee effects. Allee effects increase in severity from left to right, with values of of 2, 10,
and 20. b) The standard logistic model of population growth accounts for negative density dependence only.
Below the carrying capacity (k), growth is positive, and the population increases towards k. Above k, growth

11
is negative. Thus k is a point of stable equilibrium. c) When an Allee effect from (a) is incorporated into the
logistic equation, the dynamics are radically altered. The population now has two equilibria, C and U. The
upper equilibrium, U, is stable, at a point somewhat below k from the logistic equation. The lower
equilibrium, C, is unstable and critical. Below this, the population is highly likely to tend towards extinction.
Population growth is positive, only in the interval between C and U. The distance between these equilibria
depends on the severity of the Allee effect.

Depending on the mechanisms involved, the implications of these simple models

may apply at either group, aggregation, or population level, whilst a similar mathematical
approach can also be applied to the persistence of metapopulations78. Where the model is
considered at a group level, there is a lower, unstable equilibrium, analogous to some
minimum group size, below which, mortality is likely to exceed natality. Such thresholds
are typical of obligate cooperators6. These are species in which helpers are required for
survival or reproduction, for example, for antipredatory measures; defending territories,
nests or dens; transporting young; or provisioning young, gestating or incubating females.
Examples of these include saddle-back tamarins (Saguinus fuscicollis), that rarely or never
attempt breeding as lone pairs, probably as a result of energetic restrictions on females, for
whom foraging, lactation and transport of infants would be too costly without additional
helpers to share infant carrying79. Similarly, reproductive success for pairs of dwarf
mongooses (Helogale parvula) without helpers is negligible13. A more extreme example
has recently been demonstrated for meerkats. In an area of high predation, juvenile
mortality in this species is inversely related to group size, and is extremely high for groups
of less than four individuals. Small groups of meerkats thus have extremely limited
reproductive success, particularly in harsh environmental conditions70.
Many group-living species show dominance hierarchies and some form of
reproductive suppression, such that only one pair in any group will breed. In such cases,
differences between actual population size, N, and effective population size, Ne, can be
striking. Examples include the gray wolf (Canis lupus), where the number of breeding
groups, rather than the number of individuals, controls increases in population
persistence80. Such dynamics have been suggested to account for the slow recovery of the
Ethiopian wolf (Canis simensis), following disease epidemics a decade ago7.
At the level of the aggregation, Allee effects can also impair reproduction when
individuals are present in low numbers, leading to unstable equilibria at minimum flock or
colony sizes. The example of reduced reproductive success in small colonies of guillemots
(Uria aalge), due to less effective predator swamping, is given in Table 1. The inability of
small flocks of some species of flamingo (Pheniconais spp.) to reproduce due to a lack of
social stimulation is indicated by studies of captive populations81, and provides another
example of an Allee effect at this level.
Of considerable concern to conservation biologists, is the interval between the
upper, stable, and the lower, unstable, equilibria. Populations fluctuate as a result of a
range of factors, including weather, disease, food supply, predation, or even
overcompensating density dependence82. If the amplitude of population fluctuation is of a
similar order of magnitude to the interval between the population's equilibrium sizes, then
this leads to the possibility of extinction. This has been suggested as an additional factor
leading to the dramatic extinction of the North American passenger pigeon (Ectopistes
migratorius)83.

12
 Finally, Allee effects may also have potential as a conservation tool. Conspecific
presence can be an important factor influencing patch choice, especially for younger
individuals84, and thus decoys or call playback can be employed to encourage preferential
colonization in protected areas, or recolonization of deserted or recently restored patches of
habitat85,76.
To summarise, the major direct consequences of Allee effects for conservation arise
from the change in population dynamics, particularly at low population sizes or densities.
Conservation is usually required because habitat loss or fragmentation, exploitation, or the
impacts of introduced predators, competitors or disease, have led to increased mortality in a
species or population. Species which are subject to strong Allee effects are likely to be far
less able to withstand these additional sources of mortality, far less likely to recover, even
after the source of mortality is checked, and far more likely to decline to extinction, than
are other species.

