Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

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.     

Social experience during adolescence influences how male zebra finches (Taeniopygia guttata) group with conspecifics

Group-living animals rely on social skills which ensure beneficial interaction and prevent harmful ones with conspecifics. In a previous experiment, we demonstrated that male zebra finches reared in groups during adolescence show consistently less courtship and aggressive behaviour as adults than pair-reared males. Here we tested whether such differences affect how they group with conspecifics, as an indicator of their social integration. Zebra finches were kept in pairs (male–female or male–male) or mixed-sex groups (three males and three females) during adolescence and were introduced to an established group of unknown conspecifics during adulthood. Male courtship and aggressive behaviour were quantified directly after introduction to the group and 48 h later. At the same time, male position in relation to other birds and the number of birds in proximity were recorded. Males that grew up in a small mixed-sex group during adolescence spent more time within groups, were observed in bigger groups and lost less weight than males raised in pairs, indicating that an enriched social environment during early development may facilitate social integration. However, we observed no differences in courtship and aggressive behaviour that could predict the differences in grouping behaviour of pair- and group-reared males. We discuss alternative explanations for the difference in grouping and how to test these in future research.     

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     

Individual differences in sampling behaviour predict social information use in zebra finches

When animals have to decide where to forage, what to eat or with whom to mate, they can base their decisions on either socially or personally acquired information. In accordance with theoretical predictions, there is experimental evidence that animals adjust the weight they give to both sources of information depending on circumstances. Notably, several studies have demonstrated that individuals rely more on social information when personal information is difficult to acquire or unreliable, because these conditions leave them uncertain as how to behave. Yet, even when individuals are exposed to the same conditions, they generally differ widely in the value they attribute to social and personal information. These differences suggest that the tendency to rely on social information would also depend on intrinsic characteristics that affect, for instance, individual efficiency in collecting personal information. To address this issue, we conducted laboratory experiments using female zebra finches (Taeniopygia guttata) and we tested them under three consecutive conditions. First, we evaluated their reliance on social information in a mating context and in a foraging context. Then, we measured their efficiency in acquiring personal information by recording their sampling behaviour when searching for hidden food. We found that females that sampled their environment less actively consistently relied on social information to a greater extent compared with those that invested more in sampling. Contrary to what is generally assumed, then, our study demonstrates that social information use is not entirely flexible and context dependent.     

Status,reproductive success and fitness in Cape mountain zebra (Equus zebra zebra)

Summary Demographic data relating to herd size and stability are given for a population of Cape mountain zebra (Equus zebra zebra) under longterm observation. Temporal dispersion patterns of male and female offspring differed and were independent of the mother's status. Dispersion in females appeared to be related to physiological state, and dispersion in both sexes was related to age rather than changes in parental behaviour. Reproductive success of dominant and subordinate mares was equal and independent of age and social and reproductive variables. Fitness of dominant mares, however, was significantly higher than that of subordinates, the latter having a higher foal mortality, part of which could be attributable to dominants' aggression. The fitness of all males born was 1.6:1 compared with all females. Dominant mares produced significantly more daughters than sons. This trend was not found for subordinates. Mother's status was positively correlated with dominant status in her female offspring but not related to the subsequent status of her sons. Daughters had a more than twice as great a chance of breeding than sons. For maximum fitness gains, therefore, dominant mares should produce more daughters, since a high proportion of these would also have high status and fitness. This tendency is reflected in the sex ratio skewed towards females found for dominant mares.     

