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Kevin Brewer

ISBN: 978-1-904542-68-1

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 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 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 ( 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

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

Page Number 1. SEXUAL COERCION AND CHEATING 1.1. 1.2. 1.3. 1.4. Sexual selection and coercion Forced copulation Cheating for sex References 4

2. PARENTAL CARE 2.1. 2.2. 2.3. 2.4. 2.5. Parental care strategies Length of parental care Appendix 2A - Egg dumping Appendix 2B - Filial cannibalism References


3. REPRODUCTIVE STRATEGIES AND SUCCESS 3.1. 3.2. 3.3. 3.4. 3.5. 3.6.


Scramble competition Polyandry Choosiness Appendix 3A - Handicap and ornaments Appendix 3B - Male-male competition References

4. PRO-SOCIAL BEHAVIOUR AND CO-OPERATION 4.1. 4.2. 4.3. 4.4. Pro-social behaviour experiments Co-operation/teamwork Appendix 4A - Massen et al (2010) References




5.1. Magnetic sense 5.2. Appendix 5A - Magnetic sense in one or two eyes 5.3. References

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


1.1. 1.2. 1.3. 1.4. Sexual selection and coercion Forced copulation Cheating for sex References

1.1. SEXUAL SELECTION AND COERCION Sexual selection (as proposed by Charles Darwin in 1871) is the idea that males and females have evolved different optimum reproductive strategies. Males generally benefit most from copulation with multiple partners and providing limited or no parental care for offspring. Females invest more resources in reproduction, and so need to be choosy about who they mate with. They have the responsibility of pregnancy, and usually, childcare (table 1.1). These different strategies lead to conflict between the sexes, and coercion by males with "an evolutionary arms race where males evolve better armament and females evolve improved defences" (Dukas and Jongsma 2012). In other words, males can benefit from coercion more than females.
EXAMPLE - Male mates with ten females, who have one offspring each in the breeding season OFFSPRING MALE 10 fathered; can afford some not to survive Each female has one offspring and thus survival important STRATEGY Find many female mates; ie: indiscriminate; little concern for post-natal care Female invests time and effort in survival, but must exercise choosiness about male; ie: only mate with male who has "best genes"


Table 1.1 - Sexual selection and strategies for males and females. Males can coerce females to mate with them in three main ways (Clutton-Brock and Parker 1995): i) Harass them until they succumb. For example, male tortoiseshell butterfly (Aglais urticae) fly after females tapping them with their antennae until the female lands to allow mating (CluttonBrock and Parker 1995). There are costs to the females
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

which induce them to mate (eg: chased by male and unable to feed). Harassment (or repeated courtship) has costs to both sexes in terms of reduced feeding time, energy expended, and risk of predation. Specifically, females face the cost of competing males injuring them in inter-male fights, or "over-zealous mating" (eg: male sea otters hold mates by nose with teeth or claws; Clutton-Brock and Parker 1995). There are thus advantages for females to be part of a harem of a dominant male. For example, feral horses (Equus caballus) in male territorial harems have greater breeding success than females not, and have about 10% more time feeding (Rubenstein 1986). ii) Intimidation and punishment for refusal to mate. For example, male red and fallow deer prod females with their antlers (Clutton-Brock and Parker 1995). Observations of primates (eg: gorillas) have reported that aggressive males have more willing females (eg: based on time taken for female to present for copulation). Males are physically larger here, but in species where the body size is equal or females are larger, male aggression towards females is rare (CluttonBrock and Parker 1995). Such male aggression is more common in social species living in groups of multiple males and females. Here aggression helps the male to maintain exclusivity over the female. Male aggression is less likely in monogamous species and in harem groups (Clutton-Brock and Parker 1995). iii) Forced copulation. Usually the males of the species are stronger which facilitates this. For example, among orang-utans (Pongo pygmaeus) observed, up to half of copulations occurred after violent force by the male towards the female (Mitani 1985) 1. Males will be more likely to forcibly mate if their life expectancy is short and/or there is competition from other males if the individual waits (Clutton-Brock and Parker 1995). Forced copulation is very rare in species where a single male controls access to a group of females (harem). In this situation, the male waits until the females are ready to mate, and the females tend not to resist (Clutton-Brock and Parker 1995).

Seto (2000) questioned the parallel of forced copulation with human rape. 5

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

The "evolutionary arms race" related to coercion sees males evolve "weapons", like increased body size and strength 2, to enhance the ability to forcibly mate 3, while female evolve defences, like genitalia modifications that stop forced copulation or increased body size themselves. But, at the same time, there are restraints on development, like the energetic cost of larger male bodies, which outweigh any benefits of forced copulation (Clutton-Brock and Parker 1995). Females of different species have evolved strategies to combat harassment and intimidation including (CluttonBrock and Parker 1995): Avoid areas where males congregate. Become part of the harem of a dominant male - eg: such female deer are less likely to be harassed or interrupted by competing males during copulation. Accept matings in certain situations to avoid costs of refusal - eg: a male newly-arrived to a group can attack infants, and mating with them avoids this. Form female coalitions (eg: bonobos). Evolution of monomorphism - Sexual dimorphism is the difference in the body size and shape between males and females of the same species, while monomorphism is similarity between them. In other words, females evolve to be the same size and/or look like males (eg: the female damselfly, Ischnura ramburi, mimics male colouring). 1.2. FORCED COPULATION Dukas and Jongsma (2012) reported experiments on forced copulation with fruit flies (Drosophila melanogaster) (figure 1.1). Females who were forcibly mated had significantly fewer offspring than females who consensually mated, and had higher rates of wing damage and premature death. The forced copulation took place before the females were sexually mature (teneral 4) (day

Eg: male northern elephant seals (Mirounga angustirostris) weigh up to eight times more than females (Clutton-Brock and Parker 1995). 3 Thornhill and Sauer (1991) reported that male scorpionflies have an appendage called a notal organ that evolved specifically to clamp the female in place during forced copulation. 4 The wings not yet hardened and extended, thus females not able to fly away to prevent mating. It should be noted, however, that females can move to prevent males getting a stable mounting position. In fact, 75% of the sample avoided forced copulation (Dukas and Jongsma 2012). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 6

1), and then the females were given the opportunity to mate when sexually mature (day 3). Only 28% of the forcibly mated females took this opportunity compared to all virgins, and this accounts mostly for the reduced number of offspring as a group. There were four conditions to the experiment (figure 1.2). Males who forcibly mated sired significantly less offspring than consensually mating males mainly because forced matings were more likely to be fertile (ie: females were sexually immature). Forced copulation with sexually immature females is not a mistake by males because these females have a different odour to sexually mature females. But, say Dukas and Jongsma (2012): "In a setting where the ratio of sexually receptive females to males is close to zero, persistently pursuing young, sexually ambiguous conspecifics may be an optimal male strategy in spite of the little expected fitness gain" (p1182).

(Source: Botarus; in public domain)

Figure 1.1 - Drosophila melanogaster.

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

Figure 1.2 - Four conditions in Dukas and Jongma's (2012) experiment 1. Dunn et al (1999) reported limited reproductive benefits for males from forced extra-pair copulations among Lesser Snow geese (Chen caerulescens caerulescens) (figure 1.3) and Ross's geese (Chen rossi) nesting in Northern Canada. The birds were observed in random blocks of 4 hours over 24 hours of daylight divided into sixteen ten-minute sampling periods in June 1993 and 1995 5. In total, 65 copulations were observed, of which 32 (51%) were extra-pair among these monogamous species. All the extra-pair copulations appeared forced as the females made loud vocalisations in attempting to resist when she was on her nest (the majority of occasions - over threequarters) , or flee if off the nest. Normally there are pre-copulatory displays between the bonded pair.

(Source: Walter Siegmund)

Figure 1.3 - Lesser Snow Goose.

Focal sampling was used - the observers looks at one individual or nest for the sampling period. 8

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

The DNA fingerprinting from blood samples of 50 families of geese found that forced extra-pair copulations led to few young (less than 5%). This is a low fertility rate for approximately one-third of attempted forced copulations being successful (based on the male appearing to make cloacal contact with the female - ie: tail of male twisted underneath the tail of the female and thrust towards her). It may be that less sperm is transferred in such copulations, or, more likely, forced copulations occur when the female is incubating eggs and thus non-fertile (figure 1.4) 6. Despite this, "forced copulations are successful occasionally and may provide some males with significant increases in reproductive success" (Dunn et al 1999 p1079).

