Advantages and Disadvantages of Animal Behaviour No4

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.
4
Kevin Brewer
ISBN: 978-1-904542-70-4
This document is produced under two principles: 1. All work is sourced to the original authors. The images are all available in the public domain (most from http://commons.wikimedia.org/wiki/Main_Page). You are free to use this document, but, please, quote the source (Kevin Brewer 2013) and do not claim it as you own work. This work is licensed under the Creative Commons Attribution (by) 3.0 License. To view a copy of this license, visit http://creativecommons.org/licenses/bync-nd/3.0/ or, send a letter to Creative Commons, 171 2nd Street, Suite 300, San Francisco, California, 94105, USA.
2. Details of the author are included so that the level of expertise of the writer can be assessed. This compares to documents which are not named and it is not possible to tell if the writer has any knowledge about their subject. Kevin Brewer BSocSc, MSc (http://kmbpsychology.jottit.com/) An independent academic psychologist, based in England, who has written extensively on different areas of psychology with an emphasis on the critical stance towards traditional ideas. Orsett Psychological Services, PO Box 179, Grays, Essex RM16 3EW UK orsettpsychologicalservices@phonecoop.coop
Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4
CONTENTS
Page Number
1. SPERM COMPETITION Appendix 1A - Semelparity References
4 6 10
2. OBJECT PERMANENCE Apes Other animals Appendix 2A - Pseudo-replication References
12 13 14 16 16
3. RARE ENEMY EFFECT Tentacled snake Flush-pursuers References
18 18 22 24
4. ANIMAL NAVIGATION AND ORIENTATION USING POLARISED LIGHT Using polarised light Twilight Lunar polarisation References
25 25 27 28 29
5. TYPES OF PARASITISM Social parasitism Kleptoparasitism Hyperparasitism References
30 30 34 42 45
1. SPERM COMPETITION
Claw (2013) stated: "Sexual reproduction is ubiquitous across plants and animals - more than 90 per cent of vertebrates reproduce sexually" (p210). Reproduction has costs for its participants 1. For males it is the production of sperm, while for females it is the production of eggs (ova). These costs lead to a strategy where males adjust the number of sperm 2 transferred to females to optimise fertilisation success, while females use choosiness to decide whose sperm can fertilise their eggs. The male situation is known as sperm competition 3 4 (or "strategic ejaculation"; Gage 1991), and the number of sperm vary depending on female quality, and the number of rival males present, for example. In the latter case, it is predicted that males should give less sperm in ejaculations where competition is low and more sperm if the competition is high (sperm competition risk model). However, the sperm competition intensity model predicts that the number of sperm will increase if there is one rival male, but decrease if there are more than that (Worthington et al 2013). Using meta-analyses, Kelly and Jennions (2011) concluded that, as a generalisation, males have larger ejaculates with higher quality females 5, and when a male rival is present 6. In the latter case, significant relationships were found overall, in studies using direct measures of ejaculate size 7, both internal and external fertilisers, and with insects and with fishes (in particular) 8. There was no evidence that the number of sperm declined as the number of male rivals increased 9. The
For example, there is a trade-off for males between investment in testes and immunity (eg: crickets; Simmons 2012). Exposure to sperm competition has a cost of lower survival for the males as reproductive tissues and fluids are expensive in nutritional terms (Moatt et al 2013). 2 Ejaculates contain large numbers of sperm, depending on the species - eg: 20-50 million in humans and eight billion in domestic pigs (Claw 2013). 3 Sperm competition occurs post-copulation where females mate with multiple males among internal fertilisers and where several males are present as females spawn among external fertilisers (Parker 1970). 4 Extreme sperm competition has also been linked to suicidal reproduction (semelparity) (appendix 1A). 5 N= 40 species. 6 N = 33 species. 7 Ejaculate size is measured directly (eg: counting number of sperm) or indirectly (eg: ejaculation duration) in studies. 8 Adapting the sperm quality or quantity are classed as "plastic responses" to sperm competition (Moatt et al 2013). For example, fruit flies (Drosophilia melanogaster) alter the production of seminal fluid proteins in the face of a high risk of sperm competition (Moatt et al 2013). 9 N = 15 species. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 4
relationship between female mating status (virgin or already-mated) and number of sperm varied between studies 10 . There was no significant difference between ejaculate size and female mating status in studies using direct measures of ejaculate size, while studies using indirect measures found larger ejaculates transferred to virgin females. The findings also varied with the species studied. Worthington et al (2013) investigated the sperm competition intensity model with domestic crickets (Acheta domesticus) (figure 1.1). Females store sperm from multiple males in their spermatheca before using it for fertilisation, and an individual male will benefit by giving the female proportionally more sperm than this rivals. Sexually mature virgin males were randomly allocated to one of three conditions for the experiment - no rival males, one rival, or two rivals in clear cages nearby for five days prior to mating. Each male was given the opportunity to mate, and the number of sperm produced were measured. Male crickets transfer their sperm in a spermatophore which is produced prior to meeting a female, and is attached to her. The researchers removed the spermatophore immediately after attachment.
(Source: G-U Tolkiehn)
Figure 1.1 - Male Acheta domesticus. No significant differences in the total number of sperm or their viability (ie: number of living sperm)
10
N = 40 species. 5
were found between the three conditions. This is contrary to Gage and Barnard (1996) who found that the crickets produced more sperm in the presence of other males. This experiment allowed the males to physically interact, whereas Worthington et al (2013) only allowed visual, acoustic and olfactory cues without physical contact. The latter admitted: "Perhaps male A. domesticus determine sperm competition risk through physical contact with conspecific males during spermatophore formation prior to meeting" (Worthington et al 2013 p59). But Worthington et al (2013) found that smaller males produced significantly more viable sperm than larger males. Females prefer larger males and the mating opportunities for smaller males in the wild are less. "Although investing in higher ejaculate quality may require more resources and have significant costs associated with it, males that face limited future reproductive opportunities might strategically invest in high-quality ejaculate to increase fertilisation success in current reproduction and thus maximize their fitness" (Worthington et al 2013 p59). APPENDIX 1A - SEMELPARITY Semelparity (suicidal reproduction) is where the male dies after copulation/fertilisation 11, or the female dies after birth/laying eggs 12. It is more common in invertebrates and fish species than mammals, and exists for females where maternal care is not required after birth/hatching (Fisher et al 2013). Semelparity is present in only four genera 13 of mammals - insectivorous marsupials (eg: Antechinus "pouched mice"). The stress of mating is so great that the build up of corticosteroids in the blood leads to immune system collapse and death (Fisher et al 2013) 14. Different explanations have been given for semelparity in these mammals (Fisher et al 2013): i) Female have litters once a year to coincide with
The opposite is iteroparity (living for more than one breeding season) (Tallamy and Brown 1999). Or after weaning, as, for example, a long lactation period makes reproduction stressful and increases female mortality (Kraaijeveld et al 2003). 13 Genera is plural of genus. The biological hierarchy of living organisms has "eight levels"(taxonomic ranks) beginning with species, which are part of a genus, which are part of a family, and families make up an order (then class, phylum, kingdom, and domain). For example, the brown antechinus (Antechinus stuartii) (species), antechinus (genus), dasyuridae (family), dasyuromorphia (order), mammalia (class), chordata (phylum), animalia (kingdom). 14 Increased corticosteroids aid the breakdown of protein for energy, but also produce anaemia, gastrointestinal ulceration, and immune suppression (Oakwood et al 2001).
12
11
food peaks, and male survival between breeding seasons is low. Thus, one breeding season and death as postreproductive survivorship is poor (eg: Braithwaite and Lee 1979). ii) The behaviour is non-adaptive but is fixed in these species (eg: Oakwood et al 2001). Oakwood et al (2001) collected data on the northern quoll (Dasyurus hallucatus) (figure 1.2) in Kakadu National Park, Northern Territory, Australia 15. Mating takes place in late May and early June. In 1994 the researchers radio-tracked eight males, who died between 31st May and 4th July at a mean age of 11 months old. Generally, of males trapped in June, the majority had lice infestation (85%) (a sign of a poor immune system) compared to 8% of females at the same time and 23% of males in May. During the mating season males have increased testosterone, but weight loss, and loss of fur as well. However, the researchers did not find increased corticosteroids or gastrointestinal ulceration. Oakwood et al (2001) concluded: "These results suggest that die off may be the result of an unexplained phylogenetic predisposition in these species towards post-reproductive senescence" (p410).
(Source: John Gould (1863) "Mammals of Australia volume 1"; in public domain)
Figure 1.2 - Drawing of northern quoll.
Live trappings were made on two consecutive nights every fortnight between November 1992 and December 1993, and between January 1994 and February 1995. In total, 41 males were trapped, and 26 males were 7 months old or more (of which 85% disappeared, assumed dead, between April and June). Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 7
15
iii) The "accumulation of deleterious mutations after breeding" (Fisher et al 2013) (eg: Humphries and Stevens 2001). iv) Extreme male promiscuity involving mating with as many females as possible (that is lethally exhausting) because of low female survival ("male bet-hedging") (eg: Kraaijeveld et al 2003) 16. Kraaijeveld et al (2003) calculated the number of females that a male needs to mate with to guarantee one offspring surviving to the next breeding season. Based on data from a well-studied field population of agile antechinus (Antechinus agilis) (figure 1.3) in southern Australia, it was estimated to be between 6-14. For example, if female survival to care for offspring was only 40%, then a male would have to mate with around fourteen females to have an 80% chance of having offspring in the next generation. The mating season is only two weeks long, and each mating takes about three hours. Thus, "one can imagine that mating effort will consume large amounts of the males' energy" (Kraaijeveld et al 2003). Mills and Bencini (2000) reported that male dibblers (Parantechinus apicalis) (figure 1.4) were semelparous in a population where female mortality was high after breeding (60%), but not in a population with female mortality of half of that (ie: more females survived to the next breeding season, and consequently so did more offspring) 17.
Elgar et al (2013) argued that the term "promiscuous" to describe animal mating strategies is "anthropomorphic, inaccurate, and potentially misleading". It is more often used for female multiple mating (or polyandry). "Promiscuity has pejorative and androcentric connotations and is likely to be emotionally evocative, typically saved for the females of the species: while polygynous males maximise their fitness by mating at the highest rate, females are described as promiscuous. Perhaps promiscuous is used in titles and abstracts precisely because it is titillating, the notion of indiscriminate mating tapping into latent social taboos" (Elgar et al 2013 p5). The "Oxford English Dictionary" definition of the word is "without discrimination or method", but "the overwhelming evidence from diverse taxa confirms Darwins suggestion that females are typically circumspect about their mates, accruing a variety of benefits from their discriminate mating, including with multiple partners" (Elgar et al 2013 p1). Furthermore, when promiscuity is used an umbrella term to cover polyandry (one female and multiple males), polygyny (one male with multiple females), and polygynandry (multiple partners by either sex), it is unhelpful because it confuses the nature (discrimination or not) and the frequency of mating (Elgar et al 2013). In thirty-nine papers in the journal, "Animal Behaviour" (2000-2010) that used the term, 23 applied it to females, two to males only, and fourteen to both sexes (Elgar et al 2013). 17 Kraaijeveld et al (2003) summarised the data from eleven species of insectivorous marsupials. Eight of them had male semelparity, and female survival was less than 50%, whereas the three nonsemelparous species had female survival nearer to 70%. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 8
16
Figure 1.3 - Drawing of agile Antechinus.
Figure 1.4 - Drawing of dibblers.

Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 9
v) Altruistic paternal suicide to allow more food for offspring (eg: Diamond 1982), or avoid surviving males mating the next year with their daughters in a species with low dispersal and maternal semelparity (Kraaijeveld et al 2003). vi) Sexual selection where virgin females prefer young males or selection for male endurance. vii) Extreme sperm competition (eg: Dickman 1993) Insectivorous marsupials with low post-mating survival have longer copulation durations that those with higher survival rates (mean: 9.4 vs 3.7 hours; Fisher et al 2013). Longer duration blocks rival males from having the opportunity to displace or dilute sperm. These species also have larger testes in relation to body size (Fisher et al 2013). REFERENCES
Braithwaite, R.W & Lee, A.K (1979) A mammalian example of semelparity American Naturalist 113, 1, 151-155 Claw, K.G (2013) Rapid evolution in eggs and sperm American Scientist 101, May-June, 210-217 Diamond, J.M (1982) Big-bang reproduction and ageing in male marsupial mice Nature 298, 115-116 Dickman, C.R (1993) Evolution of semelparity in male dasyurid marsupials: A critique, and an hypothesis of sperm competition. In Carnio, J (ed) Carnivorous Marsupials Toronto: Metro Toronto Zoo Elgar, M.A et al (2013) Promiscuous words Frontiers in Zoology 10, 66
Fisher, D.O et al (2013) Sperm competition drives the evolution of suicidal reproduction in mammals Proceedings of the National Academy of Sciences, USA 110, 44, 17910-17914 Gage, A.R & Barnard, C.J (1996) Male crickets increase sperm number in relation to competition and female size Behavioral Ecology and Sociobiology 38, 349-353 Gage, M.J.G (1991) Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit fly Animal Behaviour 42, 10361037 Humphries, S & Stevens, D.J (2001) Reproductive biology. Out with a bang Nature 410, 758-759 Kelly, C.D & Jennions, M.D (2011) Sexual selection and sperm quantity: Meta-analyses of strategic ejaculation Biological Reviews 86, 4, 863-884 Kraaijeveld, K et al (2003) Does female mortality drive male semelparity in dasyurid marsupials? Proceedings of the RoyalSociety of London Series B: Biological Sciences 270, Supp 2, S251-S253 Mills, H.R & Bencini, R (2000) New evidence for facultative male dieoff in island populations of dibblers, Parantechinus apicalis Australian Journal of Zoology 48, 501-510 Moatt, J.P et al (2013) Exposure to sperm competition risk improves survival of virgin males Biology Letters 9, 20121188
10
Oakwood, M.A et al (2001) Semelparity in a large marsupial Proceedings of the RoyalSociety of London Series B: Biological Sciences 268, 407-411 Parker, G.A (1970) Sperm competition and its evolutionary consequences in the insects Biological Reviews 45, 525-568 Simmons, L.W (2012) Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus Behavioral Ecology 23, 168-173 Tallamy, D.W & Brown, W.P (1999) Semelparity and the evolution of maternal care in insects Animal Behaviour 57, 727-730 Worthington, A.M et al (2013) Do male crickets strategically adjust the number and viability of their sperm under sperm competition? Animal Behaviour 86, 55-60
11
2. OBJECT PERMANENCE
When moving prey momentarily disappears out of sight during a chase, say, predators need the cognitive ability to know that the prey still exists when not visible. This is known as "object permanence" - "the ability to spontaneously locate moving objects that have disappeared from view" (Fiset and Plourde 2012). For humans object permanence develops in the first 24 months of life through a series of six stages, according to Jean Piaget (1937). The first signs of understanding object permanence comes with the "A-not-B error". An infant sees an object hidden in location A, and they can retrieve it, but then when the object is hidden at location B, the infant searches at location A (stage 4 of object permanence). The last stage of object permanence is to understand invisible displacement 18. This is where a moving object disappears out of sight, and requires the ability to track the continued movement. The delayed response task is commonly used to study object permanence. The viewer sees an object hidden under one of three cups, say, and, after a short delay, is allowed to search for the object. This tests the basic concept of object permanence that an object still exists when out of sight, and memory. In a more advanced version (the inhibition test), objects will be placed under two of the three cups (eg: not the middle one). Call (2001) found that orangutans, chimpanzees and young children usually searched under the left or right hand cup first. "After successful retrieval of the first object, they proceeded by choosing the middle container, which they had just seen a few seconds ago to be empty. Evidently, subjects have problems skipping the middle container. Call (2001) suggested that this search error is most likely to be explained by an inhibition problem rather than a memory deficit" (Barth and Call 2006 p239). Invisible displacement is tested with three cups, say, on a rotated platform. The viewer sees the object hidden under one of the cups, and then the platform is rotated 180 or 360. In the case of 180 rotation, the left cup becomes the right one. Chimpanzees were able to recover the hidden food significantly more often than chance (Beran and Minahan 2000). Beran et al (2005) placed food rewards under two of five cups, and
The ability to pass invisible displacement tasks is evidence of "secondary representations" (Perner 1991). This is "the ability to consider multiple models of a situation - including past, future, or hypothetical models - rather than simply relying on what is immediately perceivable" (Jaakkola et al 2010 p104). Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 12
18
chimpanzees could find one of them successfully but not the second after rotation. In the transposition task, an object is hidden under one of three cups, and the cup is moved position once or twice (single or double transpositions), all in front of the viewer. Studies have found that bonobos, chimpanzees, and orangutans can find the object (as well as African grey parrots), but not cats and dogs nor children younger than three years old (Barth and Call 2006). APES Barth and Call (2006) compared the object permanence abilities of chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), orangutans (Pongo pygmaeus), and children. In the first experiment, apes at Leipzig Zoo, Germany, were used, and each individual animal performed thirty trials involving six different tasks based on placing a food reward under one of three cups. Task 1 was a delayed response task with a thirty-second delay and a control of no delay. Overall, the correct cup was chosen 85% of the time, which is significantly above chance (33%), and the apes were significantly better in the control than delay version. Task 2 was an inhibition test where food was hidden in two of three cups. The researchers were interested in whether the apes searched under the empty cup (usually the middle one). Only six of 24 apes did not search under the empty cup in four trials each. A test of the A-not-B error was the third task. The food was hidden under the left cup, for example, for three trials (A), and then under the right cup (B) on the fourth trial. Would the apes search under the left cup on the 4th trial? Only one orangutan did this. Task 4 involved rotations of 180 and 360 of the three cups after the food had been hidden. The correct cup was chosen 49% of the time, which is significantly above chance. The next task involved single or double transpositions. Overall, the correct cup was chosen 86% of the time (p<0.001). The final task (object permanence) involved the apes watching the experimenter place the food under one cup and then move it to another cup. The correct cup was chosen 72% of the time (p<0.001). The second experiment used the same tasks with 24 children (aged 2 years old) in Leipzig. The children performed significantly better than chance on most of the tasks, but poorer than the apes (overall mean: 63% correct vs 73% for the apes) (figure 2.1). The only
difference that was significant for task 5 (transpositions task) - 86% correct for the apes vs 49% for the children.
(Data from Barth and Call 2006 table 2 p244)
Figure 2.1 - Mean percentage of correct choices for different tasks. Fedor et al (2008) reported that ten gibbons from zoos in Hungary could pass single visible displacement (SVD) and single invisible displacement (SID) tests, but not the double invisible displacement (DID) one. The SVD task was seeing an object placed in one of three wooden boxes, while the SID task involved the experimenter hiding the object in their hand before placing it in one of the boxes. With the DID task, the experimenter places the hand hiding the object in one box and then moves the hand and object to another box in the view of the gibbon. OTHER ANIMALS Fiset and Plourde (2012) compared the object permanence abilities of domestic dogs (Canis lupus familiaris) and gray wolves (Canis lupus) finding no difference between the two species. In the first experiment with nineteen dogs and five wolves, invisible displacement was tested. Three black buckets were placed next to each other, and a piece of food was dropped into one bucket in front of the animal, then one of three things happened, depending on the condition: Substitution transposition condition (ST) - The bucket containing the food was moved a short distance. Double transposition condition (DT) - The bucket with the food and one empty bucket were moved.
14
Control of movement condition (CM) - The two empty buckets were moved. Success was measured by finding the food on the first search. Each animal performed in four trials for each condition. In the ST condition, the mean success rate was 0.96 (out of 4), 2.88 in the DT condition, and 2.46 in the CM condition. There were no significant differences between the two species, but overall the animals were significantly poorer in the ST condition. Fiset and Plourde (2012) stated: "The present data, therefore, support previous findings... showing that domestic dogs primarily encode the spatial location where they have seen an object disappear and do not plainly understand invisible displacement of object. Experiment 1 also extends this later conclusion to the gray wolf" (p120). The second experiment tested the A-not-B error with nine gray wolves and 22 dogs (of which about half the animals had been in Experiment 1). Each animal performed six trials in each of three conditions: A-not-B test - A piece of food is seen by the animal to be hidden behind one of three screens (screen A), and they must retrieve it. This happens on five trials, and then the food is hidden behind screen B in front of the animal. Single visible displacement condition (SVD) - The food is hidden behind one of the three screens (randomly chosen each time). Double visible displacement condition (DVD) - The animal sees the food hidden behind one screen and then immediately moved behind another screen. Both species did not commit the A-not-B error, and retrieved the food from behind screen B. The animals were successful in most trials in the SVD condition, and slightly less so in the DVD condition. This experiment established that the animals had stage 5 object permanence. Jaakkola et al (2010) confirmed bottlenose dolphins' (Tursiops truncatus) ability to perform visible but not invisible displacement tasks. Six dolphins at a research centre in Florida, USA, were tested in three ways using three large buckets after the animals had been trained on a "find the object" game. On a SVD task, where the object is placed in one of the buckets in front of the dolphin, the correct choice was made in 61% of the trials (which is significantly better
than chance). In the DVD task, where the object is placed in one bucket and then moved to another in front of the animal, a correct choice rate of 44% was not significant. The third test of invisible displacement involved the object placed in a bucket and the bucket being moved. The correct bucket was chosen in 40% of trials, which is not significantly different to chance. Scoring of the choice of bucket by the dolphin was done by an observer blind to where the object was hidden 19. APPENDIX 2A - PSEUDO-REPLICATION Researchers want to be able to generalise their findings from the sample to the whole population. A single measurement taken from each individual in a larger sample is usually best. But the amount of data can be increased by taking multiple measures of each individual in the sample and pooling them. This is an artificially inflated sample, and the data points are not independent but are classed as so, "which falsely raises statistical power and increases the chances of making a type I error (a false positive: rejecting the null hypothesis when it is true)" (Waller et al 2013 p483). It is called "pseudoreplication" (Hurlbert 1984) or the "pooling fallacy" (Machlis et al 1985) 20. Waller et al (2013) reported that over one-third of primate communication studies (published between 19602008) that used inferential statistics had at least one case of pseudo-replication data. For example, in a playback experiment, the researchers play a particular call and measure the responses. By not using only one response per individual animal, pseudo-replication occurs. Waller et al (2013) found that observation studies were the method most likely to have such data. REFERENCES
Barth, J & Call, J (2006) Tracking the displacement of objects: A series of tasks with great apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Homo sapiens) Journal of Experimental Psychology: Animal Behaviour Processes 32, 3, 239-252 Beran, M.J & Minahan, M.F (2000) Monitoring spatial transpositions by bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) International Journal of Comparative Psychology 13, 1-15
The experiments with different species are forms of replication of the original research, which confirms the generalisability of the findings (appendix 2A). 20 It is possible to take multiple measurements from individuals, but this requires "appropriate repeated measures statistical techniques" (Waller et al 2013) (eg: related t-test). Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 16
19
Beran, M.J et al (2005) Spatial memory and monitoring of hidden items through spatial displacements by chimpanzees (Pan troglodytes) Journal of Comparative Psychology 119, 14-22 Call, J (2001) Object permanence in orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes), and children (Homo sapiens) Journal of Comparative Psychology 115, 159-171 Fedor, A et al (2008) Object permanence tests on gibbons (Hylobatidae) Journal of Comparative Psychology 122, 4, 403-417 Fiset, S & Plourde, V (2012) Object permanence in domestic dogs (Canis lupus familiaris) and gray wolves (Canis lupus) Journal of Comparative Psychology 127, 2, 115-127 Hurlbert, S.H (1984) Pseudoreplication and the design of ecological experiments Ecological Monographs 54, 187-211 Jaakkola, K et al (2010) What do dolphins (Tursiops truncatus) understand about hidden objects? Animal Cognition 13, 103-120 Machlis, L et al (1985) The pooling fallacy: Problems arising when individuals contribute more than one observation to the data set Zeitschrift fur Tierpsychologie 68, 201-214 Perner, J (1991) Understanding the Representational Mind MA: MIT Press Cambridge,
Piaget, J (1937) The Construction of Reality in the Child (in French) Neuchatel: Delachaux & Niestle Suddendorf, T & Whiten, A (2001) Mental evolution and development: Evidence for secondary representation in children, great apes, and other animals Psychological Bulletin 127, 627-650 Waller, B.M et al (2013) Pseudoreplication: A widespread problem in primate communication Animal Behaviour 86, 483-488
17
3. RARE ENEMY EFFECT

