advantages and disadvantages of animal behaviour no4

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.4

Kevin Brewer ISBN: 978-1-904542-70-4

Animal Behaviour: Advantages and Disadvantages No.4; Kevin Brewer; 2013 ISBN: 978-1-904542-70-4 2

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 s ource (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 thi s license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ or, send a letter to Creative Commons, 171 2nd Street, Suite 300, San Francisco, California, 9 4105, USA. 2. Details of the author are included so that the l evel of expertise of the writer can be assessed. This co mpares to documents which are not named and it is not poss ible 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 Engl and, 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 [email protected]


CONTENTS Page Number 1. SPERM COMPETITION 4 Appendix 1A - Semelparity 6 References 10 2. OBJECT PERMANENCE 12 Apes 13 Other animals 14 Appendix 2A - Pseudo-replication 16 References 16 3. RARE ENEMY EFFECT 18 Tentacled snake 18 Flush-pursuers 22 References 24 4. ANIMAL NAVIGATION AND ORIENTATION USING POLARISED LIGHT 25 Using polarised light 25 Twilight 27 Lunar polarisation 28 References 29 5. TYPES OF PARASITISM 30 Social parasitism 30 Kleptoparasitism 34 Hyperparasitism 42 References 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 fema les it is the production of eggs (ova). These costs lead t o a strategy where males adjust the number of sperm 2 transferred to females to optimise fertilisation su ccess, while females use choosiness to decide whose sperm can fertilise their eggs. The male situation is known as sperm competiti on 3 4 (or "strategic ejaculation"; Gage 1991), and the nu mber 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 i n ejaculations where competition is low and more sper m if the competition is high (sperm competition risk mod el). However, the sperm competition intensity model pred icts that the number of sperm will increase if there is one rival male, but decrease if there are more than tha t (Worthington et al 2013). Using meta-analyses, Kelly and Jennions (2011) concluded that, as a generalisation, males have lar ger 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

1 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.


relationship between female mating status (virgin o r already-mated) and number of sperm varied between s tudies 10. There was no significant difference between ejacu late size and female mating status in studies using dire ct measures of ejaculate size, while studies using ind irect measures found larger ejaculates transferred to vir gin females. The findings also varied with the species studied. Worthington et al (2013) investigated the sper m competition intensity model with domestic crickets (Acheta domesticus) (figure 1.1). Females store spe rm from multiple males in their spermatheca before usi ng it for fertilisation, and an individual male will bene fit by giving the female proportionally more sperm than th is rivals. Sexually mature virgin males were randomly all ocated to one of three conditions for the experiment - no rival males, one rival, or two rivals in clear cages near by for five days prior to mating. Each male was given the opportunity to mate, and the number of sperm produc ed were measured. Male crickets transfer their sperm i n a spermatophore which is produced prior to meeting a female, and is attached to her. The researchers rem oved 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 sper m)

10 N = 40 species.


were found between the three conditions. This is co ntrary to Gage and Barnard (1996) who found that the crick ets produced more sperm in the presence of other males. This experiment allowed the males to physically interact , whereas Worthington et al (2013) only allowed visua l, acoustic and olfactory cues without physical contac t. The latter admitted: "Perhaps male A. domesticus determ ine sperm competition risk through physical contact wit h conspecific males during spermatophore formation pr ior to meeting" (Worthington et al 2013 p59). But Worthington et al (2013) found that smalle r males produced significantly more viable sperm than larger males. Females prefer larger males and the m ating opportunities for smaller males in the wild are les s. "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 inve st in high-quality ejaculate to increase fertilisation su ccess in current reproduction and thus maximize their fit ness" (Worthington et al 2013 p59). APPENDIX 1A - SEMELPARITY Semelparity (suicidal reproduction) is where t he 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 ex ists for females where maternal care is not required aft er 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 t hat 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

11 The opposite is iteroparity (living for more than one breeding season) (Tallamy and Brown 1999). 12 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).


food peaks, and male survival between breeding seas ons is low. Thus, one breeding season and death as post-reproductive 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 nor thern 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 bet ween 31st May and 4th July at a mean age of 11 months ol d. Generally, of males trapped in June, the majority h ad lice infestation (85%) (a sign of a poor immune sys tem) 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 o f fur as well. However, the researchers did not find incr eased corticosteroids or gastrointestinal ulceration. Oak wood et al (2001) concluded: "These results suggest that die off may be the result of an unexplained phylogeneti c predisposition in these species towards post-reprod uctive senescence" (p410).

(Source: John Gould (1863) "Mammals of Australia vo lume 1"; in public domain)

Figure 1.2 - Drawing of northern quoll.

15 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).


iii) The "accumulation of deleterious mutation s 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 exhau sting) 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. Ba sed on data from a well-studied field population of agile antechinus (Antechinus agilis) (figure 1.3) in sout hern Australia, it was estimated to be between 6-14. For example, if female survival to care for offspring w as only 40%, then a male would have to mate with aroun d 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 th ree hours. Thus, "one can imagine that mating effort wi ll consume large amounts of the males' energy" (Kraaij eveld et al 2003). Mills and Bencini (2000) reported that male di bblers (Parantechinus apicalis) (figure 1.4) were semelpar ous 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 survive d to the next breeding season, and consequently so did m ore offspring) 17.

