animal behaviour advantages disadvantages no3

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.3

Kevin Brewer ISBN: 978-1-904542-68-1

Animal Behaviour: Advantages and Disadvantages No.3; Kevin Brewer; 2013 ISBN: 978-1-904542-68-1 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. SEXUAL COERCION AND CHEATING 4 1.1. Sexual selection and coercion 1.2. Forced copulation 1.3. Cheating for sex 1.4. References 2. PARENTAL CARE 18 2.1. Parental care strategies 2.2. Length of parental care 2.3. Appendix 2A - Egg dumping 2.4. Appendix 2B - Filial cannibalism 2.5. References 3. REPRODUCTIVE STRATEGIES AND SUCCESS 27 3.1. Scramble competition 3.2. Polyandry 3.3. Choosiness 3.4. Appendix 3A - Handicap and ornaments 3.5. Appendix 3B - Male-male competition 3.6. References 4. PRO-SOCIAL BEHAVIOUR AND CO-OPERATION 37 4.1. Pro-social behaviour experiments 4.2. Co-operation/teamwork 4.3. Appendix 4A - Massen et al (2010) 4.4. References 5. MAGNETIC CUES IN ANIMAL NAVIGATION 45 5.1. Magnetic sense 5.2. Appendix 5A - Magnetic sense in one or tw o eyes 5.3. References


1. SEXUAL COERCION AND CHEATING 1.1. Sexual selection and coercion 1.2. Forced copulation 1.3. Cheating for sex 1.4. References 1.1. SEXUAL SELECTION AND COERCION Sexual selection (as proposed by Charles Darwi n in 1871) is the idea that males and females have evolv ed different optimum reproductive strategies. Males generally benefit most from copulation with multipl e partners and providing limited or no parental care for offspring. Females invest more resources in reprodu ction, 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 be tween the sexes, and coercion by males with "an evolution ary arms race where males evolve better armament and fe males evolve improved defences" (Dukas and Jongsma 2012). In other words, males can benefit from coercion more t han females. EXAMPLE - Male mates with ten females, who have one offspring each in the breeding season OFFSPRING STRATEGY MALE 10 fathered; can Find many female mates; afford some not ie: indiscriminat e; little to survive concern for post- natal care FEMALE Each female has Female invests ti me and effort one offspring in survival, but must exercise and thus survival choosiness about male; ie: only important mate with male wh o has "best genes" Table 1.1 - Sexual selection and strategies for mal es 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 (Agl ais urticae) fly after females tapping them with their antennae until the female lands to allow mating (Cl utton-Brock and Parker 1995). There are costs to the fema les


which induce them to mate (eg: chased by male and u nable to feed). Harassment (or repeated courtship) has costs t o both sexes in terms of reduced feeding time, energy expe nded, and risk of predation. Specifically, females face t he cost of competing males injuring them in inter-male fights, or "over-zealous mating" (eg: male sea otte rs hold mates by nose with teeth or claws; Clutton-Bro ck and Parker 1995). There are thus advantages for females to be part of a harem of a dominant male. For example, fe ral 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 fem ales with their antlers (Clutton-Brock and Parker 1995). Observations of primates (eg: gorillas) have reported that aggressive males have more willing fe males (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 (Cl utton-Brock and Parker 1995). Such male aggression is more common in social species living in groups of multiple males and fema les. Here aggression helps the male to maintain exclusiv ity over the female. Male aggression is less likely in monogamous species and in harem groups (Clutton-Bro ck and Parker 1995). iii) Forced copulation. Usually the males of the species are stronger which facilitates this. For example, among orang-utans (P ongo pygmaeus) observed, up to half of copulations occur red 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 competitio n from other males if the individual waits (Clutton-Brock and Parker 1995). Forced copulation is very rare in species wher e a single male controls access to a group of females (harem). In this situation, the male waits until th e females are ready to mate, and the females tend not to resist (Clutton-Brock and Parker 1995).

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


The "evolutionary arms race" related to coerci on sees males evolve "weapons", like increased body si ze and strength 2, to enhance the ability to forcibly mate 3, while female evolve defences, like genitalia modifications that stop forced copulation or increa sed 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 stra tegies to combat harassment and intimidation including (Cl utton-Brock and Parker 1995): � Avoid areas where males congregate. � Become part of the harem of a dominant male - eg: s uch

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 th e

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 ev olve 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 forcib ly mated had significantly fewer offspring than female s who consensually mated, and had higher rates of wing da mage and premature death. The forced copulation took pla ce before the females were sexually mature (teneral 4) (day

2 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).


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 compar ed to all virgins, and this accounts mostly for the reduc ed number of offspring as a group. There were four conditions to the experiment (figure 1.2). Males who forcibly mated sired significantly l ess offspring than consensually mating males mainly bec ause forced matings were more likely to be fertile (ie: females were sexually immature). Forced copulation with sexually immature femal es is not a mistake by males because these females have a different odour to sexually mature females. But, sa y Dukas and Jongsma (2012): "In a setting where the r atio of sexually receptive females to males is close to zero, persistently pursuing young, sexually ambiguous conspecifics may be an optimal male strategy in spi te of the little expected fitness gain" (p1182).

(Source: Botarus; in public domain)

Figure 1.1 - Drosophila melanogaster.


Figure 1.2 - Four conditions in Dukas and Jongma's (2012) experiment 1. Dunn et al (1999) reported limited reproductiv e benefits for males from forced extra-pair copulatio ns among Lesser Snow geese (Chen caerulescens caerules cens) (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 s ixteen ten-minute sampling periods in June 1993 and 1995 5. In total, 65 copulations were observed, of which 32 (5 1%) were extra-pair among these monogamous species. All the extra-pair copulations appeared forced as the femal es made loud vocalisations in attempting to resist whe n she was on her nest (the majority of occasions - over t hree-quarters) , 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.