4. Mating systems and their direct consequences for conservation

The study of mating systems is crucial to many areas of conservation, not only those
concerned with assessing, understanding and treating risks due to Allee effects. Two of the
most important causes of anthropogenic extinctions, are over-exploitation and the impact of
introduced species.
Overexploitation accounts for almost one quarter of all extinctions of species since
1600, for which the cause can be identified86. In general, exploitation will cause increases
in mortality which, for species subject to Allee effects, may have unforeseen consequences
(see section 3). However, exploitation may have other consequences also, on which the
study of mating systems may have a more direct bearing.
Differential mortalities due to harvesting can affect mating systems and
reproductive parameters. Sport hunting is usually biased towards larger animals, and
frequently towards males. Selective removal of adult male ungulates by tourist hunters is
believed to reduce female fecundity, and modelling indicates that it could lead to
population collapses87. A classic example of a species subject to differential harvesting
pressure between sexes, is that of the African elephant (Loxodonta africana).
Traditionally, this species has been harvested for ivory. Tusk size varies between sexes
and also with age, so that ivory based exploitation very rapidly leads to populations with
distorted sex ratios and age structures76. These authors concluded that selective removal of
males can lead to sperm limitation, whilst selective removal of females would reduce the
size of female herds, decreasing the incidence of males finding female herds and,
consequently, also lowering per-capita fecundity.
In fisheries, sexual dimorphism can also lead to differential exploitation. Young
gag groupers (Mycteroperca microlepis) are predominantly female, transforming into males
as they grow larger, a trait known as protogyny. Differential mortality of the larger males
has been shown to lead to highly skewed sex-ratios, potentially leading to sperm limitation
(Koenig et al. 1996, cited in88). Other species of fish provide a range of examples of the
complex effects of exploitation on reproductive strategies88. Fish species which mature
late are also more susceptible to overexploitation89.

13
 Study of mating systems of exploited species may suggest a range of different
approaches to methods of exploitation. First, contrary to traditional approaches, where
larger adults are removed throughout the population, removal of whole groups might be
preferable to removal of small numbers of individuals from many different groups.
Depending on the mating system of the exploited species, this could prevent the
reproductive output of remaining groups from being compromised, permitting them to
increase and fractionate, and allowing vacant habitat to be recolonised. Second, selective
removal of males can have a particularly serious effect on monogamous species63 by
reducing local male densities and creating a mate finding Allee effect. For these species,
removal of pairs, rather than individuals at random, might also be preferable. Third, where
habitat is exploited, either for agriculture or, for example, timber production, knowledge of
the biology of resident species will be important in determining whether utilisation should
be intensive or extensive. Where a species is sensitive to habitat degradation, intensive
utilisation might be favoured; whilst this will reduce the quantity of available habitat,
remaining habitat will permit species to remain at natural local densities. If, by contrast,
animals are more tolerant towards habitat degradation, extensive utilisation will be
favoured, as this will maximise available habitat, and thus will be more likely to support
populations above critical threshold sizes.
The study of mating systems can also have an important bearing on the problem of
hybridization. Almost 40% of all extinctions of species since 1600 for which the cause can
be identified, can be attributed to introduced non-native species 86. Introduced species can
impact on populations of native species in a wide variety of ways, including by direct
predation, by competition, by spreading diseases to which native species are nave, or, if
closely related to a native species, by hybridization. The effects of predation, competition
or disease were alluded to in section 3, above, and derive mainly from the increased
mortalities which these cause. In this section, we will focus on the problem of
hybridization.
Hybridization and genetic introgression have been reported in all five classes of
vertebrates61. These processes underlie concerns for the future of the rare white-headed
duck (Oxyura leucocephala) that can hybridise with ruddy duck (O. jamaicensis)
introduced to Europe from North America90. Similarly, the Ethiopian wolf is threatened by
genetic introgression by feral domestic dogs (Canis familiaris)91, and concern exists over
the extensive hybridisation between native red deer (Cervus elaphus) and sika deer (Cervus
nippon) introduced to Scotland from Japan92. Susceptibility to genetic introgression will
depend on many aspects of mating systems, including modes of fertilisation, degree of
promiscuity, and nature of courtship behaviours. However, examples exist for almost all
conceivable breeding systems, across a range of taxa with many elaborate forms of
courtship behaviour. Viability of hybrid offspring can also be crucial in determining the
extent of the problem, although even where introgression is prevented by inviable hybrids,
loss of breeding potential can threaten the parental populations, as in European mink
(Mustela lutreola), whose females generally abort after mating with introduced male
American mink (M. vison)75.
A detailed knowledge of the mating systems and breeding biology of species which
can hybridize might render policies for prevention more effective. Understanding patterns
of mating and cues for mate attraction can help to identify the potential for hybridization93.
Slight differences in timing of breeding between the two species might be exploited to