The "evolutionary arms race" (Dawkins and Krebs 1979) is an example of co-evolution where prey evolve a new strategy to survive predation, and then predators evolve a counter-measure, and so on. But the "rare enemy effect" (Dawkins 1983) describes where a predator has evolved a counter-strategy to the prey's normally adaptive behaviour. TENTACLED SNAKE The rare enemy effect can be seen in the fully aquatic tentacled snake (Erpeton tentaculatus) capturing fish. Fish have evolved an escape response when they detect sounds and/or motion in the water of a predator called the C-start. The escape response begins with a Cshaped bend in the fish's body. When there is a sound to the left ear, say, this stimulates muscles on the right side of the body, while inhibiting those on the left side, and the fish escapes to the right (Catania 2011). This strategy makes sense - turn away from the direction of the predator. But Catania (2009) observed that fish turned into the mouth of the tentacled snake. The snake has evolved a hunting strategy that takes advantage of the normal escape response. The tentacled snake hangs from vegetation in the water mimicking a stick in a J-shape with its upper body and head. As the fish (eg: minnows; Gambusia affinis) swims close to the J-shape posture, the snake moves a portion of the body which startles the fish causing the escape response and thereby turning into the mouth of the snake (ie: when the fish is parallel to the long axis of the snake's head) (figure 3.1) (Catania 2011) 21. In 78% of 30 experimental trials the fish turned towards the snake's head (Catania 2009) 22. The snake can also predict where the fish will be after the turn. When the fist is oriented at a right angle to the snake's head, the snake strikes at where the fish will be after the escape response. Catania (2009) reported a strike success rate of 48% (19 of 40 trials), but only 12% if the fish did not produce the escape response.
The C-start takes 5-6 ms, and the strike 15-20 ms (Catania 2009). "If tentacled snakes are rarely encountered compared to other predators, as seems likely, then counter adaptations in fish may never evolve, as a rapid turn away from water disturbances is most often the best response" (Catania 2010).
22
21
18
(A. When fish approach the concave area between head and body, the snake feints with its body before striking, generating a water disturbance that usually startles fish toward the striking jaws. B. When fish approach the jaws at a right angle, the body feint usually startles fish away from the body. Adult tentacled snakes bias their strike to predict this future fish movement (C)) (Source: Catania 2010 figure 2)
Figure 3.1 - Tentacled snake hunting posture and strategy.