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


The DNA fingerprinting from blood samples of 5 0 families of geese found that forced extra-pair copulations led to few young (less than 5%). This i s a low fertility rate for approximately one-third of attempted forced copulations being successful (base d on the male appearing to make cloacal contact with the female - ie: tail of male twisted underneath the ta il 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 signif icant increases in reproductive success" (Dunn et al 1999 p1079).

Figure 1.4 - Breakdown of copulations observed. Forced extra-pair copulations have not been re ported 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 gees e (Dunn et al 1999). Male birds use a number of cues to establish i f the female is fertile. These include female behaviours like nest building and egg laying 7, or male behaviours like

6 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).


mate-guarding. Low (2004) found that male stitchbir ds (Notiomystis cincta) (figure 1.5) are sensitive to increased female weight as seen in her flight behav iour (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 Z ealand (where all the birds are ringed and artificial nest boxes are provided). Females gained about one-third body weight in the twenty days before egg laying. Extra-pair copulatio ns (as measured by intrusions into another male's territor y) tended to be forced as the females actively resiste d 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

8 78% of extra-pair copulations observed were forced (Low 2004). 9 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.


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 counte red by the evolution of control of fertilisation by female s including delaying egg and sperm combination. This strategy works for internal fertilisation, but not external fertilisation. For example, in frogs the m ale attaches himself to the back of the female and hold s on (amplexus) 12 (figure 1.6); this leads to a batch of eggs being laid which he then fertilises externally. Fem ale frogs have evolved strategies to counter the stimul ation of amplexus to lay eggs including behaviours to sto p 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.

12 The male grasps the female around the middle until the eggs are released for several hours to weeks (Purves et al 1997).


Forced copulation can occur between species th at are similar (heterospecifics), though the offspring may not be viable. Hettyey et al (2009) found that, among two clo sely related species of European brown frogs (Rana dalma tina; RD; figure 1.7; and Rana temporaria; RT), females w ould lay a smaller clutch of eggs when amplexus from a m ale of the other species. This tended to cause the male to release, and the female had some opportunity to fin d a male of their own species (conspecific) in that bre eding season (though repeated egg laying is relatively ra re).

(Source: H Krisp)

Figure 1.7 - Rana dalmatina. The two species of frogs, found in central Eur ope, are "explosive breeders", which means that they hav e short breeding seasons that are a "free for all". M ales mate indiscriminately with their own and other spec ies, 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 s eason in March 2008. RD females were found in the experim ents 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 hour s).


During this time it was possible that a RD male cou ld force off the RT male (takeover), or the RT male ma y 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 sa me 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 reprodu ctive tactics (ARTs) - ie: different strategies to gain a ccess to mates by males (and females) of the same species . For example, males of a species may invest effort in bu ilding a nest to attract a female ("classical" or "bourgeo is tactic"), while other males will not build nests bu t 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 o ne 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 (satellite s) (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 satelli te tactic in that case (energetic constraint hypothesi s). Alternatively, some males will always use the sneak ing tactic because of low fighting ability or unattract ive calls, for example (inherent disadvantage hypothesi s) (Brepson et al 2012). However, this strategy only works if a minority of frogs are "satellites" or "satellites" on some night only. Ot herwise, the chorus would fall silent. Varying between calling a nd "satelliting"

13 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).


is evidence of an "evolutionary stable strategy" (E SS) (Maynard Smith 1976). "Satelliting" is a good strategy, though, fo r smaller, and for younger males. "Satellite" behaviour (or parasitic behaviour) has been found in many species of frogs. Usually silent males close t o the chorus waiting to intercept approaching females. There are variations on this behaviour: a) medium-sized Bullfrog males will infiltrat e the territory of larger males, who are mating, in order to call (Mau ger 1988); b) "satellite" males calling in unison to int erfere with the female's ability to find the chosen male (Ovaska an d Hunte 1992); c) "satellites" chase amplexing pairs and att empting to remove the male, with limited success in African leaf-fold ing frogs (Blackwell and Passmore 1991); d) silent "satellite" behaviour has also been observed in larger males in order to save energy or avoid preda tors who hunt by sound (Perrill and Magier 1988). Table 1.2 - Variations on satellite behaviour. Brepson et al (2012) investigated experimental ly the use of satellite behaviour by male European treefro g (Hyla arborea) (figure 1.8). Males of this species call for long periods of the night as part of a chorus t o attract females. One hundred males captured near Ly on, 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.

16 A recording of ten males with no male louder.


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 "c aller" (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 disadvant age hypothesis) - It was found that smaller males (base d on snout-vent length and weight) were more likely to a dopt satellite behaviour. ii) Males deprived of food will use it (energe tic constraint hypothesis) - Half the frogs were fed an d half were not for seven days before the experiment. Ther e was no difference between them in use of satellite beha viour 17. iii) Males confronted by an attractive competi tor will use it - Calls were played over the loudspeake r from an attractive and an unattractive competitor. Males were more likely to show satellite behaviour if an attra ctive call was played than an unattractive one.