Figure 1.4 - Breakdown of copulations observed. Forced extra-pair copulations have not been reported in other Canadian geese (eg: pink-feathered geese), and the key seems to be size of the male territory. In these geese males defend a large territory whereas only a small area around the nest in Lesser Snow and Ross's geese (Dunn et al 1999). Male birds use a number of cues to establish if the female is fertile. These include female behaviours like nest building and egg laying 7, or male behaviours like

Three phases were distinguished - pre-laying (arrival at site until 1st egg), laying (1st to last egg laid), and early incubation (all eggs laid until 8th day of incubation). Many of the forced copulations were during the latter period. 7 Females may try to hide their signs of fertility - eg: female stitchbirds hide the first two eggs of a clutch in the nest-lining material as extra-pair males search nests looking for signs of egg laid and thus female fertility (Low 2004). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 9

mate-guarding. Low (2004) found that male stitchbirds (Notiomystis cincta) (figure 1.5) are sensitive to increased female weight as seen in her flight behaviour (eg: changes in vertical flight speed and take-off angle). Low (2004) observed two breeding seasons of this bird on an island off the north-east coast of New Zealand (where all the birds are ringed and artificial nestboxes are provided). Females gained about one-third body weight in the twenty days before egg laying. Extra-pair copulations (as measured by intrusions into another male's territory) tended to be forced as the females actively resisted 8 9, and these correlated with increased female weight 10 11.

(Source: Duncan Wright)

Figure 1.5 - Male stitchbird. Females may resist forced copulation, though incurring a cost, for a number of reasons (Clutton-Brock

78% of extra-pair copulations observed were forced (Low 2004). Females are sometimes injured (Castro et al 1996). 10 The use of the weight as a cue would explain the observation by Ewen and Armstrong (2002) of forced copulation with juveniles. Juvenile stitchbirds weigh the same as a female about to lay her eggs (Low 2004). 11 Jones (1986) artificially increased the body weight of female sand martins with injections of saline. A 20% increase in body weight led to the most chases by extra-pair males.

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


and Parker 1995): The benefit of mating with a superior male. When breeding conditions are more favourable. The male is genetically incompatible. Accepting mating by a subordinate male leads to punishment from the dominant male. Forced copulation, where common, can be countered by the evolution of control of fertilisation by females including delaying egg and sperm combination. This strategy works for internal fertilisation, but not external fertilisation. For example, in frogs the male attaches himself to the back of the female and holds on (amplexus) 12 (figure 1.6); this leads to a batch of eggs being laid which he then fertilises externally. Female frogs have evolved strategies to counter the stimulation of amplexus to lay eggs including behaviours to stop amplexus (eg: fleeing, or taking a vertical body position), or delaying depositing eggs (Hettyey et al 2009).

(Source: Jojo)

Figure 1.6 - Rana temporaria in amplexus.

The male grasps the female around the middle until the eggs are released for several hours to weeks (Purves et al 1997). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 11


Forced copulation can occur between species that are similar (heterospecifics), though the offspring may not be viable. Hettyey et al (2009) found that, among two closely related species of European brown frogs (Rana dalmatina; RD; figure 1.7; and Rana temporaria; RT), females would lay a smaller clutch of eggs when amplexus from a male of the other species. This tended to cause the male to release, and the female had some opportunity to find a male of their own species (conspecific) in that breeding season (though repeated egg laying is relatively rare).

(Source: H Krisp)

Figure 1.7 - Rana dalmatina. The two species of frogs, found in central Europe, are "explosive breeders", which means that they have short breeding seasons that are a "free for all". Males mate indiscriminately with their own and other species, and females are unable to stop amplexus. Hettyey et al (2009) collected frogs from two areas in the Pilis Mountains in Hungary at the start of the breeding season in March 2008. RD females were found in the experiments to take significantly longer to deposit eggs after amplexus started when the male was another species (RT) (mean 60 hours) than own species (RD) (mean 35 hours).
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


During this time it was possible that a RD male could force off the RT male (takeover), or the RT male may become exhausted and release. RD females also laid significantly less eggs (average 30%) with RT males than RD males. 1.3. CHEATING FOR SEX Sexual dimorphism exists among males of the same species, as first observed in two insect species in the late nineteenth century (Bateson and Brindley 1892). This observation led to the study of alternative reproductive tactics (ARTs) - ie: different strategies to gain access to mates by males (and females) of the same species. For example, males of a species may invest effort in building a nest to attract a female ("classical" or "bourgeois tactic"), while other males will not build nests but wait nearby to catch the opportunity of mating (often by forced copulation) ("parasite" or "sneaking tactic") (Brepson et al 2012). In some species, individuals will always use one of these strategies (eg: because of body size) 13 14, whereas in other species the individuals can switch between them (eg: early or late arrival at nesting site and availability of space) 15. For example, among anurans, males calling from their territory is the classical tactic while silent males waiting nearby (satellites) (table 1.2) is the sneaking tactic. Calling and/or defending territory requires a lot of energy, and individuals lacking that energy may use the satellite tactic in that case (energetic constraint hypothesis). Alternatively, some males will always use the sneaking tactic because of low fighting ability or unattractive calls, for example (inherent disadvantage hypothesis) (Brepson et al 2012).
However, this strategy only works if a minority of frogs are "satellites" or "satellites" on some night only. Otherwise, the chorus would fall silent. Varying between calling and "satelliting"

For example, factors during development influence whether a bluegill sunfish (Lepomis macrochirus) becomes a parental or cuckolding male (Gross and Charnov 1980). The former males construct nests, attract females and provide brood care. They have more growth per year of development, based on observations between 1976 and 1979 in Lake Opinicon, Ontario, Canada. The cuckolding males sneak or mimic female behaviour to gain access to spawnings. They have less growth per year. 14 Pradham et al (2012) reported that male Sumatran orangutans (Pongo abelii) can delay puberty (developmental arrest) until physically strong enough to challenge the dominant male who controls the females (In Brief 2012). 15 For example, the solitary bee (Ptilothrix fructifera) can switch between territorial and non-territorial tactics (Oliveira and Schlindwein 2010). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 13


is evidence of an "evolutionary stable strategy" (ESS) (Maynard Smith 1976). "Satelliting" is a good strategy, though, for smaller, and for younger males. "Satellite" behaviour (or parasitic behaviour) has been found in many species of frogs. Usually silent males close to the chorus waiting to intercept approaching females. There are variations on this behaviour: a) medium-sized Bullfrog males will infiltrate the territory of larger males, who are mating, in order to call (Mauger 1988); b) "satellite" males calling in unison to interfere with the female's ability to find the chosen male (Ovaska and Hunte 1992); c) "satellites" chase amplexing pairs and attempting to remove the male, with limited success in African leaf-folding frogs (Blackwell and Passmore 1991); d) silent "satellite" behaviour has also been observed in larger males in order to save energy or avoid predators who hunt by sound (Perrill and Magier 1988).

Table 1.2 - Variations on satellite behaviour. Brepson et al (2012) investigated experimentally the use of satellite behaviour by male European treefrog (Hyla arborea) (figure 1.8). Males of this species call for long periods of the night as part of a chorus to attract females. One hundred males captured near Lyon, France, were placed individually in an artificial environment with one loudspeaker playing a chorus 16 and another playing a specific competitor.

(Source: Christian Fischer)

Figure 1.8 - European treefrog calling by expanding vocal sac.


A recording of ten males with no male louder. 14

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

Male behaviour was scored in three ways: Caller - male makes at least one call in the twenty minutes of the experiment. Satellite - male stays silent but moves close to loudspeaker of competitor. No response - no call or movement towards speaker. In 200 trials, 47 males were categorised as "caller" (23.5%) and 35 as "satellite" (17.5%). The researchers tested three hypotheses about the use of satellite behaviour (figure 1.9): i) Small males will use it (inherent disadvantage hypothesis) - It was found that smaller males (based on snout-vent length and weight) were more likely to adopt satellite behaviour. ii) Males deprived of food will use it (energetic constraint hypothesis) - Half the frogs were fed and half were not for seven days before the experiment. There was no difference between them in use of satellite behaviour 17 . iii) Males confronted by an attractive competitor will use it - Calls were played over the loudspeaker from an attractive and an unattractive competitor. Males were more likely to show satellite behaviour if an attractive call was played than an unattractive one.

Figure 1.9 - Basic design of experiment by Brepson et al (2012).