Shifting foraging strategies in colonies of the social wasp Polybia occidentalis (Hymenoptera, Vespidae)

Social insect colonies can be expected to forage at rates that maximize colony fitness. Foraging at higher rates would increase the rate of worker production, but decrease adult survival. This trade-off has particular significance during the founding stage, when adults lost are not replaced. Prior work has shown that independent-founding wasps rear the first workers rapidly by foraging at high rates. Foraging rates decrease after those individuals pupate, presumably reducing the risk of foundress death. In the swarm-founding wasps, colony-founding units have many workers, making colony death by forager attrition less likely. Do swarm-founding wasps show similar shifts in foraging rates during the founding stage? We measured foraging rates of the swarm-founding wasp, Polybia occidentalis at four stages of colony development. At each stage, foraging rates correlated with the number of larvae present, which, in the founding stages, correlated with the number of cells in the new nest. Thus, foraging rates appear to be demand-driven, with the level of demand in the founding stage set by the size of nest that is constructed. During the founding stage, foraging rates per larva were high initially, suggesting that colonies minimize the development times of larvae early in the founding stage. Later in the stage, foraging rates decreased, which would reduce worker mortality until new workers eclose. This pattern is similar to that shown for independent-founding wasps and likely results from conflicting pressures to maximize colony growth and minimize the risk of colony death by forager attrition.     

Female mate choice in the zebra finch — the effect of male beak colour and male song

Studies of female mate preference in zebra finches (Taenopygia guttata) have shown that male beak colour and song rate are important. However, the two characters are correlated. Here the effect of beak colour and song rate on female choice are examined independently. In mate choice tests involving two males, beak colour was manipulated artificially using nail varnish. The results showed that females showed a significant preference for males with a high song rate, but not with a red beak. Females did not prefer males with a red beak if song rate was low and females preferred males with orange beaks who expressed a high song rate. Female preference for males with red beaks was not found when beak and song characters were no longer correlated.     

Individual differences in foraging behavior and cortisol levels in recently emerged brook charr (Salvelinus fontinalis)

Recently emerged brook charr (Salvelinus fontinalis) foraging in still-water pools along the sides of streams tend to be either sedentary, feeding from the lower portion of the water column (a sit-and-wait tactic), or very active, feeding from the upper portion of the water column (an active search tactic). We tested whether the individual differences in foraging behavior were associated with baseline concentrations and responses of cortisol, a steroid hormone linked to personality differences in a variety of animals including fishes. We quantified the proportion of time spent on moving by focal charr in the field and then capturing them. Captured individuals were either (i) sacrificed immediately to quantify baseline cortisol concentrations, (ii) held in an unfamiliar field environment for 15 min and then sacrificed to quantify cortisol concentrations in response to handling and holding in a novel field environment, or (iii) held in an unfamiliar field environment with a white Plexiglas base (stressor) for 15 min to quantify cortisol concentrations in response to a novel object. Eleven statistical models relating cortisol concentrations to the proportion of time individuals spent on moving while searching for prey were compared using multi-model inferencing. Cortisol concentrations were higher for charr that spent a lower proportion of time on moving in the field than for charr that spent a higher proportion of time on moving. For a given proportion of time spent on moving, mean cortisol concentrations between baseline and experimental treatments, our measure of cortisol response, did not differ markedly. Our findings suggest that the foraging tactics displayed by wild brook charr in the field could reflect differences in how individuals perceive their environment.     

Short- and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch

Hormone-mediated maternal effects play an important role in the formation of a differentiated phenotype. They have been shown to influence a wide array of offspring traits, both early in life and in adulthood. One important offspring trait that is under the influence of maternal androgens is the immune system. In birds, a growing number of studies show that yolk androgens modulate immune function during the chick stage. However, there is a lack of knowledge regarding long-term effects of prenatal androgens on offspring immunity. In this study, we therefore investigated the influence of prenatal testosterone (T) on several measures of immunity in fledgling and adult zebra finches (Taeniopygia guttata). Cell-mediated immune response (towards phytohaemagglutinin, PHA) of fledglings hatching from control eggs was negatively related to brood size, whereas there was no such association for fledglings hatching from eggs with experimentally elevated T levels (T fledglings). Male control fledglings showed reduced mass gain compared to female control fledglings within 24 h after the PHA injection. This pattern was reversed in T fledglings. Total antibody levels in fledglings were not affected by egg treatment. Neither cell-mediated immunity nor total antibody levels in sexually mature zebra finches were influenced by egg treatment. However, there was an immuno-enhancing effect of elevated egg T on both primary and secondary humoral immune responses toward diphtheria and tetanus antigens in ca 5 and 7 month old zebra finches. In addition, the covariation between different immune components differed between T and control offspring, suggesting that egg treatment may have altered the potential trade-offs between different parts of the immune system. Our results suggest that prenatal androgens could be an important factor contributing to individual variation in immune function even in adulthood.     

Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>)

Food restrictions early in life can have adverse effects on the development of adult avian song structure. Nutritional deficiencies during brain development are thought to impair the growth of neural circuits responsible for learning and production of song in adulthood. Thus, the quality of song may reflect the quality of the singer due to the costs associated with neural development early in life. Recent investigations have focused on domesticated laboratory strains of zebra finches where early dietary deficiencies have significantly reduced the complexity of song and its sexual attractiveness. Domesticated zebra finches may be more sensitive to the early effects of moderate under-nutrition on song complexity than their non-domesticated counterparts. In an aviary experiment with non-domesticated zebra finch stock, we found that song complexity when measured by a linear combination of six variables was reduced in food-restricted birds, with syllable rate and maximum syllable frequency as the principal variables affected. The restriction had no effect on learning accuracy when song phrases of experimental birds were compared to those of their fathers.This result demonstrates that early nutrition may differentially affect the development of neural processes that influence learning accuracy and song complexity. While the finding of negative effects of dietary restriction on song complexity is robust for zebra finches and is not an artefact of domestication, it does not explain why some nutritionally stressed populations of wild zebra finches have more complex songs than those from other regions of Australia characterised by greater food availability.     

Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity

The survival of marine predators depends on behavioural plasticity to cope with changes in prey distribution. Variability in behaviour might predict plasticity and is easier to assess than plasticity. Using miniaturized GPS loggers over several breeding seasons in two Norwegian Northern gannet (Morus bassanus) colonies, we investigated if and how the variability within and between individuals, but also between colonies and years, affected foraging strategies. Results revealed strong individual variability (foraging trip durations, foraging effort and different foraging areas). Individuals from both colonies showed preferred commuting routes, flight bearings and feeding hotspots. Individuals from the largest colony used larger and more foraging areas than individuals from the small colony. Feeding hotspots and foraging ranges varied amongst years in the largest colony only. Our study demonstrated that gannets show flexibility by changing prey fields that are driven by shifting oceanographic conditions.     

Habitat use by juvenile Atlantic cod (Gadus morhua) in the presence of an actively foraging and non-foraging predator

Experiments were conducted in the autumn and winter of 1992/93 to examine habitat use by juvenile (age 0+) Atlantic cod, Gadus morhua L., before, during and following exposure to a passive or actively foraging predator (age 3+ cod). Experiments presented groups of juvenile cod (n=5 fish/group) with one of two combinations of three substrates; (1) gravel, sand, and a patch of artificial kelp (kelp), or (2) cobble, sand, and kelp. Cobble is known to provide juvenile cod with a refuge from predation. Kelp was used to test the hypothesis that juvenile cod associate with fleshy macroalgae in nature because of the safety it provides from predators. There was little difference in habitat use by juvenile cod before, during or following exposure to a passive predator. Under these conditions, juvenile cod appeared to prefer finer grained mineral substrates and avoided the kelp. The extent of the juvenile response to a passive predator was to avoid the predator's location in the experimental tank. In contrast, juvenile cod showed a significant shift in habitat use when exposed to an actively foraging predator, hiding in cobble or, when cobble was not available, in kelp. Use of both these habitats resulted in a significant reduction in predation risk to the juvenile cod. Our results suggest that: (1) an association with kelp provides safety from predation to juvenile cod, and (2) juvenile cod are capable for assessing the risk a predator represents and adjust their response accordingly.     