19
Tentacled snakes are born with this behaviour (figure 3.2) 23 24. Catania (2011) studied newborns removed after birth to individual housing to avoid learning before testing. A fish was presented behind a clear transparent sheet, so the snake could see and strike without contact) (figure 3.3). There were 100 trials with ten snakes (ie: ten trials each).
(AC show three different strikes at fish. The upper panels illustrate the movements of snake and fish with the initial position of the fish marked in gray. A small movement of the snake's body just prior to striking elicits a C-start escape response in the fish (despite the barrier) and the snake strikes toward the future position of the fish head) (Source: Catania 2010 figure 4)
Figure 3.2 - Strikes by newborns showing prediction of fish's future position.
The advantage of this innate ability to predict the fish's position and strike at the head increases the likelihood of capture when there is a high risk of starvation or predation, and some fish have defensive spines on their body (Catania 2010). 24 Catania (2010) described the tentacled snake as "a predator born with future prey movements in mind". Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 20
23
(A. Top view (camera view) of the apparatus. An upper water chamber with a bottom formed from a transparent plastic barrier contained the snake and was placed into the larger, lower chamber containing the fish. The upper chamber rests on two clear plastic supports creating a channel below the snake, separated from the snake by the clear barrier. A single fish was introduced in the channel. Thus snakes could see and strike at the fish without making contact. B. Side view showing the relationship between the two water chambers) (Source: Catania 2010 figure 3)
Figure 3.3 - Apparatus used by Catania (2010). Catania (2010) pointed out: "It should be emphasised that the predictive nature of the strikes... is qualitatively different from predictions of prey (or object) position based on initial movements and trajectories... Predicting the future position of a moving object is common, and equivalent to a batter striking a baseball based on brief visual information about its initial trajectory. Extending this analogy to tentacled snakes it would be as if the batter could estimate the position of the ball in time and space without ever seeing the pitch. Moreover,... they can do this without ever seeing any pitches". "Handling time" for predators is the time taken to capture the prey and eat. Catania (2010) compared the handling times (from strike onset to fish disappeared in snake's mouth) on three types of attack - head of fish first and swallow, tail of fish first and swallow, and attack tail but swallowed head first. The first attack strategy was quickest with a mean time of 15 seconds. The tail first and swallow took an average of 63 seconds, and the other strategy 87 seconds (figure 3.4). Tentacled snakes are vulnerable to predation themselves during the handling time, and Smith et al (2002) noted a tail-wiggling behaviour during this time. This seems to be a way to distract the snake's predators and focus an attack at that end rather than at the head.
21
("Moved to head" refers to fish that were grasped tail-first, but then manipulated into a head-first position for swallowing) (Source: Catania 2010 figure 9)
Figure 3.4 - Handling time for swallowing fish from different directions. FLUSH-PURSUERS "Flush-pursuers" (Remsen and Robinson 1990) are another example of the rare enemy effect. These are birds that cause their landed insect prey to produce a flight response and chase the insect in the air rather than attack the landed insect. The flight response is the normally adaptive strategy to the appearance of a predator. "Thus, the flush-pursuers are good examples of predators exploiting insect anti-predatory behaviour" (Jablonski 1999). Examples of flush-pursuers are Myioborus species (whitestart), Setophaga ruticilla (American redstart), and most Rhipidura (fantails), and they forage on the ground with constantly half-spread wings and tail exposing light patches on these parts of the body (Jablonski 1999). Jablonski (1999) studied the painted redstart (Myioborus pictus) (figure 3.5), which is a bird found in
22
the south-western USA, with a black body, but white patches on the under-surface of the wings. It hunts landed insects that mostly escape from predators by flying or jumping. Half-spread wings display the white patches which help flush the insect as the bird hops around in trees, on the ground or on rocky walls.
(Source: Dominic Sherony)
Figure 3.5 - Painted redstart. In field experiments in Arizona, Jablonski (1999) covered the white patches with black dye of seven experimental birds, and they were significantly poorer at flushing insects than before dye and compared to seven control birds (unaltered). The experimental birds dropped from an average of 2.4 chases per minute before dye to 1.5 with dye (while the control group had 2.1 - 2.7 chases per minute). Jablonski (1999) also observed that the white patches produced more flushing more often when the insect was in front and above the bird. This was based on 52 chases. Jablonski (1999) noted: "My impression from these observations, as well as from some slow-motion videorecorded foraging sequences, was that the birds do not detect these insects until after they are flushed" (p10). Subsequently, Jablonski (2001) showed that the painted redstart flush the insect to escape in a
direction across the central field of the predator's vision. Thus making it easier to track and capture the prey. Jablonski (2001) argued that the white patches against the black body of the bird not only startle the prey causing it to fly, but also confuse it in terms of direction to fly towards. Jablonski (2001) used models of redstarts in a laboratory with landed flies. When the model had a raised open tail, the flies were significantly more likely to escape in the direction of the bird's field of view than to a model without the raised open tail (68% vs 26% of escapes). Flush-pursuers are a small proportion of predators (eg: 15-30% of a guild 25; Jablonski 1999), and there are stronger selection pressures on insects to avoid birds that attack landed prey and non-avian predators. "Hence, foraging based on exploitation of insect escape responses might have evolved due to the rarity of the flushpursuing predators" (Jablonski 1999). REFERENCES
Catania, K.C (2009) Tentacled snakes turn C-starts to their advantage and predict future prey behaviour Proceedings of the National Academy of Sciences, USA 106, 27, 11183-11187 Catania, K.C (2010) Born knowing: Tentacled snakes innately predict future prey behaviour PLoS ONE 5, 6, e10953 (Freely available at http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0010953) Catania, K.C (2011) Natural-born killer Scientific American 64-67 Dawkins, R (1983) The Extended Phenotype Press Dawkins, R & Krebs, J.R (1979) Arms race between and within species Proceedings of the Royal Society, Series B. Biological Sciences 205,489-511 Jablonski, P.G (1999) A rare predator exploits prey escape behaviour: The role of tail-fanning and plumage contrast in foraging of the painted redstart (Myioborus pictus) Behavioral Ecology 10, 1, 7-14 Jablonski, P.G (2001) Sensory exploitation of prey: Manipulation of the initial direction of prey escapes by a conspicuous "rare enemy" Proceedings of the Royal Society, Series B. Biological Sciences 268, 10171022 Remsen, J.V & Robinson, S.K (1990) A classification scheme for foraging behaviour of birds in terrestrial habitats Studies in Avian Biology 13, 144-160 Smith, T.L et al (2002) Predatory strike of the tentacled snake (Erpeton tentaculatum) Journal of Zoology 256, 2, 233-242 Oxford: Oxford University April,
A "predator guild" is a term used to cover different species of predators that are hunting the same prey in the same environment. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 24
25
4. ANIMAL NAVIGATION AND ORIENTATION USING POLARISED LIGHT