Brepson et al (2012) explained this unexpected finding as due the food deprivation not been long enough. Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 15


The findings support the idea that male frogs use satellite behaviour on a permanent basis, in the case of small individuals, and switch, in the case of having an attractive competitor. 1.4. REFERENCES
Bateson, W & Brindley, H.H (1892) On some cases of variation in secondary sexual characters, statistically examined Proceedings of the Zoological Society of London 60, 585-594 Backwell, P & Passmore, N (1991) Satellite behaviour in the leaffolding frog, Afrixalis delicatus Journal of Herpetology 25, 497-498 Brepson, L et al (2012) Cheating for sex: Inherent disadvantage or energetic constraint? Animal Behaviour 84, 1253-1260 Castro, I et al (1996) Polygynandry, face-to-face copulation and sperm copulation in the hihi Notiomystis cincta (Aves: Meliphagidae) Ibis 138, 765-771 Clutton-Brock, T.H & Parker, G.A (1995) Sexual coercion in animal societies Animal Behaviour 49, 1345-1365 Darwin, C (1871) The Descent of Man, and Selection in Relation to Sex London: John Murray Dukas, R & Jongsma, K (2012) Costs to females and benefits to males from forced copulations in fruit flies Animal Behaviour 84, 1177-1182 Dunn, P.O et al (1999) Forced copulation results in few extra-pair fertilisations in Ross's and lesser snow geese Animal Behaviour 57, 10711081 Ewen, J.G & Armstrong, D.P (2002) Unusual sexual behaviour in the stitchbird (or hihi) Notiomystis cincta Ibis 144, 530-531 Gross, M.R & Charnov, E.I (1980) Alternative male life histories in bluegill sunfish Proceedings of the National Academy of Sciences, USA 77, 6937-6940 Hettyey, A et al (2009) Counter-strategies by female frogs to sexual coercion by heterospecifics Animal Behaviour 78, 1365-1372 Jones, G (1986) Sexual chases in sand martins (Riparia riparia): Cues for males to increase their reproductive success Behavioural Ecology and Sociobiology 19, 179-185 Low, M (2004) Female weight predicts the timing of forced copulation attempts in stitchbirds, Notiomystis cincta Animal Behaviour 68, 637-644 Mauger, D (1988) Observations on calling behaviour of bullfrogs in relation to male mating strategy Bulletin of Chicago Herpetological Society 23, 57-59 Maynard Smith, J (1976) Evolution and the theory of games American Scientist 64, 41-45 Mitani, J.C (1985) Mating behaviour of male orang-utans in the Kutai Reserve Animal Behaviour 33, 392-402 Oliveira, R & Schlindwein, C (2010) Experimental demonstration of alternative mating tactics of male Ptilothrix fructifera (Hymenoptera, Apidae) Animal Behaviour 80, 241-247 Ovaska, K & Hunte, W (1992) Male mating behaviour of frog Eleutherodactylus johnstonei (Leptodacxtylidae) in Barbados, West Indies

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1



48, 40-49

Perrill, S & Magier, M (1988) Male mating behaviour in Acris crepitans Copeia 1988, 245-248 Purves, W.K et al (1997) Life: The Science of Biology (5th ed) Sunderland, MA: Sinauer Associates Rubenstein, D.I (1986) Ecology and sociality in horses and zebras. In Rubenstein, D.I & Wrangham, R.W (eds) Ecological Aspects of Social Evolution Princeton, NJ: Princeton University Press Seto, M (2000) A natural history of rape (book review) Animal Behaviour 60, 5, 705-706 Thornhill, R & Sauer, K.P (1991) The notal organ of the scorpionfly (Panorpa vulgaris): An adaptation to coerce mating Behavioural Ecology 2, 2, 156-164

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


2.1. 2.2. 2.3. 2.4. 2.5. Parental care strategies Length of parental care Appendix 2A - Egg dumping Appendix 2B - Filial cannibalism References

2.1. PARENTAL CARE STRATEGIES To maximise the passing of genes into future generations, parents balance the effort/investment put into rising the current offspring with future opportunities for more offspring. Thus there is a tradeoff in terms of the parental care given to offspring. For example, a mother who guards the newly laid eggs reduces her opportunities to forage and mate again, but desertion risks predation of the vulnerable eggs waiting to hatch 18 . This is a balance of viability and fecundity. The latter term relates to the number of fertilised eggs, and viability is the fertilised egg's chances of surviving (table 2.1).
FECUNDITY VIABILITY FISH High Low EVOLUTIONARY STRATEGY Many eggs laid but few survive (parental care less important) Few or single eggs fertilised but most survive (parent care important)




Table 2.1 - Examples of fecundity and viability. There are a number of strategies that females can use (and some include assistance from males) which vary from immediate desertion after birth or eggs laid (no maternal care) to care for current offspring until mature (long-term maternal care). Variations on no maternal care include egg hiding (leaving the eggs but they are hidden from predators until hatched), coating eggs with a protective substance, egg dumping (appendix 2A) or parasitism (putting eggs in nest of another parent to be raised with their offspring), or temporary brood

Altricial offspring are dependent on parent(s) after birth/hatching while precocial offspring are independent from birth/hatching. No parental care for the former is too risky (ie: very low survival without care). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 18


desertion (Chelini and Machado 2012). No maternal care or permanent brood desertion has advantages for the mother in the following situations (Chelini and Machado 2012): Mother able to raise another brood in same breeding season. Maternal care reduce "reproductive value" (eg: ageing and loss of attraction to males). High fecundity - ie: opportunity for many offspring. Chelini and Machado (2012) reported the benefits of temporary brood desertion by a species of spider (harvestman, Neosadocus maximus (Gonyleptidae)) in Brazil. A clutch of eggs is laid on the undersurface of a leaf. They are vulnerable to predation from ants, for example, but egg guarding by the female costs in terms of no food and dehydration 19. Predation was higher at night (mean: six eggs vs 2 in day), so mothers who left the brood during the day benefited most with less cost. The median brood desertion observed by the researchers was 48% at night and 95% during the day. Exclusive care by the father is rare and occurs in only a few species. Some males who egg guard are able to protect multiple broods simultaneously, so their opportunities to mate are not reduced by paternal care. In the species where exclusive paternal care exists, females should prefer such males. In other words, males already guarding one brood of eggs will be attractive to females as this is an honest signal of the male's quality. "From the females' perspective, paternal care may be favoured by sexual selection because it offers the direct, fitness-enhancing gift of cost-free care of their offspring and the freedom to forage for additional food, which may enhance their lifetime fecundity" (Requena et al 2009). Among the species of harvestman (Iporangaia pustulosa (Gonyleptidae: Progonyleptoidellinae)), found in Brazil, females lay their eggs on the underside of leaves for the male to guard. Though the hatching process takes about forty days, other females add to the brood and the guarding period can last more than four months (figure 2.1). Males sometimes temporarily desert for up to 48 hours (Requena et al 2009).

Some species cope by eating some of the young (filial cannibalism) (appendix 2B). This allows the parent to stay with the offspring without going hungry. Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 19


(Source: Requena et al 2012)

Figure 2.1 - (A) Male Iporangaia guarding eggs. (B) Eggs at different stages of development (as shown by numbers).
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


Requena et al (2009) performed a series of experiments on the effectiveness of the Iporangaia's parental care: i) Care vs no care - Over twelve days the predation of eggs was recorded for broods with a male guard and without. In the latter case, fifteen of sixteen clutches had been predated (with six completely eaten) compared to only 6 of 12 attacked (with one completely consumed) where a male was present. In total, 60% of "no care" eggs were predated compared to 10% of the "care" eggs. Thus male guarding of eggs is beneficial in reducing predation. ii) Mucus vs no mucus - Females cover the eggs with a mucus coat before leaving them to the male to guard. Over four days 40% of "no mucus" eggs were eaten compared to 10% of "mucus" eggs. There was no male guard in either condition of this experiment. The mucus coating protects the eggs against predation, and is a strategy as the female cannot be entirely sure that the male will not desert the brood (temporarily or permanently). iii) Paternal vs maternal care - The data from the first experiment on paternal care were compared to a similar species (Acutisoma proximum) where the female guards the eggs. There was a care and no care condition. The loss of eggs in the "no care" condition of Acutisoma was highest (80%). This may be because the eggs of this species are not covered by a mucus coating. Importantly, the male care of the Iporangaia was as effective as the female care of the Acutisoma. Requena et al (2009) noted: "If males' attractiveness depends on the number of eggs they have in their clutches, even if they have not sired these eggs..., they should care for the offspring as efficiently as females". Manica and Johnstone (2004) found similar levels of success in egg guarding between two species of assassin bug - Rhinocoris tristis (paternal care) 30.4% of clutches had egg mortality, and Rhinocoris carmelita (maternal care) 34.4% of clutches. 2.2. LENGTH OF PARENTAL CARE How long for a parent to nest guard, for example? A longer period will improve the survival chances of the offspring at the expense of the future reproductive opportunities for the parent, while a shorter period is the opposite. Catry et al (2006) were interested in the cues used by grey-headed albatrosses (Thalassarche chrysastoma)
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 21

(figure 2.2) as to when to stop brood guarding. Do the parents use cues about the age of the offspring (eg: body size) or their own body resources (eg: loss of fat resources)?