16 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 Darwin’s 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 non-semelparous species had female survival nearer to 70%.


(Source: John Gould (1863) "Mammals of Australia vo lume 1"; in public domain) Figure 1.3 - Drawing of agile Antechinus.

(Source: John Gould (1863) "Mammals of Australia vo lume 1"; in public domain) Figure 1.4 - Drawing of dibblers.


v) Altruistic paternal suicide to allow more f ood for offspring (eg: Diamond 1982), or avoid survivin g 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 pref er young males or selection for male endurance. vii) Extreme sperm competition (eg: Dickman 19 93) - Insectivorous marsupials with low post-mating survi val have longer copulation durations that those with hi gher survival rates (mean: 9.4 vs 3.7 hours; Fisher et a l 2013). Longer duration blocks rival males from havi ng the opportunity to displace or dilute sperm. These spec ies also have larger testes in relation to body size (F isher et al 2013). REFERENCES Braithwaite, R.W & Lee, A.K (1979) A mammali an 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 an d 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 Fr ontiers in Zoology 10, 66 Fisher, D.O et al (2013) Sperm competition d rives 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 cricket s 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 Anima l Behaviour 42, 1036-1037 Humphries, S & Stevens, D.J (2001) Reproduct ive biology. Out with a bang Nature 410, 758-759 Kelly, C.D & Jennions, M.D (2011) Sexual sel ection and sperm quantity: Meta-analyses of strategic ejaculation Biological R eviews 86, 4, 863-884 Kraaijeveld, K et al (2003) Does female mort ality 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 die-off in island populations of dibblers, Parantechinu s apicalis Australian Journal of Zoology 48, 501-510 Moatt, J.P et al (2013) Exposure to sperm co mpetition risk improves survival of virgin males Biology Letters 9, 20121188


Oakwood, M.A et al (2001) Semelparity in a l arge 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 trad e-off between sperm quality and immunity in the field cricket, Teleogry llus 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 cricke ts strategically adjust the number and viability of their sperm under sperm competition? Animal Behaviour 86, 55-60


2. OBJECT PERMANENCE When moving prey momentarily disappears out of sight during a chase, say, predators need the cognitive a bility 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 disap peared from view" (Fiset and Plourde 2012). For humans object permanence develops in the f irst 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-n ot-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 locati on A (stage 4 of object permanence). The last stage of o bject permanence is to understand invisible displacement 18. This is where a moving object disappears out of sig ht, and requires the ability to track the continued mov ement. 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, i s allowed to search for the object. This tests the ba sic concept of object permanence that an object still e xists when out of sight, and memory. In a more advanced version (the inhibition tes t), objects will be placed under two of the three cups (eg: not the middle one). Call (2001) found that orangut ans, chimpanzees and young children usually searched und er the left or right hand cup first. "After successful ret rieval of the first object, they proceeded by choosing the middle container, which they had just seen a few se conds ago to be empty. Evidently, subjects have problems skipping the middle container. Call (2001) suggeste d that this search error is most likely to be explained by an inhibition problem rather than a memory deficit" (B arth and Call 2006 p239). Invisible displacement is tested with three cu ps, say, on a rotated platform. The viewer sees the obj ect 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 ab le to recover the hidden food significantly more often th an chance (Beran and Minahan 2000). Beran et al (2005) placed food rewards under two of five cups, and

18 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).


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 on ce or twice (single or double transpositions), all in fro nt of the viewer. Studies have found that bonobos, chimpa nzees, and orangutans can find the object (as well as Afri can grey parrots), but not cats and dogs nor children y ounger than three years old (Barth and Call 2006). APES Barth and Call (2006) compared the object perm anence 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 perf ormed thirty trials involving six different tasks based o n 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 c hosen 85% of the time, which is significantly above chanc e (33%), and the apes were significantly better in th e control than delay version. Task 2 was an inhibition test where food was h idden in two of three cups. The researchers were interest ed in whether the apes searched under the empty cup (usua lly 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, fo r 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 corr ect cup was chosen 49% of the time, which is significan tly 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 th e apes watching the experimenter place the food under one cup and then move it to another cup. The correct cup wa s chosen 72% of the time (p<0.001). The second experiment used the same tasks with 24 children (aged 2½ years old) in Leipzig. The childr en 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 f rom zoos in Hungary could pass single visible displacem ent (SVD) and single invisible displacement (SID) tests , but not the double invisible displacement (DID) one. Th e SVD task was seeing an object placed in one of three wo oden boxes, while the SID task involved the experimenter hiding the object in their hand before placing it i n one of the boxes. With the DID task, the experimenter p laces the hand hiding the object in one box and then move s the hand and object to another box in the view of the g ibbon. OTHER ANIMALS Fiset and Plourde (2012) compared the object permanence abilities of domestic dogs (Canis lupus familiaris) and gray wolves (Canis lupus) finding n o difference between the two species. In the first experiment with nineteen dogs and five wolves, invi sible displacement was tested. Three black buckets were p laced next to each other, and a piece of food was dropped into one bucket in front of the animal, then one of thre e things happened, depending on the condition: � Substitution transposition condition (ST) - The buc ket

containing the food was moved a short distance. � Double transposition condition (DT) - The bucket wi th

the food and one empty bucket were moved.


