Nest site preference depends on the relative density of conspecifics and heterospecifics in wild birds

Background

Social learning allows animals to eavesdrop on ecologically relevant knowledge of competitors in their environment. This is especially important when selecting a habitat if individuals have relatively little personal information on habitat quality. It is known that birds can use both conspecific and heterospecific information for social learning, but little is known about the relative importance of each information type. If provided with the choice between them, we expected that animals should copy the behaviour of conspecifics, as these confer the best information for that species. We tested this hypothesis in the field for Pied Flycatchers Ficedula hypoleuca arriving at their breeding grounds to select a nest box for breeding. We assigned arbitrary symbols to nest boxes of breeding pied flycatchers (conspecifics) and blue and great tits, Cyanistes caeruleus and Parus major (heterospecifics), in 2014 and 2016 in two areas with different densities of tits and flycatchers. After ca 50% of flycatchers had returned and a flycatcher symbol was assigned to their nest box, we gave the later arriving flycatchers the choice between empty nest boxes with either a conspecific (flycatcher) or a heterospecific (tit) symbol.

Results

As expected, Pied Flycatchers copied the perceived nest box choice of conspecifics, but only in areas that were dominated by flycatchers. Against our initial expectation, flycatchers copied the perceived choice of heterospecifics in the area heavily dominated by tits, even though conspecific minority information was present.

Conclusions

Our results confirm that the relative density of conspecifics and heterospecifics modulates the propensity to copy or reject novel behavioural traits. By contrasting conspecific and heterospecific ecology in the same study design we were able to draw more general conclusions about the role of fluctuating densities on social information use.

     

Infestation of fruit by conspecific and heterospecific females deters oviposition in two Tephritidae fruit fly species

Tephritidae fruit fly larvae develop entirely in the host chosen by the females. To improve the fitness of their progeny, females would benefit from rejecting previously exploited hosts. Anastrepha fraterculus and Ceratitis capitata are two species of fruit flies having similar nutritional requirements and overlapping in their distribution. Previous studies found that competition between the larvae of these species might reach high levels, suggesting that cross-recognition would be an adaptive trait. In this work, we tested the ability of A. fraterculus and C. capitata females to recognize and avoid fruits previously infested by both conspecific and heterospecific females. In laboratory behavioural arenas, females were presented with fruits that had been previously exposed to either conspecific or heterospecific females. Then, we conducted choice and non-choice assays to compare the response of A. fraterculus and C. capitata females to infested and non-infested fruits. In non-choice tests, the females from both species rejected fruits previously infested by conspecific and heterospecific individuals. However, the rejection occurred at different steps of the sequence leading to oviposition: A. fraterculus showed a lower rate of visits to infested fruits, whereas C. capitata visited both infested and non-infested fruits, but the latency to visit a fruit and the rejection frequency were higher and the duration of the visit to infested fruit was lower. In choice assays, the rejection of heterospecific infested fruit was higher than that of conspecific infested fruits, for both species. Our results suggest that, regardless of the sensory mechanism used by females, the recognition of previous infestation is bidirectional and females of both species, belonging to different genera, recognize fruit infested by heterospecifics. These responses indicate that cross-recognition, supposedly a highly beneficial trait, could be occurring in nature, thus reducing interspecific competition and contributing to the coexistence of these species.     

Observed heterospecific clutch size can affect offspring investment decisions

Optimal investment in offspring is important in maximizing lifetime reproductive success. Yet, very little is known how animals gather and integrate information about environmental factors to fine tune investment. Observing the decisions and success of other individuals, particularly when those individuals initiate breeding earlier, may provide a way for animals to quickly arrive at better breeding investment decisions. Here we show, with a field experiment using artificial nests appearing similar to resident tit nests with completed clutches, that a migratory bird can use the observed high and low clutch size of a resident competing bird species to increase and decrease clutch size and egg mass, accordingly. Our results demonstrate that songbirds can discriminate between high and low quantity of heterospecific eggs, and that social information can have long-term physiological consequences affecting reproductive strategies. Such behaviour may help animals to better adapt to changing environments and lead to convergent traits with competitors.     