(Source: Ben Tullis)

Figure 2.2 - Grey-headed albatross chick. The researchers switched chicks between nests of albatrosses on Bird Island, South Georgia (figure 2.3). In one condition of the field experiment ("Small Chick"), 12 day-old chicks were replaced by six day-olds (compared to a control group where a 12 day-old was switched for another twelve day-old). In the "Large Chick" condition, a 6 day-old chick was replaced by a 12 day-old one (along with a control group that replaced one 6 day-old with another 6 day-old). There were 49 Small Chicks (and 49 controls) and 46 Large Chicks (and 45 controls). If the parents used the chick's development as a cue to stay at the nest, they will adjust their behaviour based on the new chick - ie: stay longer in the Small Chick condition and go earlier in the Long Chick condition than the controls. But if the parents used their body resources as a cue, they will not alter their length of stay at the nest.
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


The results suggested that parents used a combination of cues about their own body resources and the offspring's body size. In the Small Chick condition, parents significantly extend their brood guarding by a mean of 1.4 days more than their controls (mean total: 27.7 vs 26.3 days) (not a full 6 days if only using the offspring's body size as a cue). While in the Large Chick condition, guarding was significantly reduced by an average of 1.2 days (compared to their controls) (mean total: 22.6 vs 23.8 days). In fact, Catry et al (2006) felt that an "internal clock" (controlled by the hormone prolactin) could determine how long the nest guarding continued, and that offspring's body size and adult's body resources were fine tuners of the whole process.

(Source: Apcbg)

Figure 2.3 - Location of Bird Island. 2.3. APPENDIX 2A - EGG DUMPING Egg dumping has been observed in birds, salamanders, fish, and insects (Tallamy 2005). Eggs can be left with other eggs of the same species (conspecifics) or another similar species (heterospecifics). Egg dumping has evolved as a compromise between the costs of not guarding the eggs (ie: high loss) and the costs of guarding (ie: loss of future reproductive
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 23

opportunities). For example, maternal protection of eggs improved the survival of offspring tenfold in two species of lace bugs (Gargaphia solani; figure 2.4; and Gargaphia tiliae), but safeguarding takes nearly half of the female's adult lifespan. Females of species of lace bugs that do not guard, lay twice as many eggs and lay them earlier in life (Tallamy 2005).


Figure 2.4 - Gargaphia solani. Among insect species where egg dumping is common, females may both dump eggs and act as a guard of egg masses (a collection of different females's eggs). For example, a treehopper (Polyglupta dispar) female observed by Eberhard (1986) guarded two clutches of her eggs, rested for five days, then dumped eggs for the next fifteen days, and lastly, guarded a mass of eggs. Females who used the "dump, then guard" strategy had a lifetime
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


fecundity about one-quarter higher than "guard only" females (Tallamy 2005). Egg dumping is also used by females without a territory as a better option than no eggs at all. For example, burying beetles lay their eggs in a dead carcass (territory), which are in short supply and so females fight fiercely over them. Defeated females stay nearby and sneak their eggs in with those of the territorial female (Tallamy 2005). The hosts can benefit from egg dumping if the dumped eggs are kin (ie: increase in common genes survive) or safety in numbers. More eggs could reduce the individual risk of predation (dilution effect). Also dumped eggs are often on the surface of the egg mass and thus more vulnerable to predation (Tallamy 2005). The dumped eggs are a buffer zone with, for example, 37% mortality among lace bugs compared to 23% for the eggs in the centre of the mass (Tallamy and Horton 1990). 2.4. APPENDIX 2B - FILIAL CANNIBALISM Filial cannibalism has been reported in some birds, mammals 20, and insects. As well as providing food for the parent to aid egg guarding 21, it my occur when food is short for the offspring and by reducing their number, there is an increased opportunity for survival of the remainder ("selective brood reduction") (Thomas and Manica 2003). Thomas and Manica (2003) reported filial cannibalism in the assassin bug (Rhinocoris tristis), where the mle guards the eggs of multiple females against parasitic wasps and other insects for 15-43 days. During the observations in Uganda, broods were checked twice a day, and ten males were weighed daily. The guarding males did not lose weight because they consumed eggs on the outside of the brood (which were more likely to be parasitised by wasps). Thomas and Manica (2003) offered three reasons for filial cannibalism by egg-guarders, particularly males: a) To remove damaged/diseased eggs - eg: female mouthbrooding cichlid (Pseudocrenilabrus multicolor)

Fowler and Hohmann (2010) reported the first case of bonobos including the mother eating an infant that had died from natural causes. A limited number of observations had been made by researchers of cannibalism among primates (Callaway 2010). 21 But three-spined sticklebacks were found to engage in filial cannibalism even when well-fed (Thomas and Manica 2003). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 25


swallow unfertilised eggs after spawning. b) To increase the brood's attractiveness to females - eg: female garibaldi damselfish (Hypsypops rubicundus) prefer to add eggs to young broods, and so males consume older eggs. c) To benefit the guarding parent now (ie: ability to guard more effectively) and later (ie: ability to produce future broods). 2.5. REFERENCES
Callaway, E (2010) Cannibal bonobos "needed the food" New Scientist 6/2, p14 Catry, P et al (2006) Factors affecting the solution of a parental dilemma in albatrosses: At what age should chicks be left unattended? Animal Behaviour 72, 383-391 Chelini, M.C & Machado, G (2012) Costs and benefits of temporary brood desertion in a Neotropical harvestman (Arachnida: Opiliones) Behavioural Ecology and Sociobiology 66, 1619-1627 Eberhard, W.G (1986) Possible mutualism between females of the subsocial membracid Polyglypta dispar (Homoptera) Behavioural Ecology and Sociobiology 19, 447-453 Fowler, A & Hohmann, G (2010) Cannibalism in wild bonobos (Pan paniscus) at Lui Kitale American Journal of Primatology 72, 6, 509-514 Manica, A & Johnstone, R (2004) The evolution of parental care with overlapping broods American Naturalist 164, 517-530 Requena, G.S et al (2009) Efficiency of uniparental male and female care against egg predators in two closely related syntopic harvestmen Animal Behaviour 78, 1169-1175 Requena, G.S et al (2012) Paternal care decreases foraging activity and body condition, but does not impose survival costs to caring males in a Neotropical Arachnid PLoS ONE 7, (10), e46701 (Freely available at Tallamy, D.W (2005) Egg dumping in insects Annual Review of Entomology 50, 347-370 Tallamy, D.W & Horton, L.A (1990) Costs and benefits of the eggdumping alternative in Gargaphia lace bugs (Hemiptera: Tingidae) Animal Behaviour 39, 352-359 Thomas, L.K & Manica, A (2003) Filial cannibalism in an assassin bug Animal Behaviour 205-210

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1



3.1. 3.2. 3.3. 3.4. 3.5. 3.6. Scramble competition Polyandry Choosiness Appendix 3A - Handicap and ornaments Appendix 3B - Male-male competition References

3.1. SCRAMBLE COMPETITION The dispersion of females in a species can determine the mating strategy used by males. Where the females live close together, as in herds, a dominant male can establish a "harem" to guard and fight off rivals (eg: northern elephant seals, Soay sheep). Males in this situation who win the fights (real or ritualistic) have the greatest reproductive success, and so characteristics that aid this will be evolutionarily beneficial (eg: larger body size, "weapons" like horns, ornaments) (appendix 3A). These species tend to be sexually dimorphic (ie: large difference in physical appearance between males and females of the species). If females are spatially dispersed, males will employ a scramble competition mating system (eg: some insects and rodents). This is where males look for females who are sexually receptive. Sexual selection will favour in males characteristics that aid the location of mates (eg: sensitivity of smell, acuity of hearing) 22. Such species may be monomorphic (ie: little difference in appearance between sexes). One animal that shows scramble competition mating is a squirrel called the Siberian chipmunk (Tamias sibiricus barberi) (figure 3.1). Marmet et al (2012) studied a population in a forest 15 miles south-east of Paris, France (Forest of Senart). The researchers captured 226 animals in 2006, and were able to calculate the annual reproductive success 23 of 63 oft-caught adults (using DNA fingerprinting). Siberian chipmunks are solitary with large overlapping home ranges. Twice per year, in March and June, females are sexually receptive for 1-2 days. This is signalled by a distinctive female call, which causes the males to congregate around the female.