� Control of movement condition (CM) - The two empty buckets were moved.

Success was measured by finding the food on th e 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 t he CM condition. There were no significant differences be tween 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 ha ve seen an object disappear and do not plainly underst and invisible displacement of object. Experiment 1 also extends this later conclusion to the gray wolf" (p1 20). The second experiment tested the A-not-B error with nine gray wolves and 22 dogs (of which about half t he animals had been in Experiment 1). Each animal perf ormed six trials in each of three conditions: � A-not-B test - A piece of food is seen by the anima l to

be hidden behind one of three screens (screen A), a nd 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 f ood

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 t hen immediately moved behind another screen.

Both species did not commit the A-not-B error, and retrieved the food from behind screen B. The animal s were successful in most trials in the SVD condition, and slightly less so in the DVD condition. This experim ent established that the animals had stage 5 object permanence. Jaakkola et al (2010) confirmed bottlenose dol phins' (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 b etter


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 signif icant. The third test of invisible displacement involved t he object placed in a bucket and the bucket being move d. The correct bucket was chosen in 40% of trials, which i s not significantly different to chance. Scoring of the c hoice of bucket by the dolphin was done by an observer bl ind to where the object was hidden 19. APPENDIX 2A - PSEUDO-REPLICATION Researchers want to be able to generalise thei r 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 indiv idual in the sample and pooling them. This is an artifici ally inflated sample, and the data points are not indepe ndent but are classed as so, "which falsely raises statis tical power and increases the chances of making a type I error (a false positive: rejecting the null hypothesis wh en it is true)" (Waller et al 2013 p483). It is called "p seudo-replication" (Hurlbert 1984) or the "pooling fallac y" (Machlis et al 1985) 20. Waller et al (2013) reported that over one-thi rd of primate communication studies (published between 19 60-2008) that used inferential statistics had at least one case of pseudo-replication data. For example, in a playback experiment, the researchers play a particu lar call and measure the responses. By not using only o ne response per individual animal, pseudo-replication occurs. Waller et al (2013) found that observation studies were the method most likely to have such da ta. REFERENCES Barth, J & Call, J (2006) Tracking the displ acement of objects: A series of tasks with great apes (Pan troglodytes, P an paniscus, Gorilla gorilla, and Pongo pygmaeus) and young children (Ho mo 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 troglod ytes) International Journal of Comparative Psychology 13, 1-15

19 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).


Beran, M.J et al (2005) Spatial memory and m onitoring of hidden items through spatial displacements by chimpanzees (Pan t roglodytes) Journal of Comparative Psychology 119, 14-22 Call, J (2001) Object permanence in oranguta ns (Pongo pygmaeus), chimpanzees (Pan troglodytes), and children (Homo s apiens) Journal of Comparative Psychology 115, 159-171 Fedor, A et al (2008) Object permanence test s on gibbons (Hylobatidae) Journal of Comparative Psychology 122, 4, 403-417 Fiset, S & Plourde, V (2012) Object permanen ce in domestic dogs (Canis lupus familiaris) and gray wolves (Canis lupus) Jou rnal of Comparative Psychology 127, 2, 115-127 Hurlbert, S.H (1984) Pseudoreplication and t he design of ecological experiments Ecological Monographs 54, 187-211 Jaakkola, K et al (2010) What do dolphins (T ursiops 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 Represent ational Mind Cambridge, MA: MIT Press Piaget, J (1937) The Construction of Reality in the Child (in French) Neuchatel: Delachaux & Niestle Suddendorf, T & Whiten, A (2001) Mental evol ution 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


3. RARE ENEMY EFFECT The "evolutionary arms race" (Dawkins and Kreb s 1979) is an example of co-evolution where prey evol ve a new strategy to survive predation, and then predato rs evolve a counter-measure, and so on. But the "rare enemy effect" (Dawkins 1983) describes where a predator h as 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) capt uring fish. Fish have evolved an escape response when the y detect sounds and/or motion in the water of a preda tor called the C-start. The escape response begins with a C-shaped bend in the fish's body. When there is a sou nd to the left ear, say, this stimulates muscles on the r ight side of the body, while inhibiting those on the lef t side, and the fish escapes to the right (Catania 20 11). This strategy makes sense - turn away from the direction of the predator. But Catania (2009) obser ved that fish turned into the mouth of the tentacled sn ake. The snake has evolved a hunting strategy that takes advantage of the normal escape response. The tentacled snake hangs from vegetation in t he water mimicking a stick in a J-shape with its upper body and head. As the fish (eg: minnows; Gambusia affini s) 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 ax is of the snake's head) (figure 3.1) (Catania 2011) 21. In 78% of 30 experimental trials the fish turned towards t he 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 righ t angle to the snake's head, the snake strikes at whe re the fish will be after the escape response. Catania (20 09) reported a strike success rate of 48% (19 of 40 tri als), but only 12% if the fish did not produce the escape response.

