Aggressive behaviour affects selection on morphology by influencing settlement patterns in a passerine bird

The importance of behaviours as instigators or inhibitors of evolutionary change remains largely unresolved and this is in part because there are very few empirical examples of how behaviours affect evolutionary processes. By determining the environment of breeding, aggressive interactions over territories have the potential to strongly impact selection pressures experienced by individuals. Western bluebirds (Sialia mexicana) provide a unique opportunity to investigate the evolutionary importance of aggression, since their highly variable breeding habitat favours distinct foraging techniques and they also compete aggressively for nest boxes, a resource that is easy to manipulate. Here, I show experimentally that more aggressive males compete more effectively for territories with a high density of nest boxes and, as a consequence, aggressive and non-aggressive males are sorted into distinct breeding habitats that differ in the strength of selection on morphological traits. Specifically, males with longer tails and tarsi were favoured in open habitats where high agility is required to forage efficiently, whereas in forested habitats, where agility is less important, selection was weak. These results show that aggression can affect selection on a local scale by determining individual settlement patterns. More generally, because territorial interactions are important across a wide variety of taxa, these results suggest that aggressive behaviour has the potential to impact the evolutionary trajectory of many animal populations.     

Heritability of selectively advantageous foraging behaviour in a small passerine

Summary I measured the heritability of foraging patch choice in a laboratory population of zebra finches (Taeniopygia guttata). Mothers and offspring were tested for their ability to discriminate between four foraging patches which provided four different rates of energy gain. Use of a foraging patch with a high rate of energy gain has been shown to confer a selective advantage on zebra finches in a similar experimental system. In this population of zebra finches there was a large amount of variation in foraging patch choice behaviour both within and among individuals. I determined that foraging patch choice was a phenotypically labile trait with a degree of stereotypy or repeatability, much lower than those typically recorded for morphological traits. The mating behaviour of zebra finches required that heritability be determined from a mother—offspring regression, which showed that narrow sense heritability of foraging patch choice was approximately 0.346. This heritability was significantly different than zero, as was heritability when it was limited by repeatability to 0.246. Foraging patch choice, a behaviour that has a demonstrated fitness consequence, had a heritable component in this laboratory population of zebra finches.     

Migratory behaviour affects the trade-off between feather growth rate and feather quality in a passerine bird

Migratory birds have less time for moulting than sedentary birds, which may force them to produce their feathers faster at the expense of reducing feather quality. However, the effects of migration on the trade-off between moult speed and plumage quality remain to be studied in natural populations. We analysed the relationship between growth rate and quality of individual feathers, taking advantage of natural variation between migratory and sedentary populations of blackcaps Sylvia atricapilla . As predicted by life-history theory, individual blackcaps showed variable individual quality, which was revealed by positive correlations between feather growth rate and feather mass within populations. However, migrants grew up their feathers faster, producing lighter feathers than sedentary blackcaps. These results support the idea that feather growth rate and feather quality are traded against each other in blackcaps. Such a trade-off is apparently caused by different selection associated to migratory and sedentary life styles, which opens new insights into the diversification of moult patterns in birds.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 98–105.     

Food availability during migratory stopover affects testis growth and reproductive behaviour in a migratory passerine

Long-distance migratory passerines initiate testicular recrudescence during spring migration to meet the demands of timely reproduction upon immediate arrival on the breeding grounds. The degree of testicular development is known to depend on environmental factors like stopover habitat quality; reproductive performance may be strongly impacted by testicular maturation upon arrival on the breeding grounds. We investigated the effect of stopover food availability on subsequent reproductive performance in garden warblers (Sylvia borin). Spring migration was simulated by repeated food deprivation and re-feeding to imitate the alternation of flight and stopover periods. During the two final stopover periods, males were either kept under ad libitum food (ad libitum males) or under limited food conditions (limited males). After simulated arrival in the breeding area, manipulation of previous stopover food availability resulted in significantly slower testicular recrudescence (p < 0.001) and decreased plasma testosterone (p < 0.01) in limited males compared to ad libitum males. Body mass change was not significantly different between the two groups (p = 0.38). Limited males also exhibited reduced performance in reproductive behaviours employed in territorial and sexual contexts. Limited males had a longer ‘freezing’ interval (p < 0.05) and decreased activity (p < 0.01) when challenged with a live male decoy. In direct confrontation between limited and ad libitum males in the presence of a female, limited males exhibited significantly fewer behavioural traits in sexual context, i.e. directed to the female (p < 0.001). Therefore, we suggest that conditions encountered during previous migratory stopover may affect subsequent annual reproductive success by influencing key reproductive behaviours.     

Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird

1.  The relationship between the composition of communities of micro-organisms and their hosts remains poorly understood. We conducted extensive field studies of feather-degrading bacteria, other cultivable bacteria, and fungi on the plumage of a migratory bird, the barn swallow Hirundo rustica Linnaeus, to understand the association between micro-organisms, host sociality and host antimicrobial defences, as reflected by the size of the uropygial gland.
2.  The abundance of feather-degrading bacteria, but not other cultivable bacteria or fungi, decreased with increasing size of the uropygial gland.
3.  Females had more feather-degrading bacteria than males.
4.  Barn swallows living in larger colonies had more feather-degrading bacteria than less social conspecifics.
5.  These findings suggest that the uropygial gland plays a specific role in regulating the abundance of feather-degrading bacteria that furthermore depends on the social environment of the host.     

Experimental evidence for adaptive personalities in a wild passerine bird

Individuals of the same species differ consistently in risky actions. Such ‘animal personality’ variation is intriguing because behavioural flexibility is often assumed to be the norm. Recent theory predicts that between-individual differences in propensity to take risks should evolve if individuals differ in future fitness expectations: individuals with high long-term fitness expectations (i.e. that have much to lose) should behave consistently more cautious than individuals with lower expectations. Consequently, any manipulation of future fitness expectations should result in within-individual changes in risky behaviour in the direction predicted by this adaptive theory. We tested this prediction and confirmed experimentally that individuals indeed adjust their ‘exploration behaviour’, a proxy for risk-taking behaviour, to their future fitness expectations. We show for wild great tits (Parus major) that individuals with experimentally decreased survival probability become faster explorers (i.e. increase risk-taking behaviour) compared to individuals with increased survival probability. We also show, using quantitative genetics approaches, that non-genetic effects (i.e. permanent environment effects) underpin adaptive personality variation in this species. This study thereby confirms a key prediction of adaptive personality theory based on life-history trade-offs, and implies that selection may indeed favour the evolution of personalities in situations where individuals differ in future fitness expectations.     

Dawn singing of the Brownish‐flanked Bush Warbler influences dawn chorusing in a bird community

Despite numerous studies on the function of the avian dawn chorus, few studies have examined whether dawn singing may influence the singing of other species. Here, we built on our previous study which found male Brownish‐flanked Bush Warblers (Horornis fortipes) increase their dawn singing intensity after conspecific playback on the previous day. We reanalyzed those recordings to quantify the start of dawn singing in other nine sympatric songbird species. Ranking‐scaling analyses identified a distinctive sequential pattern of dawn singing among these bird species between the first and the second dawn chorus, and meta‐analysis showed a significant trend to singing earlier in the bird community accompanied by the increase in dawn singing intensity in Brownish‐flanked Bush Warbler. Species with songs most similar to that of the Brownish‐flanked Bush Warbler and species that were phylogenetically distantly related to the Brownish‐flanked Bush Warbler showed a greater shift in the onset of dawn singing. Our study is one of the few studies showing how bird song influences heterospecific singing, and this may influence the temporal organization of song activity in the community, and result in synchronization in singing activities among different species, such as singing in dawn and dusk chorus.     

Photoperiod affects growth, behaviour and stress variables in Clarias gariepinus

Short periods of light or no light (18D : 06L and 24D : 00L) resulted in an increased growth compared to extended periods of light (06D : 18L and 12D : 12L) in African catfish Clarias gariepinus . Fish under longer periods of light (12D : 12L and 18D : 06L) showed higher swimming activity, more aggression (injuries on the body) and higher lactate, free fatty acids and cortisol levels compared to those who were reared at shorter periods of light (24D : 00L and 18D : 06L). Feeding activity during light and dark periods in this experiment showed that C. gariepinus had both night and day feeding activities, with a preference to diurnal feeding in the 12D : 12L photoperiod. The results showed that light plays an important role in the African catfish behaviour and its well‐being. As the hours of light increased during the 24 h cycle, data suggests that the fish were more stressed and aggressive, compared to those under a reduced number of light hours.     