For example, among North American red squirrel (Tamiasciurus hudsonicus) male reproductive success was found to be related to search ability (ie: number of receptive females located in breeding season) and size of home range (Lane et al 2009). 23 Defined as "genetically detected number of offspring for an individual in 2006" (Marmet et al 2012). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 27


(Source: Illustrierter Leitfaden der Naturgeschichte des Thierreiches (1876); in public domain)

Figure 3.1 - Drawing of Siberian chipmunk. Males with larger home ranges had greater reproductive success because of the increased chance of meeting females as they moved around the range. For example, one male's large range overlapped with nine females' ranges compared to only two females in a smaller range. Ten males with larger ranges in semi-open oak groves (mean size: 1.45 hectares) had an annual reproductive success of 2.7 offspring compared to 1.5 offspring among nineteen males with smaller ranges in closed oak-hornbeam groves (mean size: 0.63 hectares). Where males are "hunting" for females, there may evolve advantages in spatial ability and navigation in the male of the species (as compared to the female, and to species where males and females are spatially close together). For example, male meadow voles (Microtus pennsylvanicus), who compete by searching for multiple females in the breeding season, have enhanced spatial abilities over females, and over male and female prairie voles (Microtus ochrogaster), who share home ranges with their mate (Jasarevic et al 2012). The spatial abilities, like memory retention and use of spatial cues, are usually tested in laboratory
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 28

experiments with mazes (eg: speed or number of errors in finding escape holes). Using this method, Jasarevic et al (2012) compared 26 deer mice (Peromyscus maniculatus bairdii) (figure 3.2) who use mate searching, and 21 California mice (Peromyscus californicus insignis) who do not, on the Barnes maze (Barnes 1979). This is a circular maze with twelve possible escape holes (of which only one leads back to the home cage), and four cues (triangle, square, circle, and square shapes) on the maze wall. The actual escape hole was varied by random assignment for each mouse. There were two trials per day for seven days during which the speed of escaping and number of errors were measured. It was expected that in the early trials the escape would take longer, but later the mouse should be quicker and make fewer errors.

(Source: Centers for Disease Control and Prevention; in public domain)

Figure 3.2 - A deer mouse. From Day 5 onwards, male deer mice were significantly more likely to go directly to the correct escape hole when released than female conspecifics and California mice (figure 3.3). The speed to reach the escape hole was significantly faster for male than female deer mice (mean: 33 vs 81 seconds).

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


Figure 3.3 - Percentage of mice going directly to correct escape hole when released on Day 7. 3.2. POLYANDRY Polyandry is where a female mates with several males in the same breeding season. Sometimes this is forced by males, but it can also be voluntarily. If it is the latter, what are the benefits to the female? The most important is the guarantee of fertilisation (known as the fertilisation insurance hypothesis; Parker 1970). Other benefits include multiple parental care or protection from infanticide as the males cannot be sure if they are the father or not. Polyandry has been reported in over a dozen species of frogs (anuran amphibians) (Byrne and Whiting 2008). In some cases, it is not beneficial - eg: West Australian myobatrachid frog (Crinia georgiana) (Byrne and Roberts 1999). Polyandrous females had less fertilisation success 24 than single-male maters (monogamous). This may have been because of the fierce competition between males interferes with mating (eg: mating position for sperm release) or egg laying (Byrne and Whiting 2008). But among the African foam-nesting treefrog (Chiromantis xerampelina) polyandry increases fertilisation success. Byrne and Whiting (2008) studied this frog at the Tsonga Kraal Dam, South Africa in 20067. The percentage of eggs fertilised within a clutch and the total number of eggs fertilised were each significantly positively correlated with the number of males mated by the female. The mean overall fertilisation rate was 64%, but this was only 54% for monogamous females. For example, where six to eight males were


Fertilisation success = number of offspring produced from a clutch of eggs (ie: fertilised eggs). 30

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

observed to mate with the female, fertilisation success was closer to 70%. 3.3. CHOOSINESS Sexual selection is primarily based on male-male competition (appendix 3B) and female choice. The female of the species decides between competing males trying to show (through behaviour and/or appearance) who has the best quality genes. This is because females invest more in reproduction than males. But there are species where the reverse occurs. Where males invest a lot in mating, they can choose between females. Male investment includes lengthy courtship, prolonged mate guarding, sperm depletion, or brood guarding, which limit his future reproductive success. "If these costs are high, selection should favour the allocation of mating effort towards those females capable of providing maximum reproductive gains" (Reading and Backwell 2007 p867). Male choosiness exists where the benefits of mating with a highly fecund female outweighs mating indiscriminately with many females. This situation occurs if the quality of females (eg: clutch size) is highly variable. Choosiness is also influenced by the operational sex ratio (OSR) (Emlen and Oring 1977) - "the number of receptive females to competing males" (Reading and Backwell 2007). If there are more males than females, then female choosiness exists and males mate indiscriminately, but the opposite if there are more females than males. The fiddler crab (Uca mjoebergi) (figure 3.4) exhibits signs of male choosiness. Females are highly variable in body size (which correlates with fecundity 25 ), and males invest energy in mate guarding (for 1-9 days; Reading and Backwell 2007) as the last sperm has precedence. But the OSR is male biased (10 males:7 females; Reading and Backwell 2007), and males have a single enlarged claw that is used in male-male competition. Reading and Backwell (2007) explored the trade-off between costs and benefits of male choosiness in Darwin, Australia. Males were found to use two strategies - a choosiness for large females, but, at the same time, not foregoing the opportunity to mate with any sized female.

Reading and Backwell (2007) reported a significant Pearson correlation of r = 0.59 from their observations in Australia in 2005-2006. Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 31


(Source: US National Oceanic and Atmospheric Adminstration; in public domain)

Figure 3.4 - Fiddler crab. Males in the mangroves of East Point Reserve were offered a choice of two different females tethered with cotton thread glued to a carapace fastened in the mud one large (top one-third of body size) and one small (bottom one-third). The choice was either simultaneous (180 apart) or sequential (with a ten-minute interval). In the simultaneous condition, males spent significantly more time courting (waving enlarged claw 26) and mating with the large female (mean: 108 seconds) than the small female (mean: 38 seconds). In the sequential condition when a large female was presented first, the males spent significantly more time courting and mating with her than the second smaller female, but when the small female was presented first, the males spent as much time as with the second larger female. In the latter, an opportunist strategy seemed to be at work. "Males never rejected mate-searching females, regardless of their size...While males may preferentially court large females, they will not forego a mating opportunity with a small female. This is not surprising since the highly male-biased OSR means that males are unlikely to attract a second female after rejecting the first. By accepting all females available to them, but intensifying courtship towards larger more fecund females, males may be matching the cost of courtship to the potential benefits gained" (Reading and Backwell 2007 p871).

A mean of 20 waves per 5-minute period towards the large female and 9 towards the small female (p0.05). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 32


3.4. APPENDIX 3A - HANDICAP AND ORNAMENTS Male communication, whether by calling or physical behaviour and appearance, is a way of conveying the quality of genes. An honest signal is where "individuals of higher quality can pay highest costs to produce a more elaborate display or when individuals gain higher benefits for producing a display of given cost" (Hawkes and Bird 2002 p58). Only signals that are too costly to fake are the reliable ones of honesty. Zahavi (1975) coined the term "the handicap principle" for the "waste" (of energy) involved in honest signals of good quality genes. A "show-off" is saying that their quality is so good that they can afford to "waste" resources (eg: carrying heavy physical ornaments or calling for excessively long periods) 27. "Elaborate monomorphism" is where both sexes of a species have ornaments (eg: cumbersome tails, bright colours) (Tarvin and Murphy 2012). The genetic correlation hypothesis (Lande 1980) explains the situation where the females have subdued versions of the males' ornaments (eg: parulid warblers). Both sexes carry the genes for the ornaments, but only the males gain from expressing them. But where both sexes are similar in appearance (eg: parrots), there must be an advantage for females to express the genes as ornaments. For example, femalefemale competition for sexual and non-sexual resources (eg: food) could lead to their evolution. Another explanation is called "assortative pairing". Females prefer the most elaborate males while the males simultaneously prefer the most elaborate females (Tarvin and Murphy 2012). van Rooij and Griffiths (2012) struggled to find evidence for benefits of ornaments in both sexes related to sexual selection in long-tailed finches (Poephila acuticauda). It was suggested that "it is possible that the ornamental traits carried a signalling function in one or both sexes in the past but that the signalling role of the traits they measured is now redundant with other traits, or alternatively, the function of the traits may vary geographically and thus be important in some areas but not others. In essence, the costs and benefits associated with expressing and/or attending to

