Animal behaviour and cancer

Scientists are increasingly coming to realize that oncogenic phenomena are both frequent and detrimental for animals, and must therefore be taken into account when studying the biology of wildlife species and ecosystem functioning. Here, we argue that several behaviours that are routine in an individual's life can be associated with cancer risks, or conversely prevent/cure malignancies and/or alleviate their detrimental consequences for fitness. Although such behaviours are theoretically expected to be targets for natural selection, little attention has been devoted to explore how they influence animal behaviour. This essay provides a summary of these issues as well as an overview of the possibilities offered by this research topic, including possible applications for cancer prevention and treatments in humans.

Developmental stress and female mate choice behaviour in the zebra finch

The potential effects of early environmental conditions on adult female mate choice have been largely neglected in studies of sexual selection. Our study tested whether developmental stress affects the mate choice behaviour of female zebra finches, Taeniopygia guttata, when choosing between potential mates. In an experiment manipulating developmental condition, female zebra finches were raised under nutritional stress or control conditions. In adulthood, female preferences were assessed using extensive four-stimulus mate choice trials. Nutritional stress affected growth rates during the period of stress, with experimentally stressed females lighter than controls. During mate choice trials stressed females were almost three times less active than controls and made fewer sampling visits to the stimulus males, although we found no evidence of a direct effect of developmental experience on which males were preferred. Thus, developmental experience had a clear effect on behavioural patterns in a mate choice context. To test whether this effect is specific to a mate choice context, we also investigated the effect of developmental stress on female activity rates in three social contexts: isolation, contact with a conspecific male (a potential mate) and contact with a conspecific female. Here, female activity did not differ between the experimental treatments in any of the social situations. Overall, our findings suggest that environmental conditions during early development can have long-term context-dependent consequences for adult female mate choice behaviour, mediated by changes in activity rates.

The behaviour of a hawksbill turtle data-logged during the passage of hurricane Georges through the Caribbean

Recent severe hurricanes in the Caribbean and south-east United States have had devastating socio-economic effects, and there is a pressing need to learn how animals are impacted by such events. We serendipitously deployed a multi-channel data logger onto a hawksbill turtle (Eretmochelys imbricata) during the breeding season in 1998 and logged various aspects of her behaviour before, during and after passage of hurricane Georges. As Georges passed by, the turtle made shorter dives, became more active and spent less time at the surface between dives compared with its baseline, non-storm activity. However, after passage of the hurricane the turtle quickly resumed its pre-hurricane behaviour and nested successfully a few days later. These results show that, in this case, the hurricane had a minor impact on the submerged animal presumably because of the dampening effect of depth on high winds over water.

Synchronized group association in little penguins, Eudyptula Minor.

Most seabirds form groups on land and at sea, but there is little information whether seabird groups are formed deliberately or randomly. We investigated whether little penguins formed groups composed of the same individuals when they crossed the beach each day over four breeding seasons (2001–2004) using an automated penguin monitoring system (APMS). We used an association matrix to determine the number of times any two birds crossed the APMS in the same group. The number of these group associations or ‘synchronized parade’ behaviour was determined for every possible pair of individuals, giving a total association value for each pair of birds during the postguard stage of the reproductive cycle. We concluded that a penguin group was composed of 5–10 individuals within 40-s intervals. Penguin groups were formed nonrandomly in years of high breeding success (2002 and 2003), but not in years of low breeding success (2001 and 2004). Age of birds was a significant factor in composition of groups. Little penguins with higher association values shared similar characteristics or ‘quality’, which in turn may increase the functional efficiency of their groups, especially if they are also foraging together. However, low association indices indicated that seeking the same associates was not a priority. It is costly for any animal to synchronize their attendance with the same individuals, so it could be beneficial to display synchronized parade behaviour in good breeding years but it could result in intraspecific competition for food during poor breeding years.

Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus

Although 90% of passerine birds live in socially monogamous pair bonds, molecular studies have revealed that genetic polygamy occurs in 86% of surveyed passerines, because individuals engage in copulations outside the pair bond (extrapair copulations; EPCs). Most explanations for the occurrence of EPCs involve female gaining indirect benefits from the extrapair male. The sedge warbler is a socially monogamous species in which some offspring result from EPCs (8% in this study). Complex song is a sexually selected male trait used by females which select mates based on a variety of male qualities. We used microsatellite DNA profiling to detect extrapair young and assign paternity. ‘Good genes’ theory predicts that females should engage in EPCs with males of higher quality than their social mate, with resulting fitness benefits. Extrapair males had smaller song repertoires and smaller territories than the social mate. This apparent preference for small-repertoire males as extrapair mates conflicts with the predictions from previous studies of this species. Sudden cessation of song after pairing may mean that song cues are unavailable for later extrapair matings and females may switch to other cues. Such behaviour may lead to different patterns of female choice during social and extrapair mating in the sedge warbler. We conclude that multiple reasons underlie patterns of female choice in this species.

Song sharing and repertoire size in the sedge warbler, Acrocephalus schoenobaenus: changes within and between years

The complex song of the male sedge warbler functions mainly in sexual attraction and the evolution of repertoire size is driven primarily by female choice. As male song ceases upon pairing, male–male singing interactions are relatively brief and have not been studied to our knowledge. This study shows that young males in their first breeding season shared significantly more syllables with their nearest neighbour than with their fathers or more distant males. Moreover, daily recordings revealed that rapid learning and modification of syllable repertoires occurred, resulting in a progressive increase in sharing within just a few days. This does not lead to a gradual increase in repertoire size as some syllables are dropped and new ones are acquired. This turnover process allows males to share syllables with their neighbours, whilst repertoire size, known to be important in female choice, remains relatively constant in any one year. Individual males were followed for several years and also showed considerable syllable turnover between years. However, in this case, repertoire size was found to increase between years, the largest increase occurring between the first and second years. We obtained a significant positive correlation between repertoire size and age, suggesting that females choosing males with larger repertoires may gain indirect (genetic) benefits for their offspring, such as good genes for viability. Whilst these results reveal a more flexible picture of repertoire turnover than previously suspected, the relative stability of repertoire size within a season and the increase with age suggests that repertoire size remains a likely target for sexual selection by female choice.