Visual cues in the sky are the basis of navigation and orientation for many species. These cues include the position of sun, moon or other celestial bodies, and polarised light. This is the scattering of light from air molecules, water, and dust in the atmosphere, for example 26 . The polarisation pattern changes during the day as the sun apparently moves across the sky, and the time of the year. When the sun is at its zenith in the sky, the pattern is a circle around the horizon and the sky is polarised horizontally along the horizon, but at twilight the pattern is north-south (ie: vertical) (figure 4.1) 27.
(Based on drawings at http://www.polarization.com/sky/sky.html)
Figure 4.1 - Pattern of polarisation when the sun at zenith and at twilight. USING POLARISED LIGHT Ugolini et al (2013) investigated the use of skylight polarisation by sandhoppers 28 (Talitrus saltator) (figure 4.2) captured in Italy. These very small amphipod crustaceans live on the seashore and need cues to help them to return to the damp area of sand where they live. With the movement of tides, there is a risk of dehydration if they are dry for too long, so they need to know the sea-land axis direction. The experimenters placed the sandhopppers in a dry area in the middle of a plastic tube with two different
Also scattering of light as enters water gives polarisation underwater, or unpolarised light reflected by surfaces or bodies. Underwater light reflected from the surface of the sea is horizontally linearly polarised, while light from the shore is less scattered and less polarised (Hanke et al 2012). 27 The same applies with the moon. Polarised light will also be produced by starlight. 28 Sometimes called sand flea. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 25
26
(Source: Julio Reis)
Figure 4.2 - A sandhopper. options. The light from each end of the tube was varied. For example, polarised white light versus non-polarised white light. In the case of artificial light choices, the sandhoppers moved towards polarised light. In experiments with natural light at the same time of each day, sandhoppers were placed in the middle of a bowl divided into four quadrants and their direction of movement was recorded 29. Sometimes the sun was visible, and different filters were placed over the bowl to polarise the light. This also sometimes altered the perceived direction of the sun. The sandhoppers moved towards the direction or the perceived direction of the sea throughout the experiments. Some spiders have been found to response to polarised light in experiments, including the river wolf spider (Arctosa variana), funnel web spiders (Agelena labyrinthica), and the blue-grey ground spider (Drassodes cupreus) (Dacke et al 2001).
Ugolini et al (2012) tested the role of skylight gradient of luminance by creating a dome in which to place the sandhoppers. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 26
29
Dacke et al (2001) experimentally investigated the wolf spider (Pardosa tristis) by placing the spider on a lightweight ball while attached to a wire in an arena with an optical motion sensor. So when the spider moved its legs as in walking, it remained stationary and the ball moved. This showed that the spiders moved in response to changes in the polarised light. Dacke et al (2001) observed that the "luxury of having eight eyes has allowed lycosid and gnaphosid spiders to devote eyes to the detection of polarised light" (p2488). Hanke et al (2012) found that two captive trained harbour seals (Phoca vitulina) did not use polarised light in experiments using a specially designed LCD monitor. The seals were trained to move their heads when a particular shape appeared on a screen. But when shapes were presented "whose contrast was purely defined in terms of polarisation" (ie: lacked luminance contrast), the seals did not respond. TWILIGHT During twilight the light of the whole sky is polarised in one direction. At this time, the zenith of the sky has the highest degree of polarisation of the day, which stretches in a band from south to north across the sky. "The remainder of the skylight is polarised in a parallel direction with falling degrees of polarisation towards the sun and the anti-sun. On nights with a full moon, a similar pattern of polarised light will also form around the source of light" (Dacke et al 2003 p1535). Under moonless twilight skies, Dacke et al (2003) set up a filter that made the southerly-northerly oriented polarised light pattern of evening skylight appear to change by ninety degrees. Dung beetles (Scarabaeus zambesianus) rolling their ball of dung in one direction made a mean turn of 80 under the filter. "The recorded turn of the beetles under the filter thus shows that polarised light could well be the primary cue used by the beetle to maintain its bearing" (Dacke et al 2003 p1540). Dacke et al (2003) had established that the beetles follow a path in one direction by placing an obstacle in the way. Once the beetle has navigated around the obstacle, it follows the path of the original direction. But this is orientation (or leaving) (the movement in a particular direction), which is different to navigation (homing) (the movement towards a particular point). "An obvious difference between homing and leaving is, of course, that the leaving beetle has a set place to start, while the homing animal has a determined place to
stop" (Dacke et al 2003 p1539), but moving in a straight line is the best solution for both (figure 4.3).
Figure 4.3 - Difference between orientation and homing. LUNAR POLARISATION Dacke et al (2004) reported that the African dung beetle (Scarabaeus zambesianus) uses the polarisation pattern of the moonlight sky to navigate. The beetles collect dung from mammals, which they mould into a ball and roll away from competitors to bury. In the laboratory experiments, a beetle is placed in a large arena with its ball of dung. Three lamps are placed at different points and illuminated one at a time to produce the "artificial moon". One light would be on, and as the beetle moved towards it, it would be turned off and another light (say 90 away) would turn on. The beetles changed their direction within two seconds. This showed that the beetles orientate towards the light source (ie: moon). But there will be times when a clear view of the moon is not available, either because of clouds or trees, say. Dacke et al (2004) argued that the beetles use the polarisation pattern spanning the entire sky. In field experiments in South Africa when the real moon was hidden from view, an artificial moon at an angle of 180 was introduced. Thirteen of fifteen beetles did not change their direction of travel in this situation. Each animal stopped rolling its dung, "then climbed on top of its ball and performed an orientation dance, rotating about its vertical axis, presumably reading the polarisation pattern of the skylight. Each beetle then descended from the ball and continued to roll in a direction not significantly different from its original direction of travel..." (Dacke et al 2004 p363). Dacke et al (2004) concluded: "From our two
experiments, we reach the conclusion that the moon's disc serves as only a secondary cue in the orientation of S. zambesianus. Instead, the primary cue for orientation seems to be the polarisation pattern formed around the moon, a cue that is more reliable for orientation. While the moon is more easily hidden behind a single cloud or the branch of a tree, the polarisation pattern will be obscured only under completely overcast conditions. Patterns spanning the entire sky will provide the beetle with more precise compass information than will an individual pixel of the sky" (p364). REFERENCES
Dacke, M et al (2001) Polarised light detection in spiders Journal of Experimental Biology 204, 2481-2490 Dacke, M et al (2003) Twilight orientation to polarised light in the crepuscular dung beetle Scarabaeus zambesianus Journal of Experimental Biology 206, 1535-1543 Dacke, M et al (2004) Lunar orientation in a beetle Proceedings of the Royal Society of London, Series B: Biological Series 271, 361-365 Hanke, F.D et al (2012) Are harbour seals (Phoca vitulina) able to perceive and use polarised light? Journal of Comparative Physiology A 199, 6, 509-519 Ugolini, A et al (2012) The skylight gradient of luminance helps sandhoppers in sun and moon identification Journal of Experimental Biology 215, 2814-2819 Ugolini, A et al (2013) Do sandhoppers use the skylight polarisation as a compass cue? Animal Behaviour 86, 427-436
29
5. TYPES OF PARASITISM
"Parasitism is the most common life style on earth and virtually all organisms are affected by it" (Pamminger et al 2012 p39). It is the ability of one organism (parasite) to take advantage of another organism (host). There is no benefit to the latter, and it is to their complete disadvantage. Thus the parasite is able to manipulate the host. SOCIAL PARASITISM Social or brood parasitism is where the host raises the offspring of the parasite instead of or as well as their own. For example, larvae of the cuckoo butterfly (Maculinea rebeli) release chemical signals that mimic the grubs of Myrmica ants 30. The ants carry the larvae back to the colony and feed it. The larvae live there for 11-23 months and obtained all the nutrition needed to develop (Thomas et al 2013). The social parasitism is very specific for this butterfly. Thomas et al (2013) swapped cuckoo butterfly larvae from Spain and Poland with the different Myrmica ant species they each exploit, and there was 100% mortality. Thus the chemical signals given by the butterfly larvae only mimic the host in their area. Social parasitism is not a one-way street as hosts have evolved defence strategies against the exploiters. For example, the reed warbler (Acrocephalus scirpaceus) has evolved the ability to recognise the egg of its social parasite, the common (Eurasian) cuckoo (Cuculus canorus), which is different to its own, and remove it from their nest. Shortly after egg-laying the cuckoo visits a briefly unattended host's nest, removes one of the eggs, and lays her own in its place. The cuckoo then flies away until the host's egg to eat. This process takes ten seconds. Rates of parasitism in the UK of 5-20% have been reported (Britton et al 2007) 31. In response to the reed warbler's behaviour, cuckoos eggs subsequently evolved to mimic the host's eggs in size, colour, and patterning 32 (figure 5.1) 33.
Myrmica schencki and Myrmica sabuleti. Cuckoos also social parasitise the nest of great reed warblers, dunnocks, meadow pipits, robins, and pied wagtails (Britton et al 2007). 32 Or to be cryptic (ie: similar to dark nest interior and not seen by host) (Grim 2011). 33 In terms of the similarity of social parasite eggs to host eggs, human vision is different to that of birds. Thus what appears different or similar to us is not necessarily the same for birds (eg: birds pay attention to UV colours). Also olfactory cues may be involved (Grim 2011).
31
30
30
(Source: Simon Speed; in public domain)
Figure 5.1 - Four clutches of reed warbler eggs with cuckoo egg present. The cuckoo chick often hatches first and forces the other eggs out of the nest. The hosts do not stop this happening. The next step in this "evolutionary arms race" (Dawkins and Krebs 1979) would be for the reed warbler to recognise the cuckoo chick which is physically different to its own (figure 5.2), and remove the chick from the nest, but this has not occurred (Britton et al 2007). One suggestion is that this second defence strategy has not evolved due to strategy-blocking - a resource trade-off such that "the employment of one strategy affects the resources available for employing the other" (Britton et al 2007). The trade-off is in relation to getting the
(Source: Per Harald Olsen)
Figure 5.2 - Reed warbler feeding cuckoo chick. strategy wrong (ie: killing own offspring) versus the risk of being parasitised. Chick ejection requires a stronger selection pressure to evolve than egg ejection. "Obviously, a host correctly rejecting parasite eggs ('rare enemies') will have no chance to face parasite chicks (which, as a consequence of host own behaviour, become even 'rarer enemies'). Paradoxically, egg-rejecting hosts themselves eliminate selection pressure that would enable them to evolve an ability to discriminate parasite chicks... Thus, successful previous lines of defence (including