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

17 Brepson et al (2012) explained this unexpected finding as due the food deprivation not been long enough.


The findings support the idea that male frogs use satellite behaviour on a permanent basis, in the ca se of small individuals, and switch, in the case of havin g an attractive competitor. 1.4. REFERENCES Bateson, W & Brindley, H.H (1892) On some ca ses of variation in secondary sexual characters, statistically examined Proceedings of the Zoological Society of London 60, 585-594 Backwell, P & Passmore, N (1991) Satellite beh aviour in the leaf-folding frog, Afrixalis delicatus Journal of Herpet ology 25, 497-498 Brepson, L et al (2012) Cheating for sex: In herent 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: Me liphagidae) Ibis 138, 765-771 Clutton-Brock, T.H & Parker, G.A (1995) Sexu al coercion in animal societies Animal Behaviour 49, 1345-1365 Darwin, C (1871) The Descent of Man, and Sel ection in Relation to Sex London: John Murray Dukas, R & Jongsma, K (2012) Costs to female s and benefits to males from forced copulations in fruit flies Animal Behav iour 84, 1177-1182 Dunn, P.O et al (1999) Forced copulation res ults in few extra-pair fertilisations in Ross's and lesser snow geese Anim al Behaviour 57, 1071-1081 Ewen, J.G & Armstrong, D.P (2002) Unusual se xual 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 Academ y of Sciences, USA 77, 6937-6940 Hettyey, A et al (2009) Counter-strategies b y female frogs to sexual coercion by heterospecifics Animal Behaviour 78, 1365-1372 Jones, G (1986) Sexual chases in sand martin s (Riparia riparia): Cues for males to increase their reproductive success Be havioural Ecology and Sociobiology 19, 179-185 Low, M (2004) Female weight predicts the tim ing of forced copulation attempts in stitchbirds, Notiomystis cincta Animal Behaviour 68, 637-644 Mauger, D (1988) Observations on calling behav iour of bullfrogs in relation to male mating strategy Bulletin of Chicag o Herpetological Society 23, 57-59 Maynard Smith, J (1976) Evolution and the theo ry 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) Experime ntal demonstration of alternative mating tactics of male Ptilothrix fruct ifera (Hymenoptera, Apidae) Animal Behaviour 80, 241-247 Ovaska, K & Hunte, W (1992) Male mating behavi our of frog Eleutherodactylus johnstonei (Leptodacxtylidae) in Barbados, West Indies


Herpetologica 48, 40-49 Perrill, S & Magier, M (1988) Male mating beha viour 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 As pects of Social Evolution Princeton, NJ: Princeton University Press Seto, M (2000) A natural history of rape (bo ok review) Animal Behaviour 60, 5, 705-706 Thornhill, R & Sauer, K.P (1991) The notal o rgan of the scorpionfly (Panorpa vulgaris): An adaptation to coerce mating Behavioural Ecology 2, 2, 156-164


2. PARENTAL CARE 2.1. Parental care strategies 2.2. Length of parental care 2.3. Appendix 2A - Egg dumping 2.4. Appendix 2B - Filial cannibalism 2.5. 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 t rade-off in terms of the parental care given to offsprin g. For example, a mother who guards the newly laid eggs re duces her opportunities to forage and mate again, but des ertion risks predation of the vulnerable eggs waiting to h atch 18. This is a balance of viability and fecundity. The latter term relates to the number of fertilised egg s, and viability is the fertilised egg's chances of surviv ing (table 2.1). FECUNDITY VIABILITY EVOLUTI ONARY STRATEGY FISH High Low Many eg gs laid but few sur vive (parental car e less important) MAMMAL Low High Few or single eggs fertili sed but most survive (parent care imp ortant) 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 materna l care include egg hiding (leaving the eggs but they are h idden 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

18 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).


desertion (Chelini and Machado 2012). No maternal care or permanent brood desertion has advantages for the mother in the following situatio ns (Chelini and Machado 2012): � Mother able to raise another brood in same breeding

season. � Maternal care reduce "reproductive value" (eg: agei ng

and loss of attraction to males). � High fecundity - ie: opportunity for many offspring . Chelini and Machado (2012) reported the benefi ts of temporary brood desertion by a species of spider (harvestman, Neosadocus maximus (Gonyleptidae)) in Brazil. A clutch of eggs is laid on the undersurfac e of a leaf. They are vulnerable to predation from ants, f or example, but egg guarding by the female costs in te rms of no food and dehydration 19. Predation was higher at night (mean: six eggs vs 2 in day), so mothers who left t he 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 occur s in only a few species. Some males who egg guard are ab le to protect multiple broods simultaneously, so their opportunities to mate are not reduced by paternal c are. In the species where exclusive paternal care exists , females should prefer such males. In other words, m ales already guarding one brood of eggs will be attracti ve to females as this is an honest signal of the male's quality. "From the females' perspective, paternal c are may be favoured by sexual selection because it offe rs 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" (Requen a et al 2009). Among the species of harvestman (Iporangaia pustulosa (Gonyleptidae: Progonyleptoidellinae)), f ound in Brazil, females lay their eggs on the underside of leaves for the male to guard. Though the hatching p rocess takes about forty days, other females add to the br ood and the guarding period can last more than four mon ths (figure 2.1). Males sometimes temporarily desert fo r up to 48 hours (Requena et al 2009).

19 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.


(Source: Requena et al 2012)

Figure 2.1 - (A) Male Iporangaia guarding eggs. (B) Eggs at different stages of development (as shown by num bers).


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 pred ation of eggs was recorded for broods with a male guard a nd without. In the latter case, fifteen of sixteen clu tches had been predated (with six completely eaten) compa red 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. T hus 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 gua rd. Over four days 40% of "no mucus" eggs were eaten co mpared to 10% of "mucus" eggs. There was no male guard in either condition of this experiment. The mucus coating pro tects the eggs against predation, and is a strategy as th e female cannot be entirely sure that the male will n ot 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 fema le guards the eggs. There was a care and no care condi tion. The loss of eggs in the "no care" condition of Acut isoma was highest (80%). This may be because the eggs of this species are not covered by a mucus coating. Importa ntly, 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 a s efficiently as females". Manica and Johnstone (2004) found similar leve ls of success in egg guarding between two species of assa ssin bug - Rhinocoris tristis (paternal care) 30.4% of clutches had egg mortality, and Rhinocoris carmelit a (maternal care) 34.4% of clutches. 2.2. LENGTH OF PARENTAL CARE How long for a parent to nest guard, for examp le? 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 perio d is the opposite. Catry et al (2006) were interested in the cues used by grey-headed albatrosses (Thalassarche chrysastom a)


(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 Ch ick"), 12 day-old chicks were replaced by six day-olds (co mpared to a control group where a 12 day-old was switched for another twelve day-old). In the "Large Chick" condi tion, a 6 day-old chick was replaced by a 12 day-old one (along with a control group that replaced one 6 day-old wi th 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 behavio ur based on the new chick - ie: stay longer in the Sma ll Chick condition and go earlier in the Long Chick condition than the controls. But if the parents use d their body resources as a cue, they will not alter their length of stay at the nest.