14
cause disruption at the time favoured by the non-native species. Alternatively,
hybridization might be unidirectional. For example, studies of the Ethiopian wolf mating
system indicate that male dogs can mate with female Ethiopian wolves, but hybridization is
unlikely between female dogs and male Ethiopian wolves94. Selective control of free-
ranging males may thus be sufficient to prevent hybridization.
In general, the best way to avoid hybridization, or other risks of introduced species,
is to prevent the introductions from occurring. It is likely that many countries could adopt
much more stringent measures for preventing accidental spread of exotic species and
diseases, both by adopting stricter hygiene rules at docks and airports and by preventing
introduced species from becoming established. The potential impacts of roads, railways
and canals should also be considered in the light of their potential as corridors for the
movement of alien species. Even the use of deliberate habitat corridors has been criticised
on the basis that connectivity can accelerate the spread of introduced species95. Most
introduced species will be most easily eradicated whilst few individuals remain, and Allee
effects may make this even easier. However, Allee effects will also tend to depress
population increases whilst an alien species is present in low numbers, potentially
promoting complacency at the time when the species is most vulnerable to eradication.
The study of mating systems can also make a major contribution to conservation
through captive breeding and reintroductions. For many species, available habitat has been
so reduced, or remains threatened to such an extent, that the persistence of those species in-
situ cannot be assured. Habitat destruction is widely believed to be the predominant cause
of extinction96 and accounts for over a third of all recent extinctions for which the cause
can be identified86. For species threatened by habitat destruction, it might often be
necessary to take representative individuals into captivity, maintaining a reservoir
population until habitat can be restored, and other forms of threat neutralised. Despite
continued debate regarding the economic prudence of this approach97-99, this rationale has
led to a widespread commitment of zoos to captive breeding, and to the formation of a
Conservation Breeding Specialist Group (CBSG) within the World Conservation Union
(IUCN). Genetic considerations for captive breeding and release were discussed by
Frankham72 but it has been observed that for captive breeding at least, some of the
commonest difficulties are behavioural99. It is worth commenting on the contribution that
research into social and breeding systems can make to several aspects of these processes.
Social conditions may play an important role in encouraging captive animals of
many species to breed. Classically, most species kept for breeding are housed in male-
female pairs100. However, these arrangements might not always reflect the natural social
conditions of the species concerned. Some temporal variation in social organisation is also
common for many wild vertebrates. Allowing free mate choice may be an important aspect
of enhancing reproductive success in captivity67,100, even though this may conflict with
genetic considerations (see also Section 2). Detailed knowledge of mating and post-natal
behaviours may also reduce breeding failures, abandonment or death of young.
Wielebnowski100 cited the example of the cheetah (Acinonyx jubatus). As with several
other carnivore species, cheetah move their young when disturbed. Disturbance in
captivity may provoke this behaviour, and it is therefore important that more than one den
site is both available and provisioned.
Social facilitation of reproduction has been shown to be important in captive bred
lemurs. A study of the worldwide pattern of captive reproduction in Eulemur species over

15
the past 20 years showed that female black and mongoose lemurs (E. macaco and E.
mongoz, respectively) housed with additional conspecifics, have higher reproductive rates
than those maintained as part of an isolated pair55. As discussed in section 3, social
enhancement of group displays has also been indicated as an important element increasing
breeding success in several species of captive flamingos (Pheniconais spp.)101,81. It has
been shown that the incidence of breeding displays in smaller flocks can be increased by
the use of mirrors in indoor enclosures102. Mirrors provide the appearance of more birds
taking part in marching displays, which has a synergistic effect in encouraging other birds
to join the display.
Maintenance of natural social organisations may be especially important for species
intended for reintroduction. Previously, callitrichid primates were believed to breed in
isolated pairs. This is likely to be an artefact of captivity however, where energetic
constraints to breeding are far less significant than in the wild, and where the type of
cooperative polyandry seen in many wild callitrichids is thus not necessary103. Evidence
from studies of captive callitrichids suggests that experience of alloparenting and family
life are important determinants of future reproductive ability104. Callitrichids bred for
release in the wild should thus be housed in social conditions which more closely mirror
those experienced in natural habitat.
Studies of social behaviour and breeding strategies can also be of benefit to
introductions and re-establishment, particularly in making informed decisions regarding
founder population sizes, release sites and release procedure. Perhaps unsurprisingly,
number released has been shown to be positively related to likelihood of establishment for
both insects105 and birds106. Release procedure can be tailored to prevent Allee effects
which might result from aspects of the breeding behaviour. A tendency for long-range,
post-release dispersal may favour soft-release protocols involving temporary penning at the
release site. For example, simultaneous releases of male and female brush-tailed
phascogales (Phascogale tapoatafa), an arboreal Australian marsupial, resulted in
dispersing males failing to find the few females released. Staggered releases allowed
females to establish territories prior to the release of males, increasing the success of this
programme107.
To summarise, the study of mating systems can play an important role in many
areas of conservation, including management of exploited species; identification of the
risks, and subsequent control, of hybridization; and in captive breeding and reintroductions.
However, the capacity of the study of mating systems to contribute to conservation, has yet
to be fulfilled, and the links between these fields continue to offer enormous potential for
research.

16
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