21 The C-start takes 5-6 ms, and the strike 15-20 ms (Catania 2009). 22 "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).


(A. When fish approach the concave area between hea d and body, the snake feints with its body before striking, generating a water distur bance 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. Adu lt 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.


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 strik e without contact) (figure 3.3). There were 100 trial s with ten snakes (ie: ten trials each).

(A–C show three different strikes at fish. The uppe r 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 str ikes 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.

23 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".


(A. Top view (camera view) of the apparatus. An upp er 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 uppe r 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 emph asised that the predictive nature of the strikes... is qualitatively different from predictions of prey (o r 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 informati on about its initial trajectory. Extending this analog y to tentacled snakes – it would be as if the batter cou ld estimate the position of the ball in time and space without ever seeing the pitch. Moreover,... they ca n do this without ever seeing any pitches". "Handling time" for predators is the time take n to capture the prey and eat. Catania (2010) compared t he handling times (from strike onset to fish disappear ed in snake's mouth) on three types of attack - head of f ish first and swallow, tail of fish first and swallow, and attack tail but swallowed head first. The first att ack strategy was quickest with a mean time of 15 second s. The tail first and swallow took an average of 63 second s, and the other strategy 87 seconds (figure 3.4). Tentacled snakes are vulnerable to predation themselves during the handling time, and Smith et a l (2002) noted a tail-wiggling behaviour during this time. This seems to be a way to distract the snake's pred ators and focus an attack at that end rather than at the head.


("Moved to head" refers to fish that were grasped t ail-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) ar e another example of the rare enemy effect. These are birds that cause their landed insect prey to produce a fl ight response and chase the insect in the air rather tha n attack the landed insect. The flight response is th e normally adaptive strategy to the appearance of a predator. "Thus, the flush-pursuers are good exampl es of predators exploiting insect anti-predatory behaviou r" (Jablonski 1999). Examples of flush-pursuers are Myioborus speci es (whitestart), Setophaga ruticilla (American redstar t), and most Rhipidura (fantails), and they forage on t he 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 fo und in


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 wh ite patches which help flush the insect as the bird hop s around in trees, on the ground or on rocky walls.

(Source: Dominic Sherony)

Figure 3.5 - Painted redstart. In field experiments in Arizona, Jablonski (19 99) covered the white patches with black dye of seven experimental birds, and they were significantly poo rer at flushing insects than before dye and compared to se ven control birds (unaltered). The experimental birds d ropped 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 vide o-recorded 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 term s 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 preda tors (eg: 15-30% of a guild 25; Jablonski 1999), and there are stronger selection pressures on insects to avoid bi rds that attack landed prey and non-avian predators. "H ence, foraging based on exploitation of insect escape res ponses might have evolved due to the rarity of the flush-pursuing predators" (Jablonski 1999). REFERENCES Catania, K.C (2009) Tentacled snakes turn C- starts to their advantage and predict future prey behaviour Proceedings of th e 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 Scie ntific American April, 64-67 Dawkins, R (1983) The Extended Phenotype Oxford: Oxford University Press Dawkins, R & Krebs, J.R (1979) Arms race bet ween and within species Proceedings of the Royal Society, Series B. Biologi cal Sciences 205,489-511 Jablonski, P.G (1999) A rare predator exploi ts prey escape behaviour: The role of tail-fanning and plumage contrast in fo raging of the painted redstart (Myioborus pictus) Behavioral Ecology 10, 1, 7-14 Jablonski, P.G (2001) Sensory exploitation o f prey: Manipulation of the initial direction of prey escapes by a conspicu ous "rare enemy" Proceedings of the Royal Society, Series B. Biologi cal Sciences 268, 1017-1022 Remsen, J.V & Robinson, S.K (1990) A classif ication 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

25 A "predator guild" is a term used to cover different species of predators that are hunting the same prey in the same environment.


4. ANIMAL NAVIGATION AND ORIENTATION USING POLARISED LIGHT Visual cues in the sky are the basis of naviga tion and orientation for many species. These cues includ e the position of sun, moon or other celestial bodies, an d polarised light. This is the scattering of light fr om air molecules, water, and dust in the atmosphere, for e xample 26. The polarisation pattern changes during the day a s the sun apparently moves across the sky, and the time o f 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 tw ilight 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 a t 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 ver y small amphipod crustaceans live on the seashore and need cues to help them to return to the damp area of san d where they live. With the movement of tides, there is a risk of dehydration if they are dry for too long, s o 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 diffe rent

26 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.


(Source: Julio Reis)

Figure 4.2 - A sandhopper. options. The light from each end of the tube was va ried. For example, polarised white light versus non-polar ised white light. In the case of artificial light choice s, 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 directio n 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 mov ed 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 (Agele na labyrinthica), and the blue-grey ground spider (Dra ssodes cupreus) (Dacke et al 2001).

29 Ugolini et al (2012) tested the role of skylight gradient of luminance by creating a dome in which to place the sandhoppers.