Sex differences in the foraging behavior of squirrel monkeys in a seasonal habitat

Summary The effects of sex and seasonal changes in food abundance on foraging behavior was studied in squirrel monkeys (Saimiri oerstedi) in Costa Rica over an eleven-month period. Females searched for and ate food at significantly greater frequencies than did males throughout the study. The frequency of the specific foraging techniques used occasionally differed significantly within seasons, but not across the study period. Few differences were found in the foraging behaviors of nonreproductive sexually mature females compared to females that were pregnant or lactating. The major exception was that during the month following parturition reproductive females foraged for flowers and fruits more frequently than did non-reproductive females. The reduction of time spent by males in foraging activities gives them more time for other activities, especially anti-predator vigilance. Foraging techniques and the proportions of different food types in the diet changed seasonally. Foraging for arthropods was most frequent in the season when arthropod abundance was lowest, resulting in the amount of time spent eating arthropods to vary less across the seasons. Fruits and flowers were not eaten in a direct relationship to availability, but were used more than expected relative to availability when arthropod abundance was reduced. Individuals were more dispersed when foraging compared to other activities. Overall, there was little evidence of any direct foraging benefits for a squirrel monkey from being social.     

Polymodal foraging in adult female loggerheads (Caretta caretta)

To determine whether loggerhead turtles (Caretta caretta) nesting in southeastern USA exhibit polymorphic foraging strategies, we evaluated skin samples for stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) from 310 loggerheads from four locations on the east coast of Florida and epibionts from 48 loggerheads. We found a dichotomy between a depleted δ¹³C cluster and an enriched δ¹³C cluster. Epibionts from oceanic/pelagic or neritic/benthic habitats were largely consistent with this dichotomy. The bimodal distribution of δ¹³C could reflect a bimodal foraging strategy or—because of the potential for confounding among four gradients of δ¹³C in marine environments—a polymodal foraging strategy. We integrate our results with results from other stable isotope studies, satellite telemetry, and flipper tags to evaluate potential foraging strategies. Understanding foraging strategies is essential for development of management plans for this endangered species that has suffered a 43% population decline over the last decade.     

Optimal foraging and territorial defence in the Great Tit (Parus major)

Summary We describe an experiment designed to investigate the trade-off between foraging and territorial vigilance in the Great Tit. Captive territorial male Great Tits were observed while foraging in a large indoor aviary. They obtained food from two operant patches in which the supply of food was gradually depleted during a visit. We predicted that during control sessions the birds would switch between patches in such a way as to maximise their overall feeding rate. In experimental sessions, we introduced briefly a rival male as an intruder at the start of the test. The foraging male could see the rival only when travelling between patches and not while feeding within patches. We predicted that during experimental sessions birds would switch between patches more often than in control tests, sacrificing food intake for territorial vigilance. Three of the four males tested behaved in approximately the predicted manner. We discuss the use of an inverse optimality argument to provide a calibration of feeding against the benefit resulting from territorial vigilance.     

Clutch size and the cost of incubation in the Bengalese finch (Lonchura striata var. domestica)

Summary By measuring daily intake of food, we compared the cost of incubation for small and large clutches in adult Bengalese finches (Lonchura striata var. domestica). Natural clutches of captive finches were experimentally manipulated to produce two egg or six egg clutches. While incubating large clutches, parents ate significantly more food and took longer to hatch their first egg than did the same birds when provided with small clutches. This supports the hypothesis that the cost of incubation increases with clutch size. This cost should influence other energy allocation decisions in birds such as determination of clutch size and parental investment decisions.     