Webster (2012) reported the example of "phenotopic plasticity" (ie: temporary plumage change) among red-backed fairy wrens. Males of these birds have two appearances - brightly-coloured red and black or brown. Females prefer the former (and they have more offspring), but these males also face more male aggression. If such a male is not successful in mating, their plumage will change to brown as a strategy to avoid male aggression and to survive to the next breeding season. The colour of the plumage is controlled by testosterone. Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 33


ornamentation may change over time or space..." (Tarvin and Murphy 2012 p441). The ornaments could be "badges of status" or predator deterrent signals. "For example, both sexes could use ornaments as socially selected status signals to mediate competition (within and between sexes) for access to non-sexual resources such as food or territory. As this type of signal does not necessarily increase mating success (and therefore is not considered a form of sexual selection) it is unlikely to lead to assortative pairing" (Tarvin and Murphy 2012). 3.5. APPENDIX 3B - MALE-MALE COMPETITION Male-male competition can involve physical fighting, but this carries the risk of injury or death. It is important to assess the fighting ability (known as "resource holding potential"; RHP) of the opponent in order to estimate the cost of fighting them. This information is conveyed by agonistic signals (which are communications about attack and threat, escape, defence or appeasement) (Rillich et al 2007). There are a number of theories to explain the decision to fight or escape including (Rillich et al 2007): Mutual assessment hypothesis - an individual assesses their RHP relative to that of their opponent. Own RHP-dependent persistent hypothesis - no assessment of the opponent occurs, and contests continue until a threshold is passed (eg: energy costs); eg: roaring contests by male red deer. Cumulative assessment hypothesis - the decision to stop fighting occurs when "the total physical cost, (or damage) inflicted by the opponent surpasses some threshold" (Payne 1998). Rillich et al (2007) found support for the last theory in experiments with Mediterranean crickets (Gryllus bimaculatus). Two male crickets were placed, each time, at opposite ends of a small glass arena, and the level of aggression was scored 0-6 depending how far the fight went. For example, level 6 was categorised as "grappling" - "at this stage an all-out fight ensues, during which the animals may repeatedly disengage, struggle for position, bite other body parts, and reengage mandibles to push or overthrow the opponent with the assistance of the foreleg claws" (p825). The researchers manipulated aspects of the crickets including disabled mandibles or blinded by black paint.
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 34

Contests were either symmetrical (both opponents had same disability) or asymmetrical (different handicap for each fighter). The aim was to see what signals were used in deciding to fight or not. In the control group of normal crickets, most fights were rated as level 5 ("mandible engagement: the mandibles interlock and the animals push against each other") and lasted a median of nine seconds. Of 121 such fights, 62% became a physical fight. When different body parts were disabled, the fights were more aggressive and longer, suggesting that the contestants needed more time to surpass a threshold. For example, among crickets both blind and with disabled mandibles, all 22 pairings became physical fights (figure 3.5), which lasted an average of 37 seconds. The decision to stop fighting was based "solely on the opponent's actions" (as predicted by the cumulative assessment hypothesis) (Rillich et al 2007).

Figure 3.5 - Percentage of symmetrical pairings that became physical fights. 3.6. REFERENCES
Barnes, C.A (1979) Memory deficits associated with senescence: A neurophysiological and behavioural study in the rat Journal of Comparative and Physiological Psychology 93, 74-104 Byrne, P.G & Roberts, J.D (1999) Simultaneous mating with multiple males reduces fertilisation success in the myobatrachid frog Crinia georgiana Proceedings of the Royal Society of London, Series B 266, 717-721 Byrne, P.G & Whiting, M.J (2008) Simultaneous polyandry increases fertilisation success in an African foam-nesting treefrog Animal Behaviour 76, 1157-1164 Emlen, S.T & Oring, L.W (1977) Ecology, sexual selection, and the evolution of mating systems Science 197, 215-223 Hawkes, K & Bird, R.B (2002) Showing off, handicap signalling, and the evolution of men's work Evolutionary Anthropology 11, 58-67 In Brief (2012) Want sex but too puny to get it? New Scientist 19/5,

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


p15 Jasarevic, E et al (2012) Spatial navigation strategies in Peromyscus: A comparative study Animal Behaviour 84, 1141-1149 Lande, R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters Evolution 34, 292-305 Lane, J.E et al (2009) Sexually selected behaviour: Red squirrel males search for reproductive success Journal of Animal Ecology 78, 296-304 Marmet, J et al (2012) Factors affecting male and female reproductive success in a chipmunk (Tamias sibiricus) with a scramble competition mating system Behavioural Ecology and Sociobiology 66, 1449-1457 Parker, G.A (1970) Sperm competition and its evolutionary consequences in insects Biological Review 45, 525-567 Payne, R.J.H (1998) Gradually escalating fights and displays: The cumulative assessment model Animal Behaviour 56, 651-662 Pradham, G.R et al (2012) A model of the evolution of developmental arrest in male orangutans American Journal of Physical Anthropology 149, 1, 18-25 Reading, K.L & Backwell, P.R.Y (2007) Can beggars be choosers? Male mate choice in a fiddler crab Animal Behaviour 74, 867-872 Rillich, J et al (2007) Assessment strategy of fighting crickets revealed by manipulating information exchange Animal Behaviour 74, 823-836 Tarvin, K.A & Murphy, T.G (2012) It isn't always sexy when both are bright and shiny: Considering alternatives to sexual selection in elaborate monomorphic species Ibis 154, 439-443 van Rooij, E.P & Griffith, S.C (2012) No evidence of assortative mating on the basis of putative ornamental traits in long-tailed finches Poephila acuticauda Ibis 154, 444-451 Webster, M (2012) Fickle fairies Scientific American November, p16

Zahavi, A (1975) Mate selection: Selection for a handicap Journal of Theoretical Biology 53, 205-214

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1



4.1. 4.2. 4.3. 4.4. Pro-social behaviour experiments Co-operation/teamwork Appendix 4A - Massen et al (2010) References

4.1. PRO-SOCIAL BEHAVIOUR EXPERIMENTS Pro-social behaviour is "any behaviour performed by one individual to alleviate another's need or improve their welfare" (Cronin 2012), and a clear evolutionary explanation for its origin is hard to establish. The study of pro-social behaviour in experiments with non-human primates has mainly used two paradigms (Cronin 2012): a) Pro-social choice task - An individual ("donor") is offered a choice of a reward for themselves and another individual ("recipient") (known as 1/1) or just a reward for themselves (1/0). There is no difference in effort between the choices, so donors that choose 1/1 more than 1/0 are showing pro-social behaviour (and 1/0 more often are not pro-social). There is also 0/1 (where the donor receives nothing and the recipient a reward) and 0/0 (control condition - no reward for either party). b) Out-of-reach task - A needed object is placed out of reach of the recipient, but is within the reach of the donor. Does the donor give the object to the recipient (with no gain for themselves)? If so, this is pro-social behaviour. In the control condition, the object is not needed. In the pro-social experiments, a number of variables have been explored (Cronin 2012): i) The social relationship between the donor and the recipient. Reciprocal altruism (Trivers 1971) explains the evolution of pro-social behaviour between individuals in a close social relationship. Help is given on one today and returned on another day by individuals who live together, for example. For example, de Waal et al (2008), using a version of the pro-social choice task with capuchin monkeys, found more 1/1 (compared to 1/0) choices when the donor and recipient were in a close relationship (kin and nonkin). Where dominant and subordinate individuals were used
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 37

in the experiments, the results are varied in terms of pro-social behaviour up or down the dominance hierarchy. Other than chimpanzees, primates show more pro-social behaviour down the hierarchy. In other words, a dominant individual is more pro-social towards a subordinate one than vice versa (eg: Massen et al 2010; appendix 4A). One explanation is that such behaviour by the dominant animal is a honest signal of their dominance (Cronin 2012) 28. ii) The behaviour of the recipient. In the out-of-reach task the recipient can express their desire for the object through vocalisations or reaching out towards it. Pro-social behaviour here, the perception action mechanism (PAM) model (Preston and de Waal 2002) explains through emotional contagion. The expressed need of the recipient spreads to the donor which motivates them to be pro-social. In experiments with different primates, expressing need sometimes produces pro-social behaviour, sometimes not, and the effect can wane during the experiment. Where there is a direct request to the donor, chimpanzees do show pro-social behaviour. For example, Yamamoto and Tanaka (2009) placed the donor and recipient in side-by-side booths with a lever the donor could press to give a reward to the recipient. The recipient could physically nudge (pushing on shoulder) the donor (direct request) and this produces pro-social behaviour. iii) Features of the task. In the situation where the reward is food for the recipient but nothing for the donor (eg: 0/1 version of pro-social choice task), the presence of food could produce competitive and selfish behaviour (and less prosocial behaviour). Experiments have, thus, compared prosocial behaviour when the food reward is visible or hidden. Chimpanzees are not pro-social when food is the visible reward (eg: choosing 1/0 more than 1/1 in prosocial choice tasks), but do show the behaviour where the food is hidden (Cronin 2012). Capuchin monkeys, for example, are less competitive about food. Lakshminarayanan and Santos (2008) offered the donor the choice of visible high-value food for themselves and for

Zahavi (1995) argued that altruism is a product of the handicap principle. The individual is saying that they are so healthy/strong etc that they can afford to help others at their own expense. For example, among Arabian babblers (Turdoides squamiceps), the dominant birds display their good quality by sentinel duty, fighting predators, and giving food to subordinates (Zahavi 1990). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 38


the recipient (1/1) or visible high-value food for themselves and low-value for the recipient (variations on 1/0). Donors chose 1/1 more often than 1/0. iv) Pro-social behaviour produces inequity. Donors will not be pro-social if it produces a disadvantageous inequity (ie: recipient gains more than donor). Fletcher (2008) offered the choice of 1/1 or 1/3 (donor gets one piece of food while recipient gets three), and the former was preferred. Table 4.1 summarises the findings for three species used in the pro-social experiments.

