Adolescent social environment shapes sexual and aggressive behaviour of adult male zebra finches (Taeniopygia guttata)

Adolescence is the pivotal transitional phase during which animals become sexually and socially mature and acquire the skills to cope with a variety of environmental challenges on their own. We investigated in a bird species, the zebra finch, how the social environment experienced during this period influences their behaviour in a sexual context. Zebra finches were kept in pairs (male–female or male–male) or larger mixed-sex groups (three males and three females) during adolescence and the long-term consequences were studied on courtship behaviour, aggressiveness and attractiveness in 42 males. To investigate the stability of the observed effects over time, all behavioural tests were repeated approximately 4 months after the initial recordings. Males that grew up with a single female showed the most intense courtship and highest aggressiveness and were most attractive to females, while group-reared males had the lowest courtship and aggressiveness and were the least attractive. The observed differences in courtship and aggressiveness were stable, while the differences in attractiveness disappeared over time. These findings are very similar to earlier studies on guinea pigs, indicating that the observed effects represent a general phenomenon, not restricted to mammals with a similar function and presumably also similar underlying mechanisms.     

Family-related differences in social foraging tactic use in the zebra finch (Taeniopygia guttata)

When animals forage in groups, they can search for food themselves (producer tactic), or they can search for opportunities to exploit the food discoveries of others (scrounger tactic). Both theoretical and empirical work have shown that group-level use of these alternative tactics is influenced by environmental conditions including group size and food distribution, and individual tactic use can be influenced by several measures of individual state, including body condition. Because body condition has been shown to be heritable for various species, social foraging tactics may also be heritable. We looked for evidence of heritability in social foraging tactic use in the zebra finch (Taeniopygia guttata) by testing whether: (1) natural variation in body condition correlates with tactic use, (2) there are family-related differences in body condition, and (3) there are family-related differences in observed tactic use. Tactic use in the zebra finch was significantly related to body condition; individuals with lower body condition scores had a significantly higher use of the scrounger tactic as predicted from variance-sensitive producer–scrounger models. Body-condition scores differed significantly between families, suggesting that this aspect of individual state may have a heritable component. Finally, we recorded significant family-related differences in the use of producer and scrounger alternatives. These results are consistent with heritability in observed tactic use resulting from an inheritance of individual state, in this case body condition, which itself influences tactic use. Understanding how and why individuals differ in their use of alternative tactics is fundamental as it may provide important insights into inter-individual variation in fitness.     

Social feedback and attractiveness in zebra finches

The attractiveness of an individual (i.e. its ability to arouse interest in a potential mate) has important implications for its reproductive success. However, attractiveness is not a fixed trait. Previous work has shown that male birds can adjust the intensity of their courtship display in response to variation in female behaviour, but little is known about how males adjust their behaviour during mate choice in response to social feedback about their own attractiveness independent of their intrinsic quality. Such information may help to maximize the potential mating success of males. Here, we provide experimental evidence that the amount of attention given by male zebra finches to females is dependent upon the manipulated attractiveness of males. This demonstrates that, in this socially monogamous species of bird, attractiveness of males could be considered to be a social construct, at least partially determined via social feedback from females.     

Androgen-dependent maternal effects on offspring fitness in zebra finches

There is accumulating evidence that maternal hormones may play a role in offspring sex adjustment, but little is known about the costs of such hormone-mediated mechanisms. Recent studies have reported sex-specific effects of hormones on offspring viability. Specifically, we previously found that elevating the plasma androgen level in mothers results in a male-biased offspring primary sex ratio, but it affects the viability of sons negatively and daughters positively in zebra finches (Taeniopygia guttata; Rutkowska and Cichoń, Anim Behav, 71:1283–1288, 2006). In this study, we studied further fitness consequences of exposure to elevated yolk androgen levels in zebra finches. We measured growth rate and cellular immune response of nestlings that hatched from eggs laid by females injected with testosterone during egg laying and nestlings of unaffected control females. We found that sons of testosterone-treated females grew slower in comparison to sons of control females. The significant interaction between experimental group and offspring sex indicates that sons of testosterone-treated mothers suffered impaired immune responsiveness while daughters seemed to benefit from elevated androgen level in terms of enhanced immune responsiveness. We found no effects of androgens on offspring performance at adulthood—neither fecundity of females nor attractiveness of males was affected. We conclude that the benefits of biasing sex ratio towards males by increasing androgen level in the yolk may be limited due to negative effects on male offspring performance early in life.     