nest defence...) decrease positive selection pressure on later lines of defence" (Grim 2011). The opposite in defence strategies is seen in the superb fairy-wren (Malurus cyaneus) (host), which rejects the chick of the Horsfield's bronze-cuckoo (Chrysococcyx basalis) but not the egg. Social parasitism rates of 1632% have been reported in Australia (Britton et al 2007). Physically removing the invading chick is rarely seen - another example is the Mangrove gerygones (Gerygone laevigaster) ejecting Little Bronze-cuckoo (Chalcites minutillus) hatchlings from the nest (Tokue and Unda 2010) 34. This study showed that "chick discrimination may take place (a) almost immediately after the parasite hatches, and (b) without rejection errors (though in small sample sizes), thus (c) rejecting host individuals saved their whole current parental investment before the parasite chick had a chance to destroy it" (Grim 2011). Anti-social parasite strategies by birds also include the host deserting the nest, feeding the parasite chick less (ie: starvation), or attacking it (Grim 2011). One strategy would be to prevent the laying of the egg by the social parasite. This is done by the mobbing of parasites as soon as they are spotted in the vicinity by the host birds (Pamminger et al 2012). Slave-making ants (eg: Protomognathus americanus) (social parasites) depend on ant workers of other species (hosts) (eg: Temnothorax longispinosus) to perform routine tasks in the colony. Slave-making ants attack other colonies, and steal the host brood which are developed as workers. The hosts have developed defence strategies prior to enslavement including aggression or escape, and a postenslavement defence called "slave rebellion" (Achenbach and Foitzik 2009). Enslaved Temnothorax longispinosus ants kill a large proportion of the pupae of the slavemaking ants. This is an indirect benefit for the individual ant, but is beneficial to their kin in other colonies of hosts. Pamminger et al (2012) recorded a survival rate of less than 50% of slave-making ants observed in New York, West Virginia, and Ohio states in the USA. Social parasitism may actually be part of a mutualistic relationship. For example, brood parasitism by cowbirds is tolerated by the hosts because cowbird chicks remove botfly larvae from the host chicks (Smith
Grim (2011) explored factors that account for the rare number of documented cases rather than necessarily the rarity of the behaviour. Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 33
34
1968). Britton et al (2007) pointed out that this idea has been questioned. KLEPTOPARASITISM Kleptoparasitism (or "aerial piracy" by birds) is "the harassment of one bird species by another in order to force the victim to give up its food" (Riensche et al 2012) (figure 5.3), or stealing prey from an individual returning to the nest after successful foraging (Toms 2013) 35. Though birds have been most studied, it is reported by fish, mammals, reptiles among others (Flower et al 2013).
(Source: Duncan Wright; in public domain)
Figure 5.3 - Great frigatebirds chasing booby with food.
Brockmann and Bernard (1979) emphasised the opportunistic theft of food by one individual from another. Morand-Ferron et al (2007) described it as the "stealing of food items already procured by others" and the "stealing of food discovered and captured by other foragers". Cooper and PrezMellado (2003) called it "interference competition". Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 34
35
It is effective where the prey is too large to eat immediately, or requires further processing to eat (eg: breaking shell to access shellfish) (Barnett 2012) 36. Kleptoparasitism is beneficial when food sources are scarce, or when it enables a species to gain new food access. Generally, it is viewed as a high-risk, high payoff strategy (Flower et al 2013). Cooper and Prez-Mellado (2003) gave Balearic lizards (Podarcis lilfordi) pieces of fruit that were too large to swallow immediate, and thus required longer handling times. Food stealing occurred in just over half of such situations. Food owners responded by running away with the food. Other counter-measures to kleptoparasitism include increased vigilance during food handling, rapid swallowing, or foraging alone (Cooper and Prez-Mellado 2003). A number of birds have been observed using kleptoparasitism regularly - eg: herring and lesser black-beaked gulls; Arctic skuas; great skuas (Toms 2013). Reinsche et al (2012) reported interspecies kleptoparasitism with the first published observation of adult Forster's tern (Sterna forsteri) harassing adult California least terns (Sternula antillarum browni) returning to their young with fish. The attackers flew towards, chased and attempted to steal fish from the bills of the victims. When the latter is forced to drop their fish, the Forster's tern then recovers it. The observations were made at East Bay Regional Park on the eastern shore of San Francisco Bay, California, USA, where both species have nesting colonies. As a foraging strategy, kleptoparasitism can be occasional or opportunistic (eg: spotted hyenas - 20% of carcasses in one study) or the main tactic (eg: spider, Curimagua bayano) (Flower et al 2013). Shealer and Spendelow (2002) found that roseate terns (Sterna dougallii) (figure 5.4) benefit from kleptoparasitism over self-foraging (ie: hunting for own food) when at the breeding colony, and these birds have greater reproductive success than non-kleptoparasite members of the same species. The average prey delivery to the nest of ten kleptoparasitic individuals was 2-13
Longer handling time (ie: prey cannot be swallowed immediately in one go) makes the animal vulnerable to kleptoparasitism. For example, Broadley's flat lizards (Platysaurus broadleyi) observed at Augrabies Falls National Park in South Africa took about 30-60 seconds handling time for figs (eg: taking bites) compared to immediately swallowing small flies (the staple food) (Whiting and Greef 1997). Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 35
36
times higher than matched "honest" (non-kleptoparasitic) roseate terns.
(Source: US Fish and Wildlife Service Northeast Region)
Figure 5.4 - Roseate tern. Shealer et al (2004) reported data showing that chicks of kleptoparasitic roseate terns had greater survival and superior growth than chicks of "honest" parents. Ten kleptoparasitic individuals at a colony site on Falkner Island, Connecticut, USA (figure 5.5), were compared to non-kleptoparasitic individuals and the averages for the whole colony for the period 1990-99. Roseate terns usually lay two eggs, and the first to hatch is designated as the "A-chick", and the last to hatch as the "B-chick". Measures of growth were taken at three days, around thirteen days, and about 28 days after hatching. Both chicks of a kleptoparasite parent had superior growth to chicks of "honest" parents and the colony average, but the difference was larger for Bchicks. Survival was measured by the chick fledging (ie: leaving the nest), and this was significantly higher for kleptoparasitism-fed chicks. This difference can be presented as 45% more fledglings per kleptoparasite individual. Overall, kleptoparasitism was most beneficial for survival of B-chicks.
36
(Drawn with MapCreator 2.0)
Figure 5.5 - Position of Falkner Island. Only a small number of roseate terns are habitual kleptoparasites (3-5%), and it was unclear to the researchers as to why this is so when the behaviour is beneficial. Shealer et al (2004) commented: "The fact that the pool of kleptoparasites comprised the same individuals year after year... suggests that kleptoparasitic behaviour becomes fixed at some point in life... [but] some mechanism (eg: high cost or phenotypic constraint) prevents most individuals from adopting this strategy" (p375). Flower et al (2013) compared kleptoparasitism and self-foraging by a bird living in the southern Kalahari Desert in Africa - the fork-tailed drongo (Dicrurus adsimillis) (figure 5.6). Usually they forage alone for small flying insects or other prey on the ground. Their kleptoparasitism includes following other species (mostly other birds, but also meerkats, for example) and catching prey disturbed, or by physical attack on other species or use of false alarm calls. This is better described as "stealth kleptoparasitism".
(Source: In public domain)
Figure 5.6 - Fork-tailed drongo. Flower et al (2013) asked three key questions about kleptoparasitism by the fork-tailed drongo: 1. Is it mutually exclusive to other foraging strategies - ie: is it a choice between kleptoparasitism and selfforaging or can they both be used together? 2. What is the amount of time spent following other species relative to the environmental conditions? 3. What is the pay-off of keptoparasitism compared to other foraging strategies? Kleptoparasitism involves potential physical contests and energy expended in chasing prey-owner. These questions were answered by 292 focal observations of twenty-five individual birds in MarchAugust 2008 in xeric savanna (semi-arid harsh grassland) on the edge of the Kalahari Desert, Republic of South Africa (figure 5.7). The birds were observed by binoculars from 20-30 m away, though they were habituated to human presence nearby. Focal observation involves following one individual for a certain period of time. Each bird was observed for between 10-47 hours. With a hand-held computer, the observer recorded the time engaged in each foraging behaviour, whether the foraging was successful, and the size and type of prey. The size of prey caught were categorised on a fourAnimal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 38
point scale relative to the size of the drongo's bill length (eg: "tiny" = < bill length).
(Drawn with MapCreator 2.0)
Figure 5.7 - Area of observations by Flower et al (2013). The majority of time was spent foraging alone (about three-quarters of foraging time). But of the time spent following other species, half of that involved selfforaging (eg: catching disturbed prey). When following other species, the drongos perched lower to the ground and moved less frequently than when self-foraging. Thus, following other species was incompatible with effective self-foraging (answer to researchers' question 1 above). Kleptoparasitism was more common in the morning than evening, and by males, and when the temperature was low. Cold mornings were a time when food was scarce, in particular, and thus kleptoparasitism occurred when the food available was low (answer to question 2 above). The prey gained from kleptoparasitism were larger and terrestrial (eg: lizards) compared to caught alone. Thus, kleptoparasitism exploited a novel foraging niche, particularly prey that required digging up (eg: scorpions) (answer to question 3 above).
39
Flower et al (2013) noted that drongos have large brains relative to body size (ie: more intelligent than other birds). Reasons for Kleptoparasitism There are two main mutually exclusive theories for the evolution of kleptoparasitism (in birds) (brawn vs brain), and three other factors that are not mutually exclusive (Morand-Ferrin et al 2007): i) "Brawn" hypothesis - Kleptoparasitism as "a form of aggressive food competition where the thieves may use threats or actual physical aggression to force the host to abandon its prey item" (Morand-Ferron et al 2007). Thus, kleptoparasitism will be favoured by larger birds over smaller ones. ii) "Brain" hypothesis - Kleptoparasitism evolved among birds who have the skill to use it - eg: ability to predict the behaviour of others. "Cognitive abilities allowing the integration and use of more information in decision-making might thus increase the probability of kleptoparasitic success" (Morand-Ferron et al 2007). iii) "Vertebrate prey" hypothesis - Kleptoparasites tend to go for vertebrate prey, which contains more energetic value, but has longer handling time for the host. iv) "Group-foraging" hypothesis - Kleptoparasitism is more common in crowded environments where food is scarce and the opportunities for stealing are available. v) "Habitat openness" hypothesis - Open habitats (eg: grassland) offer better opportunities to detect potential victims than closed habitats (eg: forest). Morand-Ferron et al (2007) analysed 856 reported cases of interspecies kleptoparasitism by 197 species of birds from 33 avian families. The most reports were by birds in the Laridae (eg: seagull) and Accipitridae (eg: hawk, eagle) families. The likelihood of a family using kleptoparasitism was linked to larger brain relative to body, open habitat, and vertebrate prey. Host Kleptoparasitism has costs for the host in energy and time spent acquiring food that is stolen, time and energy in avoiding kleptoparasites, and less food for
young. Gorman et al (1998) calculated the cost to the African wild dog (Lycaon pictus) of kleptoparasitism by the spotted hyena (Crocuta crocuta). The wild dogs, observed in Kruger National Park, Republic of South Africa, usually hunt for 3-4 hours per day. A loss of a quarter of food through kleptoparasitism would mean hunting for over twelve hours per day to restore the energy balance, and a loss of over one-third would require non-stop hunting (ie: 24 hours per day). Daily energy expenditure (DEE) was calculated by using the doubly labelled water (DLW) technique. Temporarily captured animals were injected with radioactively labelled water, which will be taken up in the blood supply. When a later blood sample is taken (eg: after 48 hours), it is possible to establish the amount of the isotopes in the blood and calculate DEE via estimating carbon dioxide production. The principle is that energy expended involves breathing in oxygen which produces the byproduct of carbon dioxide to be exhaled. The DEE is then compared to the estimated calorie intake from food. More technically, the basis of the DLW technique is "that oxygen turnover in a body is dominated by the flow of water through the body as well as inspired oxygen and expired carbon dioxide. The turnover of body hydrogen, however, is dominated only by the flow of water through the body. Consequently, the difference between the turnovers of oxygen and hydrogen provides a measure of the excess efflux of oxygen that is equivalent to the production of carbon dioxide" (Speakman 1998 p934S). This is done by isotopes of both oxygen and hydrogen being injected into the body. A measure of carbon dioxide production (and energy expenditure) can be made from the difference in the isotopes of oxygen and hydrogen between injection (time 1) and current measure (time 2) (figure 5.8).
(Based on Speakman 1998 figure 2 p934S)
Figure 5.8 - Theoretical basis to DLW technique.