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 condi tion, parents significantly extend their brood guarding b y a mean of 1.4 days more than their controls (mean tot al: 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) (m ean total: 22.6 vs 23.8 days). In fact, Catry et al (2006) felt that an "inte rnal 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 we re 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, salama nders, fish, and insects (Tallamy 2005). Eggs can be left with other eggs of the same species (conspecifics) or an other similar species (heterospecifics). Egg dumping has evolved as a compromise betwee n the costs of not guarding the eggs (ie: high loss) and the costs of guarding (ie: loss of future reproductive


opportunities). For example, maternal protection of eggs impro ved 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 t hem earlier in life (Tallamy 2005).

(Source: bugguide.net)

Figure 2.4 - Gargaphia solani. Among insect species where egg dumping is comm on, females may both dump eggs and act as a guard of eg g masses (a collection of different females's eggs). For example, a treehopper (Polyglupta dispar) female ob served 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. F emales who used the "dump, then guard" strategy had a life time


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. F or example, burying beetles lay their eggs in a dead c arcass (territory), which are in short supply and so femal es fight fiercely over them. Defeated females stay nea rby and sneak their eggs in with those of the territori al 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 indiv idual risk of predation (dilution effect). Also dumped eg gs 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 centr e of the mass (Tallamy and Horton 1990). 2.4. APPENDIX 2B - FILIAL CANNIBALISM Filial cannibalism has been reported in some b irds, 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 numbe r, there is an increased opportunity for survival of t he remainder ("selective brood reduction") (Thomas and Manica 2003). Thomas and Manica (2003) reported filial canni balism in the assassin bug (Rhinocoris tristis), where the mle guards the eggs of multiple females against parasit ic 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 male s did not lose weight because they consumed eggs on the o utside of the brood (which were more likely to be parasiti sed by wasps). Thomas and Manica (2003) offered three reasons for filial cannibalism by egg-guarders, particularly ma les: a) To remove damaged/diseased eggs - eg: femal e mouthbrooding cichlid (Pseudocrenilabrus multicolor )

20 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).


swallow unfertilised eggs after spawning. b) To increase the brood's attractiveness to f emales - eg: female garibaldi damselfish (Hypsypops rubicu ndus) prefer to add eggs to young broods, and so males co nsume older eggs. c) To benefit the guarding parent now (ie: abi lity to guard more effectively) and later (ie: ability t o 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 b e left unattended? Animal Behaviour 72, 383-391 Chelini, M.C & Machado, G (2012) Costs and b enefits of temporary brood desertion in a Neotropical harvestman (Arachnida: O piliones) Behavioural Ecology and Sociobiology 66, 1619-1627 Eberhard, W.G (1986) Possible mutualism betw een females of the sub-social membracid Polyglypta dispar (Homoptera) Beha vioural Ecology and Sociobiology 19, 447-453 Fowler, A & Hohmann, G (2010) Cannibalism in wild bonobos (Pan paniscus) at Lui Kitale American Journal of Primato logy 72, 6, 509-514 Manica, A & Johnstone, R (2004) The evolutio n of parental care with overlapping broods American Naturalist 164, 517-530

Requena, G.S et al (2009) Efficiency of unip arental male and female care against egg predators in two closely related s yntopic harvestmen Animal Behaviour 78, 1169-1175 Requena, G.S et al (2012) Paternal care decr eases foraging activity and body condition, but does not impose survival co sts to caring males in a Neotropical Arachnid PLoS ONE 7, (10), e46701 (Freely available at http://www.plosone.org/article/info%3Adoi%2F10.1371 %2Fjournal.pone.0046701 ) Tallamy, D.W (2005) Egg dumping in insects A nnual Review of Entomology 50, 347-370 Tallamy, D.W & Horton, L.A (1990) Costs and benefits of the egg-dumping alternative in Gargaphia lace bugs (Hemipte ra: Tingidae) Animal Behaviour 39, 352-359 Thomas, L.K & Manica, A (2003) Filial cannib alism in an assassin bug Animal Behaviour 205-210


3. REPRODUCTIVE STRATEGIES AND SUCCESS 3.1. Scramble competition 3.2. Polyandry 3.3. Choosiness 3.4. Appendix 3A - Handicap and ornaments 3.5. Appendix 3B - Male-male competition 3.6. References 3.1. SCRAMBLE COMPETITION The dispersion of females in a species can det ermine the mating strategy used by males. Where the female s 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 character istics 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 appeara nce between males and females of the species). If females are spatially dispersed, males will employ a scramble competition mating system (eg: so me insects and rodents). This is where males look for females who are sexually receptive. Sexual selectio n will favour in males characteristics that aid the locati on of mates (eg: sensitivity of smell, acuity of hearing) 22. Such species may be monomorphic (ie: little differe nce in appearance between sexes). One animal that shows scramble competition mat ing is a squirrel called the Siberian chipmunk (Tamias sib iricus 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 ann ual 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 a nd June, females are sexually receptive for 1-2 days. This is signalled by a distinctive female call, which ca uses the males to congregate around the female.

22 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).