Hormone levels predict individual differences in reproductive success in a passerine bird

Hormones mediate major physiological and behavioural components of the reproductive phenotype of individuals. To understand basic evolutionary processes in the hormonal regulation of reproductive traits, we need to know whether, and during which reproductive phases, individual variation in hormone concentrations relates to fitness in natural populations. We related circulating concentrations of prolactin and corticosterone to parental behaviour and reproductive success during both the pre-breeding and the chick-rearing stages in both individuals of pairs of free-living house sparrows, Passer domesticus. Prolactin and baseline corticosterone concentrations in pre-breeding females, and prolactin concentrations in pre-breeding males, predicted total number of fledglings. When the strong effect of lay date on total fledgling number was corrected for, only pre-breeding baseline corticosterone, but not prolactin, was negatively correlated with the reproductive success of females. During the breeding season, nestling provisioning rates of both sexes were negatively correlated with stress-induced corticosterone levels. Lastly, individuals of both sexes with low baseline corticosterone before and high baseline corticosterone during breeding raised the most offspring, suggesting that either the plasticity of this trait contributes to reproductive success or that high parental effort leads to increased hormone concentrations. Thus hormone concentrations both before and during breeding, as well as their seasonal dynamics, predict reproductive success, suggesting that individual variation in absolute concentrations and in plasticity is functionally significant, and, if heritable, may be a target of selection.     

Heavy and persistent rainfall leads to brood reduction and nest failure in a passerine bird

The process of reproduction is a sensitive period for bird offspring, since they are exposed to environmental conditions for several weeks. Within the long reproductive period, adult birds do not only have to maintain their own body condition, they also have to ensure nutritional needs of their nestlings. In the worst case, if weather conditions are very harsh, breeding is not successful and fails. This suggests that weather conditions might be an important driver of breeding success. Here, we studied the effect of weather conditions (temperature and precipitation) on the survival of 350 nests of great tits Parus major during nestling period in six years (2010–2015). We used traditional generalized linear mixed model (binomial response variable) and a dedicated survival-analysis program (MARK) to analyze the data. The two approaches allowed us to highlight and compare the effect of weather conditions on a fine (nestling survival) and coarse (nest fate) scale. Both methods showed that precipitation explained most of the variation in individual nestling and overall nest survival during the 15-day nestling period. Heavy and persistent rainfall did not only lead to brood reduction, it ultimately also led to losses of the entire brood. Likely causes were the negative effects of precipitation on thermoregulation, food availability and predation risk. However, while reduced food availability most likely might have led to brood reduction through selective individual nestling death, predation might have resulted in total nest failures.     

Mobbing behaviour in a passerine community increases with prevalence in predator diet

Mobbing behaviour against predators is well documented but less is known about the factors influencing variation in behavioural response between prey species. We conducted a series of playback experiments to examine how the mobbing responses of prey species differed according to their relative risk of predation by the Eurasian Pygmy Owl Glaucidium passerinum, a predator of passerines. We found that mobbing among 22 passerine prey species was positively correlated with their prevalence in the Pygmy Owl diet. To compare mobbing behaviour between two seasons, we conducted playback experiments during spring (breeding season) and autumn (non‐breeding season). Contrary to previous studies, we found that mobbing intensity was greater during autumn than in spring. Our study shows a differential mobbing response of 22 species to the calls from one predator species and underscores the importance of considering seasonal variation in mobbing behaviour. Mobbing response differences observed among bird species strongly suggest different cooperation behaviour at the community level.     

The correlation between coloration and exploration behaviour varies across hierarchical levels in a wild passerine bird