Heterospecific attraction and food resources in migrants' breeding patch selection in northern boreal forest

We studied experimentally how heterospecific attraction may affect habitat selection of migrant passerine birds in Finnish Lapland. We manipulated the densities of resident tit species (Parus spp.). In four study plots residents were removed before the arrival of the migrants in the first study year, and in four other plots their densities were increased by releasing caught individuals. In the second year the treatments of the areas were reversed, allowing paired comparisons within each plot. We also investigated the relative abundance of arthropods in the study plots by the sweep-net method. This allowed us to estimate the effect of food resources on the abundance of birds. The heterospecific attraction hypothesis predicts that densities of migrant species (especially habitat generalists) would be higher during increased resident density. Results supported this prediction. Densities and number of the most abundant migrant species were significantly higher when resident density was increased than when they were removed. On the species level the redwing (Turdus iliacus) showed the strongest positive response to the increased abundance of tits. Migrant bird abundances seemed not to vary in parallel with relative arthropod abundance, with the exception of the pied flycatcher (Ficedula hypoleuca) which showed a strongly positive correlation with many arthropod groups. The results of the experiment indicate that migrants can use resident tit species as a cue to a profitable breeding patch. The relationship between the abundance of the birds and arthropods suggests that annual changes in food resources during the breeding season probably do not have a very important effect on bird populations in these areas. The results stress the importance of positive interspecific interactions in structuring northern breeding bird communities. Received: 1 September 1997 / Accepted: 22 January 1998     

REPRODUCTIVE BEHAVIOR OF FEMALE BUNTINGS: ISOLATING MECHANISMS IN A HYBRIDIZING PAIR OF SPECIES

The plumage characteristics of male Indigo and Lazuli Buntings are distinct, but the two species can learn each other's songs. Populations comprising Indigo, Lazuli and hybrid individuals occur in the Great Plains of North America, and assortative mating has been inferred from morphometric data. We devised a laboratory assay for determining female preferences for visual and vocal characteristics of conspecific and heterospecific males and for mixtures of these characteristics, such as might be encountered in an overlap population. Females of both species gave more copulation-solicitation displays when exposed to conspecific plumage and vocalizations than when exposed to heterospecific plumage and vocalizations. Females gave intermediate and similar responses to the combinations of conspecific plumage with heterospecific vocalizations and heterospecific plumage with conspecific vocalizations. Thus, in the absence of other potentially important variables, female reproductive behavior is consistent with the hypothesis of assortative mating, based upon both vocal and visual traits of the males and caused by female choice in this semispecies pair.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.     

Song discrimination by nestling collared flycatchers during early development

Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatry with closely related species.     

Mate choice and imprinting in birds studied by cross-fostering in the wild

Sexual-selection theories generally assume that mating preferences are heritable traits. However, there is substantial evidence that the rearing environment may be important for the development of mating preferences, indicating that they may be learnt, or modified by experience. The relative importance of such sexual imprinting across species remains largely unexplored. Here, we report results of a large-scale cross-fostering experiment in the wild in which nestling birds were raised by parents of a different species. We show that resulting sexual imprinting may have a negative effect on pairing success in one species (the great tit, Parus major), but not in two other species (the blue tit, P. caeruleus and the pied flycatcher, Ficedula hypoleuca). A remarkable variation thus seems to exist, even between species that are congeneric and have similar breeding ecologies. The cross-fostering resulted in heterospecific pairings between the two tit species (female blue tit breeding with male great tit), which has never, to our knowledge, been previously documented. However, the chicks fledging from these nests were all blue tit.     

Asymmetric Assortative Mating Behaviour Reflects Incomplete Pre‐zygotic Isolation in the Nasonia Species Complex

Preference of con‐ over heterospecific mates leading to assortative mating can substantially contribute to pre‐zygotic reproductive isolation and prevent fitness losses if post‐zygotic hybridization barriers already exist. The jewel wasp genus Nasonia displays quite strong and well‐studied post‐zygotic reproductive isolation due to a ubiquitous Wolbachia infection causing cytoplasmic incompatibility between different species. Pre‐zygotic isolation, however, has received far less research attention in this model organism, especially concerning the mechanisms and criteria of mate choice. In the present study, we analysed mate rejection and mate acceptance rates in cross‐comparisons between all four Nasonia species. We put emphasis on observing which sex is more likely to interrupt interspecific matings and how discriminatory behaviour varies across the different species in all possible combinations. We found an asymmetric distribution of assortative mating among the four Nasonia species that appears to be highly influenced by the respective combinations of sex and species. Females appeared to be the main discriminators against heterospecific mating partners, but interestingly, we could also detect mate discrimination and rejection behaviour in males, a widely neglected factor in research on mating behaviour in general and on Nasonia in particular. Moreover, the asymmetry in the assortative mating behaviour was partially reflective of sym‐ or allopatric distributions of natural Nasonia populations.     