(Source: Illustrierter Leitfaden der Naturgeschicht e 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 chanc e of meeting females as they moved around the range. For example, one male's large range overlapped with nin e females' ranges compared to only two females in a s maller range. Ten males with larger ranges in semi-open oa k 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 hectare s). Where males are "hunting" for females, there m ay 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 cl ose together). For example, male meadow voles (Microtus pennsylvanicus), who compete by searching for multi ple females in the breeding season, have enhanced spati al abilities over females, and over male and female pr airie voles (Microtus ochrogaster), who share home ranges with their mate (Jasarevic et al 2012). The spatial abilities, like memory retention a nd use of spatial cues, are usually tested in laboratory


experiments with mazes (eg: speed or number of erro rs in finding escape holes). Using this method, Jasarevic et al (2012) comp ared 26 deer mice (Peromyscus maniculatus bairdii) (figu re 3.2) who use mate searching, and 21 California mice (Peromyscus californicus insignis) who do not, on t he Barnes maze (Barnes 1979). This is a circular maze with twelve possible escape holes (of which only one lea ds back to the home cage), and four cues (triangle, sq uare, circle, and square shapes) on the maze wall. The ac tual escape hole was varied by random assignment for eac h mouse. There were two trials per day for seven days during which the speed of escaping and number of er rors were measured. It was expected that in the early tr ials the escape would take longer, but later the mouse s hould 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 cor rect escape hole when released than female conspecifics and California mice (figure 3.3). The speed to reach th e escape hole was significantly faster for male than female deer mice (mean: 33 vs 81 seconds).


Figure 3.3 - Percentage of mice going directly to c orrect 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 forc ed by males, but it can also be voluntarily. If it is the latter, what are the benefits to the female? The mo st important is the guarantee of fertilisation (known as the fertilisation insurance hypothesis; Parker 1970). O ther benefits include multiple parental care or protecti on from infanticide as the males cannot be sure if the y are the father or not. Polyandry has been reported in over a dozen sp ecies of frogs (anuran amphibians) (Byrne and Whiting 200 8). In some cases, it is not beneficial - eg: West Austral ian myobatrachid frog (Crinia georgiana) (Byrne and Rob erts 1999). Polyandrous females had less fertilisation s uccess 24 than single-male maters (monogamous). This may hav e been because of the fierce competition between male s interferes with mating (eg: mating position for spe rm 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) stu died this frog at the Tsonga Kraal Dam, South Africa in 2006-7. The percentage of eggs fertilised within a clutc h and the total number of eggs fertilised were each significantly positively correlated with the number of males mated by the female. The mean overall fertili sation rate was 64%, but this was only 54% for monogamous females. For example, where six to eight males were

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


observed to mate with the female, fertilisation suc cess was closer to 70%. 3.3. CHOOSINESS Sexual selection is primarily based on male-ma le competition (appendix 3B) and female choice. The fe male of the species decides between competing males tryi ng 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 w here the reverse occurs. Where males invest a lot in mat ing, they can choose between females. Male investment in cludes lengthy courtship, prolonged mate guarding, sperm depletion, or brood guarding, which limit his futur e reproductive success. "If these costs are high, sel ection should favour the allocation of mating effort towar ds those females capable of providing maximum reproduc tive gains" (Reading and Backwell 2007 p867). Male choosiness exists where the benefits of m ating with a highly fecund female outweighs mating indiscriminately with many females. This situation occurs if the quality of females (eg: clutch size) is high ly variable. Choosiness is also influenced by the operation al 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 female s, then female choosiness exists and males mate indiscriminately, but the opposite if there are mor e females than males. The fiddler crab (Uca mjoebergi) (figure 3.4) exhibits signs of male choosiness. Females are high ly variable in body size (which correlates with fecund ity 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 Da rwin, 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 fe male.

25 Reading and Backwell (2007) reported a significant Pearson correlation of r = 0.59 from their observations in Australia in 2005-2006.


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

Figure 3.4 - Fiddler crab. Males in the mangroves of East Point Reserve w ere offered a choice of two different females tethered with cotton thread glued to a carapace fastened in the m ud - one large (top one-third of body size) and one smal l (bottom one-third). The choice was either simultane ous (180° apart) or sequential (with a ten-minute inter val). In the simultaneous condition, males spent signific antly 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 femal e was presented first, the males spent significantly more time courting and mating with her than the second smalle r female, but when the small female was presented fir st, the males spent as much time as with the second lar ger female. In the latter, an opportunist strategy seem ed to be at work. "Males never rejected mate-searching fe males, regardless of their size...While males may preferen tially court large females, they will not forego a mating opportunity with a small female. This is not surpri sing since the highly male-biased OSR means that males a re 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 courtshi p to the potential benefits gained" (Reading and Backwel l 2007 p871).

26 A mean of 20 waves per 5-minute period towards the large female and 9 towards the small female (p0.05).


3.4. APPENDIX 3A - HANDICAP AND ORNAMENTS Male communication, whether by calling or phys ical behaviour and appearance, is a way of conveying the quality of genes. An honest signal is where "indivi duals 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" (Ha wkes and Bird 2002 p58). Only signals that are too costl y to fake are the reliable ones of honesty. Zahavi (1975 ) coined the term "the handicap principle" for the "w aste" (of energy) involved in honest signals of good qual ity 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 o f a species have ornaments (eg: cumbersome tails, brigh t colours) (Tarvin and Murphy 2012). The genetic correlation hypothesis (Lande 1980 ) explains the situation where the females have subdu ed versions of the males' ornaments (eg: parulid warbl ers). Both sexes carry the genes for the ornaments, but o nly 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, female -female competition for sexual and non-sexual resour ces (eg: food) could lead to their evolution. Another explanation is called "assortative pairing". Female s prefer the most elaborate males while the males simultaneously prefer the most elaborate females (T arvin and Murphy 2012). van Rooij and Griffiths (2012) struggled to fi nd evidence for benefits of ornaments in both sexes re lated to sexual selection in long-tailed finches (Poephil a 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 signalli ng role of the traits they measured is now redundant w ith other traits, or alternatively, the function of the traits may vary geographically and thus be importan t in some areas but not others. In essence, the costs an d benefits associated with expressing and/or attendin g to

27 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.