In vertebrates, darker individuals are often found to be more active and willing to take risks (representing characteristics of a ‘proactive’ coping style), whereas lighter individuals are instead more cautious and less active (representing characteristics of a ‘reactive’ coping style). It is thus generally expected that melanin‐based coloration and proactivity form a suite of positively integrated traits at the among‐individual level. Here, we use a multigenerational pedigree of free‐living great tits (Parus major) to partition variation in, and the correlation between, melanin‐based breast stripe (‘tie’) size and exploration behaviour (a proxy for coping style) into its among‐ and within‐individual components. We show that both traits harbour heritable variation. Against predictions, tie size and speed of exploration were negatively correlated at the among‐individual level due to the combined influences of permanent environmental and additive genetic effects. By contrast, the two traits were weakly positively correlated within individuals (i.e. individuals increasing in tie size after moult tended to become more explorative). The patterns of among‐individual covariance were not caused by correlational selection as we found additive and opposite selection pressures acting on the two traits. These findings imply that testing hypotheses regarding the existence of a ‘syndrome’ at the among‐individual level strictly requires variance partitioning to avoid inappropriate interpretations as the negative ‘unpartitioned’ phenotypic correlation between exploration and tie size resulted from counteracting effects of within‐ and among‐individual correlations. Identifying sources and levels of (co)variation in phenotypic traits is thus critical to our understanding of biological patterns and evolutionary processes.     

Bargaining babblers: vocal negotiation of cooperative behaviour in a social bird

Wherever individuals perform cooperative behaviours, each should be selected to adjust their own current contributions in relation to the likely future contributions of their collaborators. Here, we use the sentinel system of pied babblers (Turdoides bicolor) to show that individuals anticipate contributions by group mates, adjusting their own contribution in response to information about internal state broadcast by others. Specifically, we show that (i) short-term changes in state influence contributions to a cooperative behaviour, (ii) individuals communicate short-term changes in state, and (iii) individuals use information about the state of group mates to adjust their own investment in sentinel behaviour. Our results demonstrate that individual decisions about contributions to a cooperative effort can be influenced by information about the likely future contribution of others. We suggest that similar pre-emptive adjustments based on information obtained from collaborators will be a common feature of cooperative behaviour, and may play an important role in the development of complex communication in social species.     

It is time to move: linking flight and foraging behaviour in a diving bird

Although the adaptive value of flight may seem obvious, it is the most difficult behaviour of birds to monitor. Here, we describe a technique to quantify the frequency and the duration of flights over several months by implanting a data logger that records heart rate (fH), hydrostatic pressure (diving depth) and the body angle of a large sea duck species, the common eider (Somateria mollissima). According to the mean fH recorded during flight and the parameters recorded to identify the fH flight signature, we were able to identify all flights performed by 13 individuals during eight months. We cumulated local flight time (outside migrations) and found that activity occurs primarily during dawn and morning and that flying activities are strongly related to diving activities (Pearson's r=0.88, permutation test p<0.001). This relationship was interpreted as a consequence of living in a dynamic environment where sea currents move the ducks away from the food patches. We believe that the technique described here will open new avenues of investigation in the adaptive value of flight.     

Testing hypotheses about the function of repeated nest abandonment as a life history strategy in a passerine bird

Nest structures are essential for successful reproduction in most bird species. Nest construction costs time and energy, and most bird species typically build one nest per breeding attempt. Some species, however, build more than one nest, and the reason for this behaviour is often unclear. In the Grey Fantail Rhipidura albiscapa, nest abandonment before egg‐laying is very common. Fantails will build up to seven nests within a breeding season, and pairs abandon up to 71% of their nests before egg‐laying. We describe multiple nest‐building behaviour in the Grey Fantail and test four hypotheses explaining nest abandonment in this species: cryptic depredation, destruction of nests during storm events, and two anti‐predatory responses (construction of decoy nests to confuse predators, and increasing concealment to ‘hide’ nests more effectively). We found support for only one hypothesis – that abandonment is related to nest concealment. Abandoned nests were significantly less concealed than nests that received eggs. Most abandoned nests were not completely built and none received eggs, thus ruling out cryptic predation. Nests were not more likely to be abandoned following storm events. The decoy nest hypothesis was refuted as abandoned nests were constructed at any point during the breeding season and some nests were dismantled and the material used to build the subsequent nest. Thus, Grey Fantails are flexible about nest‐site locations during the nest‐building phase and readily abandon nest locations if they are found to have deficient security.     