CHIMPANZEES Close relationship between donor & recipient Donor higher in dominance hierarchy than recipient Recipient expresses interest in object Recipient directly requests object No /No/ No /No



/No X

( = increases pro-social behaviour; No = no effect; = reduces; X = no research) (Source: Cronin 2012 table 1 p1091)

Table 4.1 - General findings on pro-social behaviour in three species. 4.2. CO-OPERATION/TEAMWORK Co-operation (or "teamwork") between individual animals is of mutual benefit. It can be facilitated by physical intimacy (eg: grooming, preening, mating) or vocal intimacy ((eg: choruses, synchronised calls) (Roughgarden 2012). Teamwork produces a physiological reinforcement called "pleasure", which is indirectly fitness-enhancing. "A participant is hypothesised to 'feel good' if other participants feel good too. Each participant is further hypothesised to feel even better if it can accomplish some task jointly rather than individually. Thus, the act of co-operation itself is hypothesised to be pleasurable. That is, a participant is hypothesised not only to feel good if other participants feel good, but to feel extra good if its welfare is increased through a co-operative action. The pursuit of social pleasure is hypothesised to
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 39

motivate animals to cooperate" (Roughgarden 2012 p1454) 29 . Roughgarden (2012) used a payoff matrix to show the benefits of co-operation between two birds in terms of guarding the nest and foraging for food (figure 4.1). Situation D is the worst option (ie: both guard nest) both for each bird individually and together (combined score), while situation B is best when co-operating (total = 15). This involves Bird 2 foraging while Bird 1 guards. Situation C is also a reasonably good strategy for co-operation. The point is that an individual bird could not achieve both foraging and guarding. It is also important that one bird trusts the other to carry out their side of the bargain, and this is where "pleasure" reinforces the co-operative relationship.
BIRD 1 Forage BIRD 2 Forage Guard 2/6 (A) 4/8 (C) 10/5 (B) 0/0 (D) Guard

(Source: Roughgarden 2012 appendix)

Figure 4.1 - Payoff matrix for two birds. There are variations on co-operation where individuals are not directly working together. For example, "vacancy chain" behaviour, where an individual claims a "more desirable possession abandoned by another individual" (eg: hermit crabs and larger shells) (Chase 2012). The resource must have three properties for this to happen - a coveted resource that is hard to get; the resource is only available to one individual/family at a time; and it cannot be taken unless vacant (Chase 2012). Asynchronous vacancy chain is when one individual at a time checks out the resource, while the synchronous version is when individuals queue up to examine a resource. Sea urchins are prey to ornate wrasse (Thalassoma pevo) (who eat the tube feet) and a starfish (Marthesterias glacialis). But the latter is too slow to catch the prey, and the wrasse cannot get at the feet buried in the sea bed. Nicola Galasso and others reported


This feeling of "pleasure" will only evolve if it enhances the evolutionary fitness of the individual animal (Roughgarden 2012). 40

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

"teamwork" between the two predators. The starfish attacks the sea urchin, which moves away, thereby exposing its tube foot. The wrasse attacks this, and the sea urchin is disabled for the starfish (In Brief 2011). 4.3. APPENDIX 4A - MASSEN ET AL (2010) Long-tailed macaques (Macaca fascicularis) (figure 4.2) have a clear dominance hierarchy and are viewed as a "despotic species" (Massen et al 2010). Pro-social behaviour up the hierarchy (subordinates to dominants) could be similar to grooming, or down the hierarchy as a way for dominants to maintain or enhance their status (Massen et al 2010).

(Source: Eric Bajart)

Figure 4.2 - Adult long-tailed macaque. Massen et al (2010) studied ten male and ten female macaques at a colony at the University of Utrecht in the Netherlands using the pro-social choice task method. An individual could choose a reward for themselves only (option A in figure 4.3; asocial option) or for themselves and a neighbouring individual (option B in figure 4.3; pro-social option). The relationship between the two monkeys was varied on dominance and kin.

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


The drawing shows the subject in the middle compartment having the choice between either granting itself and its partner (in compartment three) access to a banana (choice B, the "pro-social" choice), or granting only itself access to a banana and leaving a banana in front of an empty compartment (compartment one) (choice A, the "asocial" choice). (Source: Massen et al 2010 figure 1)

Figure 4.3 - Drawing of two monkeys in the experiment. The macaques chose the pro-social option significantly more often with neighbouring kin than nonkin. Among non-kin, higher ranking individuals chose the pro-social option more often with subordinate neighbours than vice versa. There was a negative correlation between ranking of macaque (with 1 for dominant animal) and "prosocial tendency" (preference for pro-social option when neighbour present compared to when alone - control condition) (figure 4.4). "Hence, Machiavellian macaques rule not through "fear above love", but through "be feared when needed and loved when possible" (Massen et al 2010). However, the authors admitted: "Alternatively, it may be that not an individual's high dominance rank leads to its pro-social behaviour, but that the pro-social behaviour of an individual has lead it to achieve such a high dominance rank. For male long-tailed macaques it has already been suggested that not only their strength, but also their social capacities influence their position within a dominance hierarchy...".

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


Pro-social tendency (difference between the preference for partner side in the test condition and the preference for the same side in the control condition) and absolute rank number (nr 1 is the alpha male) of all subjects towards kin (open circles and dotted line) and non-kin (closed circles and full line). Lines indicate linear regressions significant at the p<0.05 level. (Source: Massen et al 2010 figure 3)

Figure 4.4 - Pro-social tendency and rank. 4.4. REFERENCES

Chase, I (2012) Life is a shell game Scientific American June, 60-63

Cronin, K.A (2012) Pro-social behaviour in animals: The influence of social relationships, communication and rewards Animal Behaviour 84, 10851093 de Waal et al, F.B.M (2008) Putting the altruism back into altruism: The evolution of empathy Annual Review of Psychology 59, 279-300 Fletcher, G.E (2008) Attending to the outcome of others: Disadvantageous inequity aversion in male capuchin monkeys (Cebus apella) American Journal of Primatology 70, 901-905 In Brief (2011) Wrasse and starfish join forces to catch dinner New Scientist 3/9, p18 Lakshminarayanan, V.R & Santos, L.R (2008) Capuchin monkeys are sensitive to others' welfare Current Biology 18, R999-R1000 Massen, J.J.M et al (2010) Generous leaders and selfish underdogs: Pro-sociality in despotic macaques PLoS ONE 5, 3, e9734 (Freely available at Preston, S.D & de Waal, F.B.M (2002) Empathy: Its ultimate and

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


proximal bases Behavioural and Brain Sciences

25, 1-20

Roughgarden, J (2012) Teamwork, pleasure and bargaining in animal social behaviour Journal of Evolutionary Biology 25, 1454-1462 Trivers, R.L (1971) The evolution of reciprocal altruism Quarterly Review of Biology 46, 35-57 Yamamoto, S & Tanaka, M (2009) Do chimpanzees (Pan troglodytes) spontaneously take turns in a reciprocal co-operation task? Journal of Comparative Psychology 123, 242-249 Zahavi, A (1990) Arabian babblers: The quest for social status in a co-operative breeder. In Stacey, P.B & Koenig, W.D (eds) Co-operative Breeding in Birds: Long-Term Studies of Ecology and Behaviour Cambridge: Cambridge University Press Zahavi, A (1995) Altruism as a handicap - the limits of kin selection and reciprocity Avian Biology 26, 1-3

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1



5.1. Magnetic sense 5.2. Appendix 5A - Magnetic sense in one or two eyes 5.3. References 5.1. MAGNETIC SENSE Animal navigation using magnetic fields has been reported in birds (most notably, homing pigeons), monarch butterflies, sea turtles, lobsters, ants, and whales (among others) (Castelvecchi 2012) 30. The earth is a "huge magnet" with magnetic field lines that leave the ground at the magnetic south pole, curve around the earth, and re-enter the ground at the magnetic north pole. Thus "the magnetic field lines point upward on the southern hemisphere, run parallel to the earth's surface at the magnetic equator and point downward in the northern hemisphere" (Wiltschko and Wiltschko 2005) (figure 5.1). The magnetic inclination (the angle between the local magnetic vector and the horizontal) changes throughout the globe (from -90 at the southern magnetic pole to +90 at the northern magnetic pole, and 0 at the magnetic equator) 31. The intensity of the geomagnetic field also varies from high at the poles to low at the magnetic equator (Wiltschko and Wiltschko 2005). Animals can use this information in two ways - the direction of the magnetic field lines as a compass (magnetic orientation), and the intensity and/or inclination as a map (magnetic orientation) (Wiltschko and Wiltschko 2005). a) Magnetic orientation. Migratory birds have been studied here because even captive ones show a preference for a certain direction during the migratory season. An artificial magnetic field can be created using Helmholtz coils, which moves the magnetic north and then the behaviour of the birds is observed. For example, Cochran et al (2004) showed the use of