ornamentation may change over time or space..." (Ta rvin and Murphy 2012 p441). The ornaments could be "badges of status" or predator deterrent signals. "For example, both sexe s could use ornaments as socially selected status sig nals to mediate competition (within and between sexes) f or access to non-sexual resources such as food or terr itory. As this type of signal does not necessarily increas e mating success (and therefore is not considered a f orm of sexual selection) it is unlikely to lead to assorta tive pairing" (Tarvin and Murphy 2012). 3.5. APPENDIX 3B - MALE-MALE COMPETITION Male-male competition can involve physical fig hting, 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, def ence or appeasement) (Rillich et al 2007). There are a number of theories to explain the decision to fight or escape including (Rillich et a l 2007): � Mutual assessment hypothesis - an individual assess es

their RHP relative to that of their opponent. � Own RHP-dependent persistent hypothesis - no assess ment

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 las t theory in experiments with Mediterranean crickets (Gryllus bimaculatus). Two male crickets were place d, each time, at opposite ends of a small glass arena, and the level of aggression was scored 0-6 depending ho w far the fight went. For example, level 6 was categorise d as "grappling" - "at this stage an all-out fight ensue s, during which the animals may repeatedly disengage, struggle for position, bite other body parts, and r e-engage mandibles to push or overthrow the opponent with the assistance of the foreleg claws" (p825). The researchers manipulated aspects of the cri ckets including disabled mandibles or blinded by black pa int.


Contests were either symmetrical (both opponents ha d 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 ea ch 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 aggressiv e 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 avera ge 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 20 07).

Figure 3.5 - Percentage of symmetrical pairings tha t became physical fights. 3.6. REFERENCES Barnes, C.A (1979) Memory deficits associate d 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) Simultaneou s mating with multiple males reduces fertilisation success in the myobatra chid frog Crinia georgiana Proceedings of the Royal Society of Londo n, Series B 266, 717-721 Byrne, P.G & Whiting, M.J (2008) Simultaneou s polyandry increases fertilisation success in an African foam-nesting tr eefrog Animal Behaviour 76, 1157-1164 Emlen, S.T & Oring, L.W (1977) Ecology, sexu al selection, and the evolution of mating systems Science 197, 215-223 Hawkes, K & Bird, R.B (2002) Showing off, ha ndicap 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,


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 se lection, and adaptation in polygenic characters Evolution 34, 292-305 Lane, J.E et al (2009) Sexually selected beh aviour: Red squirrel males search for reproductive success Journal of Animal E cology 78, 296-304 Marmet, J et al (2012) Factors affecting mal e and female reproductive success in a chipmunk (Tamias sibiricus) with a scr amble 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 fig hts and displays: The cumulative assessment model Animal Behaviour 56, 651-662 Pradham, G.R et al (2012) A model of the evo lution of developmental arrest in male orangutans American Journal of Physi cal Anthropology 149, 1, 18-25 Reading, K.L & Backwell, P.R.Y (2007) Can be ggars 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 Anima l Behaviour 74, 823-836 Tarvin, K.A & Murphy, T.G (2012) It isn't al ways sexy when both are bright and shiny: Considering alternatives to sexua l selection in elaborate monomorphic species Ibis 154, 439-443 van Rooij, E.P & Griffith, S.C (2012) No evi dence of assortative mating on the basis of putative ornamental traits i n long-tailed finches Poephila acuticauda Ibis 154, 444-451 Webster, M (2012) Fickle fairies Scientific American November, p16 Zahavi, A (1975) Mate selection: Selection f or a handicap Journal of Theoretical Biology 53, 205-214


4. PRO-SOCIAL BEHAVIOUR AND CO-OPERATION 4.1. Pro-social behaviour experiments 4.2. Co-operation/teamwork 4.3. Appendix 4A - Massen et al (2010) 4.4. References 4.1. PRO-SOCIAL BEHAVIOUR EXPERIMENTS Pro-social behaviour is "any behaviour perform ed by one individual to alleviate another's need or impro ve their welfare" (Cronin 2012), and a clear evolution ary explanation for its origin is hard to establish. The study of pro-social behaviour in experimen ts with non-human primates has mainly used two paradig ms (Cronin 2012): a) Pro-social choice task - An individual ("do nor") 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 rewa rd) and 0/0 (control condition - no reward for either p arty). b) Out-of-reach task - A needed object is plac ed out of reach of the recipient, but is within the reach of the donor. Does the donor give the object to the recipi ent (with no gain for themselves)? If so, this is pro-s ocial behaviour. In the control condition, the object is not needed. In the pro-social experiments, a number of var iables have been explored (Cronin 2012): i) The social relationship between the donor a nd the recipient. Reciprocal altruism (Trivers 1971) explains th e evolution of pro-social behaviour between individua ls in a close social relationship. Help is given on one t oday and returned on another day by individuals who live together, for example. For example, de Waal et al (2008), using a ver sion of the pro-social choice task with capuchin monkeys , found more 1/1 (compared to 1/0) choices when the d onor and recipient were in a close relationship (kin and non-kin). Where dominant and subordinate individuals wer e used


in the experiments, the results are varied in terms of pro-social behaviour up or down the dominance hiera rchy. Other than chimpanzees, primates show more pro-soci al behaviour down the hierarchy. In other words, a dom inant 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 exp ress their desire for the object through vocalisations o r reaching out towards it. Pro-social behaviour here, the perception action mechanism (PAM) model (Preston an d de Waal 2002) explains through emotional contagion. Th e expressed need of the recipient spreads to the dono r which motivates them to be pro-social. In experiments with different primates, expres sing need sometimes produces pro-social behaviour, somet imes 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 examp le, Yamamoto and Tanaka (2009) placed the donor and rec ipient in side-by-side booths with a lever the donor could press to give a reward to the recipient. The recipient co uld physically nudge (pushing on shoulder) the donor (d irect 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 versio n of pro-social choice task), the presence of food could produce competitive and selfish behaviour (and less pro-social behaviour). Experiments have, thus, compared pro-social behaviour when the food reward is visible or hidden. Chimpanzees are not pro-social when food is th e visible reward (eg: choosing 1/0 more than 1/1 in p ro-social choice tasks), but do show the behaviour whe re the food is hidden (Cronin 2012). Capuchin monkeys, for example, are less competitive about food. Lakshminarayanan and Santos (2008) offered the dono r the choice of visible high-value food for themselves an d for

28 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).


the recipient (1/1) or visible high-value food for themselves and low-value for the recipient (variati ons 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 o r 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 sp ecies used in the pro-social experiments.