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 are na with an optical motion sensor. So when the spider m oved 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 e t al (2001) observed that the "luxury of having eight ey es has allowed lycosid and gnaphosid spiders to devote eye s to the detection of polarised light" (p2488). Hanke et al (2012) found that two captive trai ned harbour seals (Phoca vitulina) did not use polarise d 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 s hapes were presented "whose contrast was purely defined i n terms of polarisation" (ie: lacked luminance contra st), the seals did not respond. TWILIGHT During twilight the light of the whole sky is polarised in one direction. At this time, the zenit h of the sky has the highest degree of polarisation of t he day, which stretches in a band from south to north across the sky. "The remainder of the skylight is polarise d in a parallel direction with falling degrees of polarisa tion towards the sun and the anti-sun. On nights with a full moon, a similar pattern of polarised light will als o form around the source of light" (Dacke et al 2003 p1535 ). Under moonless twilight skies, Dacke et al (20 03) set up a filter that made the southerly-northerly oriented polarised light pattern of evening skyligh t 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 fil ter. "The recorded turn of the beetles under the filter thus shows that polarised light could well be the primar y cue used by the beetle to maintain its bearing" (Dacke et al 2003 p1540). Dacke et al (2003) had established that the be etles follow a path in one direction by placing an obstac le in the way. Once the beetle has navigated around the obstacle, it follows the path of the original direc tion. But this is orientation (or leaving) (the move ment in a particular direction), which is different to navigation (homing) (the movement towards a particu lar point). "An obvious difference between homing and l eaving is, of course, that the leaving beetle has a set pl ace to start, while the homing animal has a determined pla ce to


stop" (Dacke et al 2003 p1539), but moving in a str aight line is the best solution for both (figure 4.3).

Figure 4.3 - Difference between orientation and hom ing. LUNAR POLARISATION Dacke et al (2004) reported that the African d ung beetle (Scarabaeus zambesianus) uses the polarisati on pattern of the moonlight sky to navigate. The beetl es collect dung from mammals, which they mould into a ball and roll away from competitors to bury. In the laboratory experiments, a beetle is pla ced in a large arena with its ball of dung. Three lamps ar e placed at different points and illuminated one at a time to produce the "artificial moon". One light would b e on, and as the beetle moved towards it, it would be tur ned 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 t he 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 fi eld experiments in South Africa when the real moon was hidden from view, an artificial moon at an angle of 180° w as introduced. Thirteen of fifteen beetles did not cha nge their direction of travel in this situation. Each a nimal stopped rolling its dung, " then climbed on top of its ball and performed an orientation dance, rotating a bout its vertical axis, presumably reading the polarisat ion 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 o f S. zambesianus. Instead, the primary cue for orientati on 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 clou d 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 b eetle with more precise compass information than will an individual pixel of the sky" (p364). REFERENCES Dacke, M et al (2001) Polarised light detect ion in spiders Journal of Experimental Biology 204, 2481-2490 Dacke, M et al (2003) Twilight orientation t o polarised light in the crepuscular dung beetle Scarabaeus zambesianus Jour nal 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 Serie s 271, 361-365 Hanke, F.D et al (2012) Are harbour seals (P hoca vitulina) able to perceive and use polarised light? Journal of Compar ative Physiology A 199, 6, 509-519 Ugolini, A et al (2012) The skylight gradien t of luminance helps sandhoppers in sun and moon identification Journal of Experimental Biology 215, 2814-2819 Ugolini, A et al (2013) Do sandhoppers use t he skylight polarisation as a compass cue? Animal Behaviour 86, 427-436


5. TYPES OF PARASITISM "Parasitism is the most common life style on e arth and virtually all organisms are affected by it" (Pamminger et al 2012 p39). It is the ability of on e organism (parasite) to take advantage of another or ganism (host). There is no benefit to the latter, and it i s to their complete disadvantage. Thus the parasite is a ble to manipulate the host. SOCIAL PARASITISM Social or brood parasitism is where the host r aises 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 mi mic the grubs of Myrmica ants 30. The ants carry the larvae back to the colony and feed it. The larvae live the re for 11-23 months and obtained all the nutrition needed to develop (Thomas et al 2013). The social parasitism is very specific for thi s butterfly. Thomas et al (2013) swapped cuckoo butte rfly larvae from Spain and Poland with the different Myr mica 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 h osts have evolved defence strategies against the exploit ers. For example, the reed warbler (Acrocephalus scirpac eus) has evolved the ability to recognise the egg of its social parasite, the common (Eurasian) cuckoo (Cucu lus canorus), which is different to its own, and remove it from their nest. Shortly after egg-laying the cucko o visits a briefly unattended host's nest, removes on e of the eggs, and lays her own in its place. The cuckoo then flies away until the host's egg to eat. This proces s 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, c uckoos eggs subsequently evolved to mimic the host's eggs in size, colour, and patterning 32 (figure 5.1) 33.