Risk-sensitive foraging behaviour of the round-eared elephant shrew (Macroscelides proboscideus)

We examined the risk-sensitive foraging behaviour of the round-eared elephant shrew by open-economy choice experiments, in which animals were deprived of food immediately prior to experiments but given food ad libitum afterwards, to test the energy budget rule. The energy budget rule states that if an animal's (daily) energy budget is negative it should behave in a risk-prone manner. A risk-prone elephant shrew should select food from a more variable rather than a constant feeding station, although both feeding stations yield the same average return. The choice of a variable station can indicate the degree to which an animal is an energy-shortfall minimizer. Elephant shrews running below energy requirement did not choose feeding stations in accordance with the rule. Under laboratory conditions, approximating either average summer or winter temperatures, elephant shrews showed risk-averse behaviour. A polycyclic activity profile, the ability to switch the diet, and greater than expected physiological control over energy balance, may favour a continuously foraging animal such that short-term energy deficits are minimized. We argue that, under these conditions, a risk-averse response to reward-size variance is expected, because an elephant-shrew may not reliably perceive those circumstances under which risk-prone behaviour should be adopted.     

Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats (Rhinolophus ferrumequinum) exhibit strong natal philopatry to their maternity roost over many years, leading to the aggregation of matrilineal kin. Maternity colonies may, therefore, be expected to comprise highly related individuals, and, as such, provide conditions suitable for the evolution of kin-selected behaviours. To test these predictions, we examined relatedness and behaviour among matrilineal kin within a colony in south-west Britain. Genetic analysis of 15 matrilines, identified from microsatellite genotyping and long-term ringing surveys, revealed average relatedness levels of 0.17 to 0.64. In contrast, background relatedness among colony females approximated to zero (0.03). These results suggest that inclusive fitness benefits may only be accrued through discriminate cooperation within matrilines, and not at the wider colony level. To examine whether the potential for such benefits is realised through kin- biased cooperation during foraging, females from two matrilines were radio-tracked simultaneously over 3 years. Pairwise home-range overlap correlated significantly with Hamilton's relatedness coefficient. The greatest spatial associations were observed between females and their adult daughters, which shared both foraging grounds and night roosts, sometimes over several years. Tagged females, however, generally foraged and roosted alone, suggesting that kin-biased spatial association probably does not result from either information-transfer or cooperative territorial defence. Such patterns may instead result from a mechanism of maternal inheritance of preferred foraging and roosting sites.     

The organisation of collective foraging in the harvester termite Hodotermes mossambicus (Isoptera)

Summary The process by which the foragers build up a foraging system between the nest hole and the food source, starting from an initial random distribution, was investigated under conditions of both light and dark in the laboratory.The extent to which trail pheromone is used can be determined by observing the abdominal position of workers moving outside the nest and can be classified into three categories, namely no trail-laying, marking and directional trail-laying.When workers of this species emerge from the nest hole into light emitted from a certain direction they orientate photo-menotactically. First, they mark the area around the nest hole, moving in small loops; they then make larger exploratory loops without trail-laying. Once they find a source of food they return directly to the immediate vicinity of the nest hole. As the area around the hole has already been marked it is easy for the termites to locate the hole. When a piece of food has been deposited by the hole the termites display directional trail-laying behaviour by leaving a trail in the direction of the source of food, this trail being stronger nearer the nest and decreasing as it approaches its goal. Inexperienced explorers are biased in this direction with a statistically higher frequency. If successful they join in the foraging and repeatedly contribute to the trail, which then gradually brings together most of the foraging population.In darkness exploratory loops are made with continuous marking, always returning to the nest hole, whereby a scent gradient decreasing away from the hole is formed. Once a source of food has been discovered the termites are neither able to return directly to the nest hole nor to return along their outward marking trail. They leave marking trails making exploratory loops from the food source with successively increasing radii. Another scent gradient, decreasing outwards from the food, is created. If the termite reaches the increasing scent around the nest hole from the decreasing scent around the food source it will locate the hole chemotactically. As other food finders repeatedly cross from one field to the other the scents will combine and become concentrated, thus forming a foraging path.