( ↑ = 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 behaviou r in three species. 4.2. CO-OPERATION/TEAMWORK Co-operation (or "teamwork") between individua l 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 reinforcemen t called "pleasure", which is indirectly fitness-enha ncing. "A participant is hypothesised to 'feel good' if ot her participants feel good too. Each participant is fur ther hypothesised to feel even better if it can accompli sh some task jointly rather than individually. Thus, t he act of co-operation itself is hypothesised to be pleasu rable. That is, a participant is hypothesised not only to feel good if other participants feel good, but to feel e xtra good if its welfare is increased through a co-opera tive action. The pursuit of social pleasure is hypothesi sed to

CHIMPANZEES CAPUCHINS MACAQUES

Close relationship between donor & recipient

No ↑ ↑/No

Donor higher in dominance hierarchy than recipient

↑/No/ ↓ ↑/No ↑/No

Recipient expresses interest in object

No ↓ No

Recipient directly requests object

↑/No X X


motivate animals to cooperate" (Roughgarden 2012 p1 454) 29. Roughgarden (2012) used a payoff matrix to sho w 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 nes t) both for each bird individually and together (combi ned score), while situation B is best when co-operating (total = 15). This involves Bird 2 foraging while B ird 1 guards. Situation C is also a reasonably good strat egy for co-operation. The point is that an individual b ird could not achieve both foraging and guarding. It is also important that one bird trusts the other to carry o ut their side of the bargain, and this is where "pleas ure" reinforces the co-operative relationship. BIRD 1 Forage Guard BIRD 2 Forage 2/6 (A) 10/5 (B) Guard 4/8 (C) 0/0 (D) (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 indivi dual claims a "more desirable possession abandoned by an other individual" (eg: hermit crabs and larger shells) (C hase 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 2 012). Asynchronous vacancy chain is when one individual a t 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 (Thalass oma pevo) (who eat the tube feet) and a starfish (Marthesterias glacialis). But the latter is too sl ow to catch the prey, and the wrasse cannot get at the fe et buried in the sea bed. Nicola Galasso and others re ported

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


"teamwork" between the two predators. The starfish attacks the sea urchin, which moves away, thereby exposing its tube foot. The wrasse attacks this, an d the sea urchin is disabled for the starfish (In Brief 2 011). 4.3. APPENDIX 4A - MASSEN ET AL (2010) Long-tailed macaques (Macaca fascicularis) (fi gure 4.2) have a clear dominance hierarchy and are viewe d as a "despotic species" (Massen et al 2010). Pro-social behaviour up the hierarchy (subordi nates to dominants) could be similar to grooming, or down the hierarchy as a way for dominants to maintain or enh ance 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 f emale macaques at a colony at the University of Utrecht i n the Netherlands using the pro-social choice task method . An individual could choose a reward for themselves onl y (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 be tween the two monkeys was varied on dominance and kin.


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

Figure 4.3 - Drawing of two monkeys in the experime nt. The macaques chose the pro-social option significantly more often with neighbouring kin than non-kin. Among non-kin, higher ranking individuals chos e the pro-social option more often with subordinate neigh bours than vice versa. There was a negative correlation b etween ranking of macaque (with 1 for dominant animal) and "pro-social tendency" (preference for pro-social option when neighbour present compared to when alone - control condition) (figure 4.4). "Hence, Machiavellian macaques rule not throug h "fear above love", but through "be feared when need ed and loved when possible" (Massen et al 2010). However, the authors admitted: "Alternatively, it may be that no t an individual's high dominance rank leads to its pro-s ocial behaviour, but that the pro-social behaviour of an individual has lead it to achieve such a high domin ance rank. For male long-tailed macaques it has already been suggested that not only their strength, but also th eir social capacities influence their position within a dominance hierarchy...".


Pro-social tendency (difference between the prefere nce for partner side in the test condition and the preference for the same side in t he control condition) and absolute rank number (nr 1 is the alpha male) of all subject s towards kin (open circles and dotted line) and non-kin (closed circles and full l ine). 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 Scienti fic American June, 60-63 Cronin, K.A (2012) Pro-social behaviour in a nimals: The influence of social relationships, communication and rewards Ani mal Behaviour 84, 1085-1093 de Waal et al, F.B.M (2008) Putting the altr uism back into altruism: The evolution of empathy Annual Review of Psycholog y 59, 279-300 Fletcher, G.E (2008) Attending to the outcom e 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 for ces to catch dinner New Scientist 3/9, p18 Lakshminarayanan, V.R & Santos, L.R (2008) C apuchin 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 http://www.plosone.org/article/info%3Adoi%2F10.1371 %2Fjournal.pone.0009734 ) Preston, S.D & de Waal, F.B.M (2002) Empathy : Its ultimate and


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 recipro cal altruism Quarterly Review of Biology 46, 35-57 Yamamoto, S & Tanaka, M (2009) Do chimpanzee s (Pan troglodytes) spontaneously take turns in a reciprocal co-operati on 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 - th e limits of kin selection and reciprocity Avian Biology 26, 1-3


5. MAGNETIC CUES IN ANIMAL NAVIGATION 5.1. Magnetic sense 5.2. Appendix 5A - Magnetic sense in one or tw o eyes 5.3. References 5.1. MAGNETIC SENSE Animal navigation using magnetic fields has be en reported in birds (most notably, homing pigeons), m onarch butterflies, sea turtles, lobsters, ants, and whale s (among others) (Castelvecchi 2012) 30. The earth is a "huge magnet" with magnetic fie ld lines that leave the ground at the magnetic south p ole, 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 inclinat ion (the angle between the local magnetic vector and th e 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 (Wiltsc hko 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) (Wiltsc hko and Wiltschko 2005). a) Magnetic orientation. Migratory birds have been studied here because even captive ones show a preference for a certain direct ion during the migratory season. An artificial magnetic field can be created using Helmholtz coils, which moves t he magnetic north and then the behaviour of the birds is observed. For example, Cochran et al (2004) showed the u se of

30 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).