Immunoregulatory activity of different dietary carotenoids in male zebra finches

Summary. Many animals use carotenoid pigments to color their integument and become sexually attractive. These colorants can also serve physiological functions, protecting cells and tissues from oxidative damage as well as stimulating the immune system. Because animals often acquire several different carotenoid pigments from their diet, there is the potential for different carotenoids to exhibit different free-radical-scavenging or immunoenhancing activity. We experimentally tested how two common dietary xanthophylls - lutein and zeaxanthin - may differentially affect the immune system in male zebra finches (Taeniopygia guttata). Male T. guttata derive their red sexual beak colorants from these two carotenoids, and prior studies with this species have shown that lutein and zeaxanthin together boost cell-mediated immunity. We experimentally elevated these two dietary carotenoids separately in two groups of non-breeding zebra finches, but found that lutein-supplemented and zeaxanthin-supplemented males mounted similar cell-mediated immune responses (to phytohaemagglutinin, or PHA). Although zeaxanthin is a more conjugated carotenoid than lutein and has the potential to be a more potent antioxidant, our study suggests that such a subtle structural difference between these two biochemicals does not differentially affect immune performance in this songbird.     

Parentally biased favouritism in relation to offspring sex in zebra finches

Family conflicts over parental care result in offspring attempting to exert control using solicitation behaviours, whilst the parents are potentially able to retaliate through provisioning rules. However, the evolutionary interests of one parent may not necessarily support the evolutionary interests of the other parent, and such conflicts of interest may be expressed in how the two parents allocate the same form of parental care to individual offspring. Theory suggests that such parentally biased favouritism is a universally predicted outcome of evolutionary conflicts of interest, and empirical evidence suggests that parentally biased favouritism occurs in relation to offspring size and solicitation behaviours. However, unequivocal empirical evidence of parentally biased favouritism in relation to offspring sex is absent, due to being strongly confounded by sex differences in size and solicitation behaviours. Here, we present strong evidence for parentally biased favouritism in relation to offspring sex in zebra finches (Taeniopygia guttata), independent of the effects of chick size and begging intensity. Mothers preferentially provisioned sons over daughters, whilst fathers showed no bias, meaning that sons received more food than daughters. Parentally biased favouritism in relation to offspring sex facilitates parental control over evolutionary conflicts of interest and is probably more widespread than previously realised.     

Carry-over effects of male extra-pair copulation opportunity on biparental effort in zebra finches

Whether parental effort can be negotiated between partners over ecological time and adjusted across different contexts is not well understood. We manipulated male extra-pair copulation (EPC) opportunity in captive zebra finches, Taeniopygia guttata, to test whether males adjust incubation effort to the mating context and to examine how females respond to their partner’s effort. Birds without previous breeding experience were paired randomly and bred with the same partner twice. In the first breeding attempt, half the males received EPC opportunities with ‘extra-pair females’ during incubation, while the other half did not. Males that received EPC opportunities in the first breeding attempt did not in the second breeding attempt and vice versa. We recorded incubation effort on days when EPC opportunities were not presented. In their first breeding attempt, males with EPC opportunities incubated less than those without. Females compensated fully for the deficit in male care so that a pair’s combined incubation effort was unchanged. In the second attempt, when a male’s opportunity for EPCs was switched, individuals showed the same level of incubation effort that they had previously, irrespective of the current availability of extra-pair females. This suggests that division of effort was negotiated in the first breeding attempt and maintained without significant adjustments in the second attempt. The effects of male EPC opportunity in the first breeding attempt on subsequent incubation effort suggests that individual parental decisions can be shaped by previous experience and this may partly explain conflicting results in studies where individuals’ histories were not known.     