Wiltschko and Wiltschko (2005) listed 47 species including nine of insects, 5 crustaceans, 5 fish, 20 bird and 3 mammal species known to use a "magnetic compass". 31 "Poleward" - magnetic field lines point to ground (northern hemisphere). "Equatorward" - point upward (southern hemisphere). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 45




((a) Source: US Geological Survey; in public domain. (b) Based on Wiltschko and Wiltschko 2005 figure 1 p676)

Figure 5.1 - Magnetic field of the earth. magnetic cues by thrushes in an experiment that created an artificial magnetic field which pointed east (instead of north). Eighteen birds released at night from this special cage flew west (instead of the normal south migration) (figure 5.2). But they subsequently corrected their path the next night, which suggested that the "magnetic compass" is recalibrated every day.

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


Figure 5.2 - Migration direction in natural and experimental situations. Birds seem to have an "inclination compass" which means that they do not distinguish between magnetic north and south, but between poleward and equatorward, and the intensity of the field (Wiltschko and Wiltschko 2005). But salmon and rodents, for example, have a "polarity compass" (ie: use magnetic north and south in navigation) (Wiltschko and Wiltschko 2005). b) Magnetic navigation. The variations in magnetic intensity can be used in navigation. For example, knowing that the magnetic intensity increases towards north, an animal experiencing intensity greater than at home would head south (Wiltschko and Wiltschko 2005). Magnetic variations can also act as "sign-posts" to change direction. For example, pied flycatchers (Ficedula hypoleuca) in central Europe initially migrate to the southwest, but when they experience the magnetic field of north Africa, they change to a southeasterly direction. This is an innate behaviour 32, which means the birds end up travelling around the Alps, the Mediterranean Sea, and the central Sahara desert rather than through them (Wiltschko and Wiltschko 2005).

For birds that migrate from hemisphere to hemisphere, a simple "instruction" is always applicable eg: "when the days get shorter, start out heading equatorward". This would apply in autumn (September-November) in the northern hemisphere and in March-May (autumn in the southern hemisphere). Hand-raised birds without ever seeing celestial cues (eg: star constellations) show this behaviour suggesting that it is innate (Wiltschko and Wiltschko 1996). Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 47


Magnetic information works with other cues (eg: sun stars) in birds. For example, small coils placed on the heads of homing pigeons in order to artificially change the direction of magnetic north had little effect in sunlight, but did cause a change of direction under overcast skies (Wiltschko and Wiltschko 1996). Finding the physiological components of a "magnetic sense" has proved controversial, and includes three main hypotheses for birds (Keary and Bischof 2012): i) Magnetic particles in beaks of pigeons, for example, that are moved by the forces of the magnetic field ("magnetite hypothesis") (eg: Hanzlik et al 2000). ii) Magnetic particles in the lagona organ in the inner ear (eg: Harada et al 2001). iii) The protein cryptochrome, in the retina of some birds which reacts chemically to the earth's magnetic field ("photoreceptor-based magnoreceptors") (eg: Ritz et al 2000) 33. 5.2. APPENDIX 5A - MAGNETIC SENSE IN ONE OR TWO EYES Subsequent research to Ritz et al (2000) on the light-dependent photo-pigments suggested that this process occurred only in the right eye, and involved a specialised forebrain region (called Cluster N) in the left hemisphere in European robins (Erithacus rubecula) and Australian silvereyes (Zosterops lateralis) (eg: Wiltschko et al 2002; robins). This idea of hemispheric lateralisation of the magnetic sense has been questioned. Engels et al (2012) argued that it would "seem counterproductive from an evolutionary perspective. The survival of a bird having a magnetic compass located exclusively in its right eye would be more easily affected by eye-infection or monocular damage than a bird having a functional magnetic compass in both eyes". Furthermore, cryptochromes (the molecule involved in the magnetic sense) are found in both eyes, and Cluster N in both hemispheres of the brain (eg: garden warblers (Sylvia borin) and European robins). Hein et al (2011) showed that European robins could orientate using the magnetic compass with both eyes open, only the right eye open, and only the left one open. Healthy birds (both eyes open) migrate southwesterly. Then eye-covers made of light-tight, artificial leather


There has been some debate over whether this ability occurs in both eyes or only one (appendix 5A). 48

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1

were used to blind one eye. Whether the right eye was open or the left eye, the birds still flew southwesterly. The researchers kept the birds in an artificial magnetic field (counter-clockwise 120). This means that the direction of migration would be north-east. Birds using both eyes, or one eye only flew in that direction (figure 5.3).

(AB: European robins equipped with eye covers with a hole in front of both eyes, CD: birds equipped with eye covers allowing light and visual input to reach only the right eye, EF: birds equipped with eye covers allowing light and visual input to reach only the left eye. The data in A, C, and E were collected in an unchanged magnetic field (NMF). The data in B, D, and F were collected in a magnetic field turned 120 counter clockwise (CMF). mN = magnetic North) (Source: Engels et al 2012 figure 1)

Figure 5.3 - Directions of flight in Hein et al (2011). Wiltschko et al (2011) criticised this experiment. They argued that the birds may orientate with the right eye in the spring migration (when Wiltschko et al 2002 did their experiment), but not in the autumn migration (when Hein et al 2011 did their experiment). "The rationale behind this explanation relates to the fact that the birds might to a higher degree rely on learned map-based information on their way home in spring than on their way out in autumn" (Engels et al 2012). Engels et al (2012) found that robins studied in Germany could orientate with their left eye only in the autumn and spring migrations (figure 5.4). The researchers concluded that "the notion of a strong right eye lateralisation of the magnetic compass of migratory
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 49

songbirds... cannot be supported by double-blind, independent experiments performed in our lab" (Engels et al 2012).

(European robins equipped with eye covers allowing light and visual input to reach only the left eye were tested in autumn (A, B) and spring (C, D). The data in A and C were collected in an unchanged magnetic field (NMF). The data in B and D were collected in a magnetic field turned 120 counter clockwise (CMF). mN = magnetic North) (Source: Engels et al 2012 figure 2)

Figure 5.4 - Directions of flight in Engels et al (2012). In these experiments the direction of flight is measured using an Emlen funnel (figure 5.5) (Emlen and Emlen 1966) rather than actually releasing the birds. The funnel is coated with scratch sensitive paper on which the birds leave scratches (or ink stains if their feet are covered in ink) as they try to move in a certain direction. Then two researchers independently determine a bird's mean preferred direction of movement (which is assumed to be the way they would fly given the opportunity) (Engels et al 2012).
Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1


(Source: L Shyamal; in public domain)

Figure 5.5 - The Emlen funnel. 5.3. REFERENCES

Castelvecchi, D (2012) The compass within Scientific American January, 36-41 Cochran, W.W et al (2004) Migrating songbirds recalibrate their magnetic compass daily from twilight cues Science 304, 405-408 Emlen, S.T & Emlen, J.T (1966) A technique for recording migratory orientation of captive birds Auk 83, 361-367 Engles, S et al (2012) Night-migratory songbirds possess a magnetic compass in both eyes PLoS ONE 7, 9, e43271 (Freely available at Hanzlik, M et al (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons Biometals 13, 325-331 Harada, T et al (2001) Magnetic materials in otoliths of bird and fish laguna Acta Oto-larryngologica 121, 590-595 Nature Hein, C.M et al (2011) Robins have a magnetic compass in both eyes 471, e11-e12

Keary, N & Bischof, H.J (2012) Activation changes in zebra finch (Taeniopygia guttata) brain areas evoked by alterations of the earth magnetic field PLoS ONE 7, 6, e38697 (Freely available at Ritz, T et al (2000) A model for photoreceptor-based magnetoreception in birds Biophysical Journal 78, 707-718 Wiltschko, W & Wiltschko, R (1996) Magnetic orientation in birds Journal of Experimental Biology 199, 29-38 Wiltschko, W & Wiltschko, R (2005) Magnetic orientation and magnetoreception in birds and other animals Journal of Comparative Physiology A 191, 675-693 Wiltschko, W et al (2002) Lateralisation of magnetic compass orientation in a migratory bird Nature 419, 467-470 Wiltschko, W et al (2011) Wiltschko et al reply Nature 471, e12-e13

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1