30 Myrmica schencki and Myrmica sabuleti. 31 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).


(Source: Simon Speed; in public domain)

Figure 5.1 - Four clutches of reed warbler eggs wit h cuckoo egg present. The cuckoo chick often hatches first and force s the other eggs out of the nest. The hosts do not stop t his happening. The next step in this "evolutionary arms race" (Dawkins and Krebs 1979) would be for the reed warb ler to recognise the cuckoo chick which is physically diff erent 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 t he resources available for employing the other" (Britt on et al 2007). The trade-off is in relation to getting t he


(Source: Per Harald Olsen)

Figure 5.2 - Reed warbler feeding cuckoo chick. strategy wrong (ie: killing own offspring) versus t he risk of being parasitised. Chick ejection requires a stronger selection pressure to evolve than egg ejection. "Obviously, a host correctly rejecting parasite eggs ('rare enemi es') will have no chance to face parasite chicks (which, as a consequence of host own behaviour, become even 'rar er enemies'). Paradoxically, egg-rejecting hosts thems elves eliminate selection pressure that would enable them to evolve an ability to discriminate parasite chicks.. . Thus, successful previous lines of defence (includi ng


nest defence...) decrease positive selection pressu re on later lines of defence" (Grim 2011). The opposite in defence strategies is seen in the superb fairy-wren (Malurus cyaneus) (host), which r ejects the chick of the Horsfield's bronze-cuckoo (Chrysoc occyx basalis) but not the egg. Social parasitism rates o f 16-32% have been reported in Australia (Britton et al 2007). Physically removing the invading chick is rare ly seen - another example is the Mangrove gerygones (Gerygone laevigaster) ejecting Little Bronze-cucko o (Chalcites minutillus) hatchlings from the nest (To kue and Unda 2010) 34. This study showed that "chick discrimination may take place (a) almost immediatel y after the parasite hatches, and (b) without rejecti on errors (though in small sample sizes), thus (c) rej ecting host individuals saved their whole current parental investment before the parasite chick had a chance t o destroy it" (Grim 2011). Anti-social parasite strategies by birds also include the host deserting the nest, feeding the pa rasite 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 mob bing of parasites as soon as they are spotted in the vic inity by the host birds (Pamminger et al 2012). Slave-making ants (eg: Protomognathus american us) (social parasites) depend on ant workers of other s pecies (hosts) (eg: Temnothorax longispinosus) to perform routine tasks in the colony. Slave-making ants atta ck other colonies, and steal the host brood which are developed as workers. The hosts have developed defence strategies pr ior to enslavement including aggression or escape, and a p ost-enslavement defence called "slave rebellion" (Achen bach and Foitzik 2009). Enslaved Temnothorax longispinos us ants kill a large proportion of the pupae of the sl ave-making ants. This is an indirect benefit for the individual ant, but is beneficial to their kin in o ther 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 state s in the USA. Social parasitism may actually be part of a mutualistic relationship. For example, brood parasi tism by cowbirds is tolerated by the hosts because cowbi rd chicks remove botfly larvae from the host chicks (S mith

34 Grim (2011) explored factors that account for the rare number of documented cases rather than necessarily the rarity of the behaviour.


1968). Britton et al (2007) pointed out that this i dea has been questioned. KLEPTOPARASITISM Kleptoparasitism (or "aerial piracy" by birds) is "the harassment of one bird species by another in o rder to force the victim to give up its food" (Riensche et al 2012) (figure 5.3), or stealing prey from an indivi dual returning to the nest after successful foraging (To ms 2013) 35. Though birds have been most studied, it is reported by fish, mammals, reptiles among others (F lower et al 2013).

(Source: Duncan Wright; in public domain)

Figure 5.3 - Great frigatebirds chasing booby with food.

35 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 Pérez-Mellado (2003) called it "interference competition".


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 ar e scarce, or when it enables a species to gain new fo od access. Generally, it is viewed as a high-risk, hig h pay-off strategy (Flower et al 2013). Cooper and Pérez-Mellado (2003) gave Balearic lizards (Podarcis lilfordi) pieces of fruit that we re too large to swallow immediate, and thus required longe r handling times. Food stealing occurred in just over half of such situations. Food owners responded by runnin g away with the food. Other counter-measures to kleptoparasitism inc lude increased vigilance during food handling, rapid swallowing, or foraging alone (Cooper and Pérez-Mel lado 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 observati on of adult Forster's tern (Sterna forsteri) harassing ad ult California least terns (Sternula antillarum browni) returning to their young with fish. The attackers f lew towards, chased and attempted to steal fish from th e bills of the victims. When the latter is forced to drop their fish, the Forster's tern then recovers it. Th e 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 b e occasional or opportunistic (eg: spotted hyenas - 2 0% of carcasses in one study) or the main tactic (eg: spi der, Curimagua bayano) (Flower et al 2013). Shealer and Spendelow (2002) found that roseat e terns (Sterna dougallii) (figure 5.4) benefit from kleptoparasitism over self-foraging (ie: hunting fo r own food) when at the breeding colony, and these birds have greater reproductive success than non-kleptoparasit e members of the same species. The average prey deliv ery to the nest of ten kleptoparasitic individuals was 2-1 3

36 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).