Mate choice in zebra finches: does corticosterone play a role?

The importance of stress as a factor in influencing life history strategies has received considerable attention in recent years, because it appears to have a substantial impact on an individual's behaviour and physiology. Birds respond to environmental and social stressors by the production of corticosterone, a glucocorticoid hormone released by the adrenal gland. In this experiment, we tested whether female zebra finches preferred males selected to produce low or high peak levels of circulating plasma corticosterone. Plasma corticosterone and testosterone levels of the males were recorded, as were morphometric measurements and perch activity. Spectrophotometric measurements were also taken from several putatively sexually selected regions of the males. The females preferred the males from the low corticosterone lines to the high corticosterone males. In addition to, and consistent with this effect, females preferred males with the lowest corticosterone titres. Male activity, testosterone level, body size and mass had no effect on female preference. Leg and beak brightness were important, however, as were the brightness and chromaticity of the male cheek patch. These results are discussed in relation to contemporary hypotheses in sexual selection, particularly in the context of stress-mediated signalling.

Begging and provisioning of thin-billed prions, Pachyptila belcheri, are related to testosterone and corticosterone

Vigorous begging is usually seen as an expression of parent–offspring conflict over limited resources. Chicks signal need by begging, but the evolution of honest signals requires the signals to be costly. Although some possible costs have been identified, the cost-inducing mechanisms underlying this widely distributed signalling system remain unclear. Because hormones associated with stress and hunger (corticosterone) and aggressive behaviour (testosterone) have deleterious side-effects, signalling costs may be coupled to the expression of such hormones, if they are closely associated with the signal. We tested whether begging in chicks of thin-billed prions (Aves, Procellariiformes) is associated with secretion of corticosterone and testosterone. Prion chicks honestly signalled their nutritional state. Begging increased with decreased body condition, both within and between chicks. Adults responded to more intense begging by delivering larger meals. Chick testosterone levels were positively correlated with measures of begging intensity and the mean body condition of chicks was correlated positively with testosterone and negatively with corticosterone. In a cross-fostering experiment, the change in testosterone and corticosterone between control and experimental periods was positively correlated with the change in begging intensity. This is the first experimental evidence that the control of chick begging by endogenously produced testosterone and corticosterone may form a mechanism controlling parental provisioning in birds, and that chick behaviour can help to explain the variation in growth patterns between individual birds.

Testing the immunocompetence handicap hypothesis : a review of the evidence

The immunocompetence handicap hypothesis was formulated 12 years ago in an attempt to offer a proximate mechanism by which female choice of males could be explained by endocrine control of honest signalling. The hypothesis suggested that testosterone has a dual effect in males of controlling the development of sexual signals while causing immunosuppression. Our purpose in this review is to examine the empirical evidence to date that has attempted to test the hypothesis, and to conduct a meta-analysis on two of the assumptions of the hypothesis, that testosterone reduces immunocompetence and increases parasitism, to ascertain any statistical trend in the data. There is some evidence to suggest that testosterone is responsible for the magnitude of trait expression or development of sexual traits, but this is by no means conclusive. The results of many studies attempting to find evidence for the supposed immunosuppressive qualities of testosterone are difficult to interpret since they are observational rather than experimental. Of the experimental studies, the data obtained are ambiguous, and this is reflected in the result of the meta-analysis. Overall, the meta-analysis found a significant suppressive effect of testosterone on immunity, in support of the hypothesis, but this effect disappeared when we controlled for multiple studies on the same species. There was no effect of testosterone on direct measures of immunity, but it did increase ectoparasite abundance in several studies, in particular in reptiles. A funnel analysis indicated that the results were robust to a publication bias. Alternative substances that interact with testosterone, such as glucocorticoids, may be important. Ultimately, a greater understanding is required of the complex relationships that exist both within and between the endocrine and immune systems and their consequences for mate choice decision making.

The effect of flicker from fluorescent lights on mate choice in captive birds

The visual systems of birds are hypothesized to have higher temporal resolution than those of humans, suggesting that they may be able to perceive the flicker emitted from conventional low-frequency fluorescent lights (LF; 100 Hz in Europe, 120 Hz in the U.S.A.). These lights are commonly used in the housing of captive birds and this may affect both their welfare and performance in experiments. We carried out mate choice experiments on European starlings, Sturnus vulgaris, under both low- and high-frequency fluorescent lights (HF; > 30 kHz, at which flicker is imperceptible). Indicators of male condition and size, together with the reflectance spectra and length of the males' throat feathers, were also recorded to ascertain which variables correlated with female preference. Females ranked males consistently under HF, but not LF, lighting, and individual females chose different males under the two lighting types. Under HF lighting, females chose to spend more time with males that had longer throat feathers. The flicker rate of the light clearly affected the choices made by the females, possibly because of nonspecific stress effects or decreased discrimination ability. Our results imply that careful interpretation of mate choice experiments is needed, especially with regard to the lighting types used, to elucidate the real cause behind any variation shown. (c) 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.