41
The main advantage of the DLW technique is that the animal can be free-living (ie: not confined to respirometry chamber in a laboratory that measures oxygen use). HYPERPARASITISM Hyperparasites are parasites that parasitise other parasites. For example, the false king crab (Paralomis granulosa) is parasitised by a barnacle (Briarosaccus callosus), and this, in turn, is hyperparatised by Liriopsis pygmaea (Blackman 2013). Figure 5.9 shows the basic process with caterpillars and parasitic wasps.
(The primary parasitoid Cotesia glomerata (CG) and the solitary Cotesia rubecula (CR) attack caterpillars of Pieris (PR) butterflies, which are in turn attacked by several hyperparasitoids: Acrolyta nens (1), Lysibia nana (2), Pteromalus semotus (3), Mesochorus gemellus (4), and Baryscapus galactopus (5)) (Source: Poelman et al 2012 figure 1)
Figure 5.9 - Hyperparasite and parasite community on Brassica oleracea plants.

One well studied example of hyperparasitism is the large cabbage white butterfly (Pieris brassicae) (figure 5.10). Its caterpillar lives on cabbage leaves and is parasitised by a small parasitic wasp (Cotesia glomerata) (figure 5.11) which injects (oviposts) its eggs into the caterpillar. They grow inside, feeding on the caterpillar, and emerge as adults. The eggs of this wasp are hyperparistised by another parasitic wasp (Lysibia nana) (figure 5.12) which injects its eggs into the eggs of Cotesia glomerata.
(Source: http://www.commanster.eu/commanster.html)
Figure 5.10 - Large cabbage white butterfly caterpillar. Poelman et al (2012) showed in laboratory experiments that Lysibia nana preferred plants that released chemical signals that they were under attack from caterpillars. These signals are meant to attract Cotesia glomerata to attack the caterpillar, but also tell the hyperparasite where their hosts are to be found.
43
(Source: Heinrich von Schubert et al (1886) "Naturgeschichte des Tierreichs"; in public domain)
Figure 5.11 - Drawing of Cotesia glomerata.
(Source: Poelman et al 2012)
Figure 5.12 - Drawing of Lysibia nana. The "usurpation hypothesis" (Brodeur and Vet 1994) proposes that the parasite will manipulate the defence mechanisms of the host to protect against the hyperparasite 37. For example, the large cabbage white butterfly remains alive well after parasitism and spins a thick layer of silk to protect the parasitoid cocoon from the hyperparasite. The Lysibia nana females can chew through the silk webs, but it takes a long time. So the silk web does not eliminate the threat of hyperparasitism as much as "decrease the foraging efficiency in the hyperparasitoids by extending their handling time per
37
This is an example of the host-parasite arms race (Greischar and Koskella 2007). 44
host brood. Ultimately, this temporal 'delay' may importantly allow parasitoid broods to escape hyperparasitism if the hyperparasitoids are disturbed by other factors such as wind, rain or other insects while they are attempting to parasitise host cocoons" (Harvey et al 2008 p706). Harvey et al (2008) tested how many broods of Cotesia glomerata were hyperparatised depending on the presence or absence of silk web spun by the host caterpillar. Female Lysibia nana were placed in an arena with a choice of Cotesia glomerata broods to hyperparasitise (eg: silk layer vs no silk layer). It was found that significantly less Lysibia nana adults emerged from broods of Cotesia glomerata covered by a silk layer. Tanaka and Ohsaki (2006) reported that the silk web produced by the parastised caterpillars was denser than that produced by unparasitised caterpillars. These researchers also found that the hyperparasite Trichomalopis apanteloctena (which also attacks Cotesia glomerata) was not deterred by the presence of a silk web. REFERENCES
Achenbach, A & Foitzik, S (2001) First evidence for slave rebellion: Enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus Evolution 63, 4, 1068-1075 Barnett, C (2012) An observation of interspecific kleptoparasitism of North Island robins (Petroica longipes) by hihi (Notiomystis cincta) Notornis 59, 178-179 Blackman, S (2013) Stranger but true: When a foe's foe's foe is no friend BBC Wildlife March, 96-97 Britton, N.F et al (2007) Exploitation of defence portfolios in exploiter-victim systems Bulletin of Mathematical Biology 69, 957-988 Brockmann, H.J & Barnard, C.J (1979) Kleptoparasitism in birds Animal Behaviour 27, 487-514 Brodeur, J & Vet, L.E.M (1994) Usurpation of host behaviour by a parasitic wasp Animal Behaviour 48, 187-212 Cooper, W.E & Prez-Mellado, V (2003) Kleptoparasitism in the Balearic lizard, Podarcis lilfordi Amphibia-Reptilia 24, 219-224 Dawkins, R & Krebs, J.R (1979) Arms race between and within species Proceedings of the Royal Society, Series B. Biological Sciences 205, 489511 Flower, T.P et al (2013) The ecological economics of kleptoparasitism: Pay-offs from self-foraging versus kleptoparasitism Journal of Animal Ecology 82, 245-255 Gorman, M.L et al (1998) High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyenas Nature 391, 479-481 Greischar, M.A & Koskella, B (2007) A synthesis of experimental work on parasite local adaptation Ecology Letters 10, 418-434 Grim, T (2011) Ejecting chick cheats: A changing paradigm? Frontiers
45
in Zoology
8, 14
Harvey, J.A et al (2008) Do parasitised caterpillars protect their parasitoids from hyperparasitoids? A test of the "usurpation hypothesis" Animal Behaviour 76, 701-708 Morand-Ferron, J et al (2007) Food stealing in birds: Brain or brawn Animal Behaviour 74, 1725-1734 Pamminger, T et al (2012) Geographic distribution of the anti-parasite trait "slave rebellion" Evolutionary Ecology 27, 1, 39-49 Poelman, E.H et al (2012) Hyperparasites use herbivore-induced plant volatiles to locate their parasitoid host PLoS Biology 10, 11, e1001435 (Freely available at http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001435?ima geURI=info:doi/10.1371/journal.pbio.1001435.g002) Riensche, D.L et al (2012) Kleptoparasitism by Forster's tern on California least tern Pacific Seabirds 39, 2, 55-56 Shealer, D.A & Spendelow, J.A (2002) Individual foraging strategies of kleptoparasitic roseate terns Waterbirds: The International Journal of Waterbird Biology 25, 436-441 Shealer, D.A et al (2004) The adaptive significance of stealing in a marine bird and its relationship to parental quality Behavioral Ecology 16, 2, 371-376 Smith, N (1968) The advantage of being parasitised Nature 694 Speakman, J.R (1998) The history and theory of the doubly labelled water technique American Journal of Clinical Nutrition 68, supplement, 932S-938S Tanaka, T & Ohsaki, N (2006) Behaviour manipulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L) to construct defensive webs against hyperparasitism Ecological Research 570-577 269, 690-
21,
Thomas, J.A et al (2013) Mimetic host shifts in an endangered social parasite of ants Proceedings of the Royal Society of London, Series B: Biological Series 280, 1751 Tokue, K & Unda, K (2010) Mangrove gerygones Gerygone laevigaster eject Little Bronze-cuckoo Chalcites minutillus hatchlings from parasitised nests Ibis 152, 835-839 Toms, M (2013) Is it unusual to see a gull attack a puffin? BBC Wildlife March, p91 Whiting, M.J & Greef, J.M (1997) Facultative frugivory in the Cape flat lizard, Platysaurus capensis (Sauria: Cordylidae) Copeia 811-818
46