(a)

(b)

((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 cre ated an artificial magnetic field which pointed east (in stead of north). Eighteen birds released at night from th is special cage flew west (instead of the normal south migration) (figure 5.2). But they subsequently corr ected their path the next night, which suggested that the "magnetic compass" is recalibrated every day.


Figure 5.2 - Migration direction in natural and experimental situations. Birds seem to have an "inclination compass" wh ich means that they do not distinguish between magnetic north and south, but between poleward and equatorward, an d the intensity of the field (Wiltschko and Wiltschko 200 5). But salmon and rodents, for example, have a "polari ty compass" (ie: use magnetic north and south in navig ation) (Wiltschko and Wiltschko 2005). b) Magnetic navigation. The variations in magnetic intensity can be us ed in navigation. For example, knowing that the magnetic intensity increases towards north, an animal experi encing intensity greater than at home would head south (Wiltschko and Wiltschko 2005). Magnetic variations can also act as "sign-post s" to change direction. For example, pied flycatchers (Fi cedula hypoleuca) in central Europe initially migrate to t he southwest, but when they experience the magnetic fi eld of north Africa, they change to a southeasterly direct ion. This is an innate behaviour 32, which means the birds end up travelling around the Alps, the Mediterranean Se a, and the central Sahara desert rather than through them (Wiltschko and Wiltschko 2005).

32 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).


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 ch ange the direction of magnetic north had little effect i n sunlight, but did cause a change of direction under overcast skies (Wiltschko and Wiltschko 1996). Finding the physiological components of a "mag netic 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 magnet ic field ("magnetite hypothesis") (eg: Hanzlik et al 2 000). ii) Magnetic particles in the lagona organ in the inner ear (eg: Harada et al 2001). iii) The protein cryptochrome, in the retina o f some birds which reacts chemically to the earth's magnet ic field ("photoreceptor-based magnoreceptors") (eg: R itz et al 2000) 33. 5.2. APPENDIX 5A - MAGNETIC SENSE IN ONE OR TWO EYES Subsequent research to Ritz et al (2000) on th e light-dependent photo-pigments suggested that this process occurred only in the right eye, and involve d a specialised forebrain region (called Cluster N) in the left hemisphere in European robins (Erithacus rubec ula) and Australian silvereyes (Zosterops lateralis) (eg : Wiltschko et al 2002; robins). This idea of hemisph eric lateralisation of the magnetic sense has been quest ioned. Engels et al (2012) argued that it would "seem counterproductive from an evolutionary perspective. The survival of a bird having a magnetic compass lo cated 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 i n 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 southwesterl y. Then eye-covers made of light-tight, artificial lea ther

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


were used to blind one eye. Whether the right eye w as open or the left eye, the birds still flew southwes terly. The researchers kept the birds in an artificial mag netic field (counter-clockwise 120°). This means that the direction of migration would be north-east. Birds u sing both eyes, or one eye only flew in that direction ( figure 5.3).

(A–B: European robins equipped with eye covers with a hole in front of both eyes, C–D: birds equipped with eye covers allowing light and v isual input to reach only the right eye, E–F: birds equipped with eye covers allowing l ight and visual input to reach only the left eye. The data in A, C, and E were collecte d 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 (20 11). Wiltschko et al (2011) criticised this experim ent. They argued that the birds may orientate with the r ight eye in the spring migration (when Wiltschko et al 2 002 did their experiment), but not in the autumn migrat ion (when Hein et al 2011 did their experiment). "The rationale behind this explanation relates to the fa ct that the birds might to a higher degree rely on lea rned map-based information on their way home in spring t han 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 migra tory


songbirds... cannot be supported by double-blind, independent experiments performed in our lab" (Enge ls 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 c lockwise (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 i s measured using an Emlen funnel (figure 5.5) (Emlen and Emlen 1966) rather than actually releasing the bird s. The funnel is coated with scratch sensitive paper on wh ich the birds leave scratches (or ink stains if their f eet are covered in ink) as they try to move in a certai n direction. Then two researchers independently deter mine 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).


(Source: L Shyamal; in public domain)

Figure 5.5 - The Emlen funnel. 5.3. REFERENCES Castelvecchi, D (2012) The compass within Sc ientific American January, 36-41 Cochran, W.W et al (2004) Migrating songbird s recalibrate their magnetic compass daily from twilight cues Science 304, 405-408 Emlen, S.T & Emlen, J.T (1966) A technique f or recording migratory orientation of captive birds Auk 83, 361-367 Engles, S et al (2012) Night-migratory songb irds possess a magnetic compass in both eyes PLoS ONE 7, 9, e43271 (Freely available at http://www.plosone.org/article/info%3Adoi%2F10.1371 %2Fjournal.pone.0043271 ) Hanzlik, M et al (2000) Superparamagnetic ma gnetite 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 Hein, C.M et al (2011) Robins have a magneti c compass in both eyes Nature 471, e11-e12 Keary, N & Bischof, H.J (2012) Activation ch anges in zebra finch (Taeniopygia guttata) brain areas evoked by alterat ions of the earth magnetic field PLoS ONE 7, 6, e38697 (Freely available at http://www.plosone.org/article/info%3Adoi%2F10.1371 %2Fjournal.pone.0038697 ) Ritz, T et al (2000) A model for photorecept or-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 re ply Nature 471, e12-e13

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