Singing activity stimulates partner reproductive investment rather than increasing paternity success in zebra finches

Song is used as a signal in sexual selection in a wide range of taxa. In birds, males of many species continue to sing after pair formation. It has been suggested that a high song output after pair formation might serve to attract extra-pair females and to minimise their own partner’s interest in extra-pair copulations. A non-exclusive alternative function that has received only scant attention is that the amount of song might stimulate the own female’s investment into eggs in a quantitative way. We address these hypotheses in a captive population of zebra finches, Taeniopygia guttata, by relating male undirected song output (i.e. non-courtship song) to male egg siring success and female reproductive investment in two different set-ups. When allowed to breed in aviaries, males with the highest song output were no more attractive than others to females in an analysis of 4,294 extra-pair courtships involving 164 different males, and they also did not sire more offspring (both trends were against the expectation). When breeding in cages with two different partners subsequently, females produced larger eggs with more orange yolks when paired to a male with a high song output. These findings suggest that singing activity in paired zebra finch males might primarily function to stimulate the partner and not to attract extra-pair females.     

Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches

Several recent studies have tested the hypothesis that song quality in adult birds may reflect early developmental conditions, specifically nutritional stress during the nestling period. Whilst all of these earlier studies found apparent links between early nutritional stress and song quality, their results disagree as to which aspects of song learning or production were affected. In this study, we attempted to reconcile these apparently inconsistent results. Our study also provides the first assessment of song amplitude in relation to early developmental stress and as a potential cue to male quality. We used an experimental manipulation in which the seeds on which the birds were reared were mixed with husks, making them more difficult for the parents to obtain. Compared with controls, such chicks were lighter at fledging; they were thereafter placed on a normal diet and had caught up by 100 days. We show that nutritional stress during the first 30 days of life reduced the birds’ accuracy of song syntax learning, resulting in poorer copies of tutor songs. Our experimental manipulations did not lead to significant changes in song amplitude, song duration or repertoire size. Thus, individual differences observed in song performance features probably reflect differences in current condition or motivation rather than past condition.     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations.

When breeding diet is restricted, domesticated zebra finches,Taeniopygia guttata, produce male-biased primary and secondary sex ratios, but unexpectedly produce unbiased ratios when food is unrestricted. We investigated the primary sex ratios (at laying) of wild zebra finches in southeastern Australia in response to food supplementation and environmental factors predicted to enhance female breeding condition and to bias the primary sex ratio towards daughters. Molecular sexing of all nestlings in 54 complete broods where every egg hatched, failed to show any significant biases from random. Time of egg laying (month, season) and environmental conditions (rainfall, temperature) did not significantly predict variation in the primary sex ratio, but time of breeding did affect clutch size. Wild zebra finches at our colony did not bias their sex allocation as there were no differences in the primary sex ratio and no differences in the numbers and mass of sons and daughters at the end of parental care (day 35–40 post-hatch). Biases in primary sex ratio of our wild population are probably weak or non-existent possibly due to the unpredictable environment and/or multiple contrary selective forces acting on sex ratios. We also investigated the effects of photoperiod, biases in the adult sex ratio, and parental attractiveness on primary sex ratios of semi-domesticated, laboratory zebra finches. Molecular sexing of three-day old embryos from complete clutches, failed to reveal significant biases from random. In contrast to previous studies, sex of eggs did not correlate with laying order and egg mass declined with order, rather than increased. Domestication may be responsible for these differences.     

Searching behavior and use of sampling information by free-ranging bison (Bos bison)

I examined the searching behavior of free-ranging plains bison (Bos bison bison) in their natural habitat, and determined whether their assessment of food patch quality was influenced by the short-term sampling information acquired during search. Bison used area-concentrated search during their winter foraging activity. Their movements between areas of suitable food patches were influenced by local environmental conditions, being sometimes less sinuous, and at other times more sinuous, than expected from a correlated random walk model. Bison also systematically avoided digging in areas where plants of low profitability lay under the snow. Where they dug, there was evidence that a bison's perception of food quality varied during a foraging bout, and was therefore influenced by short-term sampling information. After controlling for forage quality, I found that small feeding craters were more likely to be preceded by samples of high quality food patches. My observations suggest that bison take advantage of the structural characteristics of their environment during searching activity, and base foraging decisions on local rather than global availability.     