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

(Source: US Fish and Wildlife Service Northeast Reg ion)

Figure 5.4 - Roseate tern. Shealer et al (2004) reported data showing tha t chicks of kleptoparasitic roseate terns had greater survival and superior growth than chicks of "honest " parents. Ten kleptoparasitic individuals at a colon y site on Falkner Island, Connecticut, USA (figure 5.5), w ere compared to non-kleptoparasitic individuals and the averages for the whole colony for the period 1990-9 9. Roseate terns usually lay two eggs, and the fi rst to hatch is designated as the "A-chick", and the last to hatch as the "B-chick". Measures of growth were tak en at three days, around thirteen days, and about 28 days after hatching. Both chicks of a kleptoparasite parent ha d superior growth to chicks of "honest" parents and t he colony average, but the difference was larger for B -chicks. Survival was measured by the chick fledging (ie: leaving the nest), and this was significantly highe r for kleptoparasitism-fed chicks. This difference can be presented as 45% more fledglings per kleptoparasite individual. Overall, kleptoparasitism was most bene ficial for survival of B-chicks.


(Drawn with MapCreator 2.0)

Figure 5.5 - Position of Falkner Island. Only a small number of roseate terns are habit ual 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 fa ct that the pool of kleptoparasites comprised the same individuals year after year... suggests that kleptoparasitic behaviour becomes fixed at some poi nt in life... [but] some mechanism (eg: high cost or phen otypic 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 Kala hari 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. T heir kleptoparasitism includes following other species ( mostly other birds, but also meerkats, for example) and ca tching prey disturbed, or by physical attack on other spec ies 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 strat egies - ie: is it a choice between kleptoparasitism and s elf-foraging 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 involve s potential physical contests and energy expended in chasing prey-owner. These questions were answered by 292 focal observations of twenty-five individual birds in Mar ch-August 2008 in xeric savanna (semi-arid harsh grass land) on the edge of the Kalahari Desert, Republic of Sou th Africa (figure 5.7). The birds were observed by binoculars from 20-30 m away, though they were habi tuated to human presence nearby. Focal observation involve s following one individual for a certain period of ti me. Each bird was observed for between 10-47 hours. Wit h a hand-held computer, the observer recorded the time engaged in each foraging behaviour, whether the for aging was successful, and the size and type of prey. The size of prey caught were categorised on a four-


point scale relative to the size of the drongo's bi ll length (eg: "tiny" = <¼ 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 s pent following other species, half of that involved self -foraging (eg: catching disturbed prey). When follow ing other species, the drongos perched lower to the gro und and moved less frequently than when self-foraging. Thus, following other species was incompatible with effec tive self-foraging (answer to researchers' question 1 ab ove). Kleptoparasitism was more common in the mornin g 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 lar ger and terrestrial (eg: lizards) compared to caught al one. Thus, kleptoparasitism exploited a novel foraging n iche, particularly prey that required digging up (eg: scorpions) (answer to question 3 above).


Flower et al (2013) noted that drongos have la rge 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 mutual ly exclusive (Morand-Ferrin et al 2007): i) "Brawn" hypothesis - Kleptoparasitism as "a form of aggressive food competition where the thieves ma y 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 b irds over smaller ones. ii) "Brain" hypothesis - Kleptoparasitism evol ved among birds who have the skill to use it - eg: abil ity to predict the behaviour of others. "Cognitive abiliti es allowing the integration and use of more informatio n in decision-making might thus increase the probability of kleptoparasitic success" (Morand-Ferron et al 2007) . iii) "Vertebrate prey" hypothesis - Kleptopara sites tend to go for vertebrate prey, which contains more energetic value, but has longer handling time for t he host. iv) "Group-foraging" hypothesis - Kleptoparasi tism is more common in crowded environments where food i s scarce and the opportunities for stealing are avail able. v) "Habitat openness" hypothesis - Open habita ts (eg: grassland) offer better opportunities to detec t potential victims than closed habitats (eg: forest) . Morand-Ferron et al (2007) analysed 856 report ed cases of interspecies kleptoparasitism by 197 speci es 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 u sing kleptoparasitism was linked to larger brain relativ e to body, open habitat, and vertebrate prey. Host Kleptoparasitism has costs for the host in ene rgy and time spent acquiring food that is stolen, time and energy in avoiding kleptoparasites, and less food f or


young. Gorman et al (1998) calculated the cost to the African wild dog (Lycaon pictus) of kleptoparasitis m 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 th e energy balance, and a loss of over one-third would require non-stop hunting (ie: 24 hours per day). Da ily energy expenditure (DEE) was calculated by using th e 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: aft er 48 hours), it is possible to establish the amount of t he isotopes in the blood and calculate DEE via estimat ing carbon dioxide production. The principle is that en ergy expended involves breathing in oxygen which produce s 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 techniq ue is "that oxygen turnover in a body is dominated by the flow of water through the body as well as inspired oxyge n and expired carbon dioxide. The turnover of body hydrog en, however, is dominated only by the flow of water thr ough the body. Consequently, the difference between the turnovers of oxygen and hydrogen provides a measure of the excess efflux of oxygen that is equivalent t o the production of carbon dioxide" (Speakman 1998 p934S) . This is done by isotopes of both oxygen and hydrogen bei ng injected into the body. A measure of carbon dioxide production (and energy expenditure) can be made fro m the difference in the isotopes of oxygen and hydrogen b etween injection (time 1) and current measure (time 2) (fi gure 5.8).