Cooperative nest‐defence behaviour and territory quality in a resident and socially monogamous passerine

Nest defence is a fundamental aspect of parental care in secondary cavity‐nesting birds, and predation or competition for nesting sites can involve different defensive behaviours. Because habitat quality determines breeding success, we were interested in whether breeding pairs of the Eurasian nuthatch, Sitta europaea, established in more favourable environment also manifest higher probability of cooperative behaviour during their nest‐site defence. To explore this relationship, we quantified behavioural displays of both parents and analysed activity budget ethogram data from simulated territorial intrusions performed in the chick‐feeding phase with one conspecific and two different heterospecific stimuli (dummies of nuthatch, starling and woodpecker). We found that paired individuals shared their roles during nest‐site defence to a considerable extent. Males had a significantly higher number of attacks on intruders than females, and females performed more threat displays and controls of the brood than males. Multinomial analysis of the cooperative behaviour suggested that pairs in a high‐quality territory had higher probability of reciprocal substitution of different roles towards a balance between attacks, threat displays and nest controls. Contrary to this, pairs in a low‐quality territory had less likely pairwise combinations of simultaneous behavioural states that are associated with effective nest‐site defence. The difference in response probability according to territory quality was, however, highly variable in view of the stimulus that was used in simulated territorial intrusion. Because individual roles and the complex behavioural repertoire of pairs altered in response to territory quality and potential nest‐site competitor or brood predator, our results suggest that the cooperative nest‐defence behaviour could be linked to the breeding success of this year‐round territorial species living in a heterogeneous forest habitat.     

Diet affects female mating behaviour in a seed‐feeding beetle

In species where males provide nuptial gifts, females can improve their nutritional status and thus increase their fecundity by mating when in need of resources. However, mating can be costly, so females should only mate to acquire resources when the need for resources is large, such as when females are nutritionally‐deprived. Two populations of the seed‐feeding beetle Callosobruchus maculatus, a species that produces relatively large nuptial gifts, are used to test whether female nutritional status affects mating behaviour. Female access to water, sugar and yeast are manipulated and the fitness consequences of these manipulations are examined together with the effects of diet on the propensity of nonvirgin females to mate. Access to water has a small but significant effect on mass loss over time, lifespan and fecundity of females, relative to unfed controls. Access to sugar (dissolved in water) improves female fecundity and lifespan above that of hydrated females but access to yeast has no positive effects on female survival or reproduction. Diet has a large effect on both receptivity of nonvirgin females to a male and how quickly they accept that male. Unfed females are both more likely to mate, and accept a mate more quickly, than females provided access to water, which are more likely to mate and accept a mate more quickly than females provided with sugar. This rank order of behaviours matches the order predicted if females increase their mating rate when nutritionally deprived (i.e. it matches the effect of diet on female fitness). The results obtained also suggest that mate choice may be condition‐dependent: females from one population (Burkina Faso) show a preference for large males when well‐fed but not when unfed, although this result is not found in a second population (South India). It is concluded that nutritionally‐deprived females are more receptive to mates than are well‐fed females, consistent with the hypothesis that females ‘forage’ for nuptial gifts, or at least more willingly accept sperm in exchange for nuptial gifts, when they are nutritionally deprived.     

Heavy metal pollution in Antarctica: a molecular ecotoxicological approach to exposure assessment

Trematomus bernacchii sampled from two sites at Ross Island, Antarctica, were assessed for condition (gonadal and hepatic somatic indices and condition factor), pathological state (liver and gill histology), hepatic metal (Zn, Cu, Cd and Ni) concentrations, and metallothionein induction by quantitative competitive (qc) RT-PCR. Fish from a polluted site (Winter Quarters Bay) had pathological anomalies including necrosis and periductal inflammation in their livers, and X-cell disease, epithelial hyperplasia, lamellar fusion and aneurysms in their gills. Such anomalies were less common in fish from a relatively pristine site (Backdoor Bay, Cape Royds). Fish from both sites had similar liver concentrations of Zn, Cu and Cd and qcRT-PCR revealed similar levels of hepatic metallothionein mRNA. Ni in the livers of fish from Winter Quarters Bay were higher than those in fish from Backdoor Bay, but the differences were not great enough to affect hepatic metallothionein mRNA significantly. Despite the polluted state of Winter Quarters Bay waters, it seems that the heavy metals present may have only limited impact on the health status of fish collected from this locality. This may reflect a low bioavailability of the heavy metals in Ross Island marine sediments and suggests that other factors, such as relatively high levels of organic pollutants (PAHs, PCBs) or pathogens from the nearby sewage outlet, may play a more significant role in the aetiology of pathological conditions in fish from Winter Quarters Bay.