Advantages and Disadvantages of Animal Behaviour No4

Uploaded by

Copyright:

Available Formats

You might also like

Advantages and Disadvantages of Animal Behaviour No4

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Advantages and Disadvantages of Animal Behaviour No4

Uploaded by

Copyright:

Available Formats

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.

1. SPERM COMPETITION Appendix 1A - Semelparity References

2. OBJECT PERMANENCE Apes Other animals Appendix 2A - Pseudo-replication References

3. RARE ENEMY EFFECT Tentacled snake Flush-pursuers References

5. TYPES OF PARASITISM Social parasitism Kleptoparasitism Hyperparasitism References

(Source: G-U Tolkiehn)

Figure 1.2 - Drawing of northern quoll.

Figure 1.3 - Drawing of agile Antechinus.

Figure 1.4 - Drawing of dibblers.

(Data from Barth and Call 2006 table 2 p244)

3. RARE ENEMY EFFECT

Figure 3.1 - Tentacled snake hunting posture and strategy.

Figure 3.2 - Strikes by newborns showing prediction of fish's future position.

(Source: Dominic Sherony)

4. ANIMAL NAVIGATION AND ORIENTATION USING POLARISED LIGHT

(Based on drawings at http://www.polarization.com/sky/sky.html)

(Source: Julio Reis)

(Source: Simon Speed; in public domain)

(Source: Per Harald Olsen)

(Source: Duncan Wright; in public domain)

Figure 5.3 - Great frigatebirds chasing booby with food.

times higher than matched "honest" (non-kleptoparasitic) roseate terns.

(Source: US Fish and Wildlife Service Northeast Region)

(Drawn with MapCreator 2.0)

(Source: In public domain)

(Drawn with MapCreator 2.0)

(Based on Speakman 1998 figure 2 p934S)

Figure 5.8 - Theoretical basis to DLW technique.

Figure 5.9 - Hyperparasite and parasite community on Brassica oleracea plants.

Figure 5.11 - Drawing of Cotesia glomerata.

(Source: Poelman et al 2012)

You might also like