Individual differences and within-flock convergence in chickadee calls

Summary A detailed sound analysis of the Chick-adee call of the black-capped chickadee (Parus atricapillus) was performed in order to determine a basis for individual recognition and for imitation within winter flocks. During the winter of 1978–1979 members of five free-living black-capped chickadee flocks were uniquely marked for individual identification, and their calls were recorded in the field. Nested analysis of variance of temporal call parameters measured from sonagrams and spectral parameters from frequency spectra showed that there were significant differences between individuals within flocks for every parameter measured. There were significant differences between flocks in the frequency ranges 800–2,200 Hz and 4,000–5,300 Hz, in the spectral parameters bandwidth and maximum frequency, and in the duration of the Dee syllable and total call duration.Members of four of the five flocks were captured in December 1978 and held in aviaries segregated by original flock membership. In January 1979 the memberships of the three aviaries were rearranged to form experimental flocks. After one month, there were significant differences among the experimental flocks in the duration of the Dee syllable and total call duration. Convergence, as indicated by a significant decrease in variance among members (F-test), occurred in the experimental flock in Aviary 1 and was concentrated in the frequency ranges 1,300–1,800 and 6,200–6,900 Hz. The members of this experimental flock differed from each other in the number of 100 Hz frequency intervals within which each changed its own call.The Chick-a-dee call contains sufficient information that it can potentially be used by black-capped chickadees for individual recognition. In addition, both field and aviary data suggest that flock members converge in some call characteristics. Possible explanations of the social significance of vocal convergence in chickadee flocks are discussed.     

Individual differences in the behavior of juvenile yellow-bellied marmots

Summary Yellow-bellied marmots express considerable individuality as measured by behavior in a maze, mirror-image stimulation (MIS), and social behavior in the field. Maze behavior discriminated between residents and dispersers; residents explored the maze more widely than did dispersers. Males could not be distinguished from females nor survivors from non-survivors by their maze behavior. A group of six yearling females was established to examine the relationship between individual behavioral phenotypes (as determined by MIS) and social behavior in the field. This experiment provided a situation in which social behavior was not influenced by age, sex, or reproduction (female yearlings are non-reproductive). The number of social interactions per individual ranged from 25 to 69. The number of observed interactions per individual differend significantly from the expected for greeting, allogrooming, total amicable, play, and total social interactions. Rankings of greeting, total amicable, and total interactions were directly correlated with rankings on the avoidance axis; play was inversely correlated with the approach axis. These results suggest that marmots have individual behavioral phenotypes that are expressed in their social interactions with their conspecifics.     

Vicarious sampling: the use of personal and public information by starlings foraging in a simple patchy environment

Group foragers may be able to assess patch quality more efficiently by paying attention to the sampling activities of conspecifics foraging in the same patch. In a previous field experiment, we showed that starlings foraging on patches of hidden food could use the successful foraging activities of others to help them assess patch quality. In order to determine whether a starling could also use another individual’s lack of foraging success to assess and depart from empty patches more quickly, we carried out two experimental studies which compared the behaviour of captive starlings sampling artificial patches both when alone and when in pairs. Solitary starlings were first trained to assess patch quality in our experimental two-patch system, and were then tested on an empty patch both alone and with two types of partner bird. One partner sampled very few holes and thus provided a low amount of public information; the other sampled numerous holes and thus provided a high amount of public information. In experiment 1, we found no evidence of vicarious sampling. Subjects sampled a similar number of empty holes when alone as when with the low and high information partners; thus they continued to rely on their own personal information to make their patch departure decisions. In experiment 2, we modified the experimental patches, increasing the ease with which a bird could watch another’s sampling activities, and increasing the difficulty of acquiring accurate personal sampling information. This time, subjects apparently did use public information, sampling fewer empty holes before departure when with the high-information partner than when with the low-information partner, and sampling fewer holes when with the low-information partner than when alone. We suggest that the degree to which personal and public information are used is likely to depend both on a forager’s ability to remember where it has already sampled and on the type of environment in which foraging takes place. Received: 31 January 1995/Accepted after revision: 11 September 1995     

Humans use social information to adjust their quorum thresholds adaptively in a simulated predator detection experiment

Quorum sensing is used in many biological systems to increase decision accuracy. In quorum sensing, the probability that an individual adopts a behavior is a nonlinear function of the number of other individuals adopting this behavior. From an optimal decision-making perspective, individuals should adjust their quorum threshold to the particulars of the decision problem. Recent work predicts that a key factor here is the quality of social information. In particular, it is predicted that individuals should adjust their quorum thresholds such that it lies in between the average true and false positive rate of the other group members. We here test this prediction with a predator detection experiment. First, human groups observed a group of animals (projected on a white screen) in which a predator was present or absent, and each individual made an independent decision to escape or not. Second, individuals received social information on the decisions of their group members, after which individuals decided again. This social information, however, did not represent their own decisions but consisted of responses that either came from a high-performing group (i.e., many individuals detecting the predator) or from a low-performing group (i.e., few individuals detecting the predator). We found that individuals adaptively adjust their quorum threshold to the quality of the social information: when receiving social information from high-performing groups, individuals employed higher quorum thresholds than when receiving information from low-performing groups. Our study demonstrates that humans can quickly evaluate the quality of publicly available information and adaptively adjust their decision rules.     