(Based on Speakman 1998 figure 2 p934S)

Figure 5.8 - Theoretical basis to DLW technique.


The main advantage of the DLW technique is tha t 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 o ther parasites. For example, the false king crab (Paralo mis granulosa) is parasitised by a barnacle (Briarosacc us 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, whi ch 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 o n Brassica oleracea plants.


One well studied example of hyperparasitism is the large cabbage white butterfly (Pieris brassicae) (f igure 5.10). Its caterpillar lives on cabbage leaves and is parasitised by a small parasitic wasp (Cotesia glom erata) (figure 5.11) which injects (oviposts) its eggs int o the caterpillar. They grow inside, feeding on the caterpillar, and emerge as adults. The eggs of this wasp are hyperparistised by another parasitic wasp (Lysi bia 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 caterpi llar. Poelman et al (2012) showed in laboratory experiments that Lysibia nana preferred plants that released chemical signals that they were under atta ck from caterpillars. These signals are meant to attra ct Cotesia glomerata to attack the caterpillar, but al so tell the hyperparasite where their hosts are to be found.


(Source: Heinrich von Schubert et al (1886) "Naturg eschichte 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 1 994) proposes that the parasite will manipulate the defe nce mechanisms of the host to protect against the hyperparasite 37. For example, the large cabbage white butterfly remains alive well after parasitism and s pins a thick layer of silk to protect the parasitoid cocoo n from the hyperparasite. The Lysibia nana females can che w through the silk webs, but it takes a long time. So the silk web does not eliminate the threat of hyperpara sitism as much as "decrease the foraging efficiency in the hyperparasitoids by extending their handling time p er

37 This is an example of the host-parasite arms race (Greischar and Koskella 2007).


host brood. Ultimately, this temporal 'delay' may importantly allow parasitoid broods to escape hyperparasitism if the hyperparasitoids are disturb ed by other factors such as wind, rain or other insects w hile they are attempting to parasitise host cocoons" (Ha rvey 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 e merged from broods of Cotesia glomerata covered by a silk layer. Tanaka and Ohsaki (2006) reported that the sil k 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 Cot esia glomerata) was not deterred by the presence of a si lk web. REFERENCES Achenbach, A & Foitzik, S (2001) First evide nce 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 interspe cific kleptoparasitism of North Island robins (Petroica longipes) by hihi (No tiomystis 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 de fence portfolios in exploiter-victim systems Bulletin of Mathematical B iology 69, 957-988 Brockmann, H.J & Barnard, C.J (1979) Kleptop arasitism 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 & Pérez-Mellado, V (2003) Klepto parasitism in the Balearic lizard, Podarcis lilfordi Amphibia-Reptilia 24, 219-224 Dawkins, R & Krebs, J.R (1979) Arms race bet ween and within species Proceedings of the Royal Society, Series B. Biologi cal Sciences 205, 489-511 Flower, T.P et al (2013) The ecological econ omics 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 synthe sis of experimental work on parasite local adaptation Ecology Letters 10, 418-434 Grim, T (2011) Ejecting chick cheats: A chan ging paradigm? Frontiers


in Zoology 8, 14 Harvey, J.A et al (2008) Do parasitised cate rpillars protect their parasitoids from hyperparasitoids? A test of the "u surpation 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 distrib ution 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 Biol ogy 10, 11, e1001435 (Freely available at http://www.plosbiology.org/article/info:doi/10.1371 /journal.pbio.1001435?imageURI=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) Individ ual foraging strategies of kleptoparasitic roseate terns Waterbirds: The Inter national Journal of Waterbird Biology 25, 436-441 Shealer, D.A et al (2004) The adaptive signi ficance of stealing in a marine bird and its relationship to parental qualit y Behavioral Ecology 16, 2, 371-376 Smith, N (1968) The advantage of being paras itised Nature 269, 690-694 Speakman, J.R (1998) The history and theory of the doubly labelled water technique American Journal of Clinical Nutrit ion 68, supplement, 932S-938S Tanaka, T & Ohsaki, N (2006) Behaviour manip ulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L) to construct defensive webs against hyperparasitism Ec ological Research 21, 570-577 Thomas, J.A et al (2013) Mimetic host shifts in an endangered social parasite of ants Proceedings of the Royal Society o f London, Series B: Biological Series 280, 1751 Tokue, K & Unda, K (2010) Mangrove gerygones Gerygone laevigaster eject Little Bronze-cuckoo Chalcites minutillus hat chlings from parasitised nests Ibis 152, 835-839 Toms, M (2013) Is it unusual to see a gull a ttack a puffin? BBC Wildlife March, p91 Whiting, M.J & Greef, J.M (1997) Facultative frugivory in the Cape flat lizard, Platysaurus capensis (Sauria: Cordylid ae) Copeia 811-818

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