Individual differences in nest defense in the colonial breeding Black-tailed Gulls

Often in colonial seabirds, all colony members are believed to defend against nest predators and experience equal nest predation risk. However, the variation of defense behavior among members and its reproductive consequences are largely unknown. We investigated (1) individual variation in the nest defense of breeding Black-tailed Gulls Larus crassirostris against a natural egg predator, the Jungle Crow Corvus macrorhynchos and (2) how this behavioral variation affects an individual’s own nest predation risk and that of their neighbors. Results were compared between 2 years where crow attack levels were manipulated to average 5 and 22 times normal rates (“low” and “high” predation risk years, respectively) by the placement of varying numbers of artificial nests containing unguarded eggs at the perimeter of the gull colony. In both years, 23–38% of parents, mostly males, showed “aggressive” defense behavior (strikes or chases) against crows and decoys. Other “non-aggressive” gulls showed no defense. In the year of low predation risk, intrusion rates by crows (landing within 0.5 m of an individual gull’s nest) were similar for aggressive and non-aggressive gulls. In the year of high predation risk, however, the rates of intrusion for aggressive gulls (4%) and for non-aggressive gulls with an aggressive neighbor (37%) were significantly lower than for non-aggressive gulls without an aggressive neighbor (76%). These results indicate that aggressive individuals reduce nest predation risk for themselves and conspecific neighbors in a colonially breeding species.     

Mate-choice copying by female zebra finches, <Emphasis Type="Italic">Taeniopygia guttata</Emphasis>: what happens when model females provide inconsistent information?

For a long time, mate-choice copying was thought to be restricted to lekking and polygynous species. Yet, recent experimental studies revealed that social information can play a role in the evolution of mate preferences in monogamous species with biparental care. However, this phenomenon has been demonstrated only under particular conditions and the prevalence and importance of this phenomenon therefore remains to be evaluated. In particular, previous laboratory experiments have consisted in exposing test females to only one paired male at a time, while under natural conditions monogamous females are likely to observe the choice of several females before making a decision. Thus, in the present study, female zebra finches (Taeniopygia guttata) could observe two model females simultaneously, that provided either inconsistent or consistent information, depending on whether they were interacting with different types of males or with males of a same phenotype. We found that the relative importance given to private and social information on females’ preferences varied with the consistency of social information and females significantly changed their preference only when social information was consistent. There was, nevertheless, a large variation in their responses. We suggest that such variations could be due to the fact that the benefits of mate-choice copying are frequency-dependent, and that this constrain would further contribute to limit the use of social information in monogamous species.     

Manipulating the perceived opportunity to cheat: an experimental test of the active roles of male and female zebra finches in mate guarding behavior

Birds are commonly sexually promiscuous, which can lead to conflict between the sexes and the evolution of paternity assurance strategies, such as mate guarding. Adaptive explanations for mate guarding have tended to focus on fitness consequences for males, but mate guarding and participation in being guarded is also likely adaptive for females in certain contexts. To better understand the adaptive explanations for mate guarding as well as the observed variation in paternity patterns, it is necessary to explore the relative costs and benefits of guarding (and being guarded) from both the male and female perspective. To investigate these costs and benefits, we conducted an experiment with the Australian zebra finch (Teniopygia guttata) in which we independently varied the perceived opportunity for each member of a captive breeding pair to engage in extra-pair copulation (EPC) solicitation behavior; as an individual’s EPC opportunity increased, the partner’s EPC opportunity remained constant. Our results indicate that, for males, mate guarding intensity increases when their female’s EPC opportunity increases but decreases when their own (i.e., male) EPC opportunity increases. We did not find evidence of flexible female guarding behavior, but we found that females do not evade their partners more as female EPC opportunity increases.