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.     

The roles of natural and sexual selection during adaptation to a novel environment

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.     

Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty‐seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab‐raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free‐living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free‐living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5–5.8% of the total variance—a large effect for a single gene influencing a complex behavioural trait—but not in three others. The confirmation of an association between SNP830 genotype and personality‐related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.     

Song learning and mate choice in estrildid finches raised by two species

Male zebra finches, Taeniopygia guttata, and Bengalese finches, Lonchura striata, were raised normally or cross-fostered to the other species until 35 days of age and then housed until 70 days old with two song tutors, one from each species. Males raised normally based their song on that of the conspecific tutor whereas cross-fostered males also learned from the other tutor, reflecting both own-species bias and a tendency to learn from the tutor whose song was similar to the father's. Males raised by one bird from each species learned from the father as well as the tutor(s) but were more likely to learn from the tutor whose song was similar to the father's if the father was a conspecific. Comparing these song learning results with those from male choice tests suggests there is no direct link between song learning and sexual imprinting.     

Spatial distribution of phytophagous mites (Acari: Tetranychidae) on strawberry plants

Many phytophagous mites can attack strawberry plants, Fragaria x ananassa, among them the southern red mite, Oligonychus ilicis McGregor, and the two-spotted spider mite, Tetranychus urticae Koch. They are found together feeding on the same plant on the upper and underside of the leaves, respectively. Here we studied the choice for feeding sites of O. ilicis and T. urticae on strawberry plants. The first hypothesis tested whether the feeding site choice would be related to the fitness of the species. The second hypothesis dealt whether the feeding site would be determined by the presence of a heterospecific mite. We evaluated the preference, biology and reproductive success of O. ilicis and T. urticae on the under and upper side surface of strawberry leaves infested or not by the heterospecific. O. ilicis preferred to stay on the upper side surface while T. urticae preferred the underside. The preference for the leaf surface correlated with the reproductive success of the species (measured by the intrinsic growth rate). The choice pattern of feeding sites did not alter when the choice test was applied using sites previously infested by heterospecific. Although O. ilicis and T. urticae, apparently, do not interact directly for feeding sites, there is a chance that the first species induces defenses in strawberry plant enabling to reduce the fitness of the second species. The possibility of those species stay together on strawberry plant increases the damage capacity to the culture.     

Spatial and behavioural measures of social discrimination by captive male zebra finches: Implications of sexual and species differences for recognition research

All bird species reproduce sexually and individuals need to correctly identify conspecifics for successful breeding. Captive zebra finches are a model system for studying the factors involved in species recognition and mate choice. However, male zebra finches’ behavioural responses in a spatial preference paradigm to a range of estrildid finch species, other than domesticated Bengalese finches, remain unknown. We investigated spatial and display responses of male zebra finch subjects to stimulus females between conspecific and four phylogeographically relevant finch species, in addition to female Bengalese finches. Surprisingly, male subjects did not show consistent spatial association with conspecific over heterospecific females. Overall, as predicted by sexual selection theory, the spatial proximity responses of males were less discriminatory compared to female zebra finches’ responses tested previously using the same paradigm. However, male subjects showed consistently more behavioural displays towards female conspecifics than heterospecifics which were positively related to the behavioural display rates of the respective female stimuli. Some male behavioural responses, other than song, also showed significant differences between the different stimulus species and consistently differed across individual test subjects, with the most individual subject variation seen in choice trials between female conspecific and Bengalese finch stimuli. The results are important for the design and interpretation of future behavioural and neurobiological experiments on species recognition systems using the zebra finch as a model species.     

The ABC-D of animal linguistics: are syntax and compositionality for real?

In several animal species, an alarm call (e.g. ABC notes in the Japanese tit Parus minor) can be immediately followed by a recruitment call (e.g. D notes) to yield a complex call that triggers a third behaviour, namely mobbing. This has been taken to be an argument for animal syntax and compositionality (i.e. the property by which the meaning of a complex expression depends on the meaning of its parts and the way they are put together). Several additional discoveries were made across species. First, in some cases, animals respond with mobbing to the order alarm–recruitment but not to the order recruitment–alarm. Second, animals sometimes respond similarly to functionally analogous heterospecific calls they have never heard before, and/or to artificial hybrid sequences made of conspecific and heterospecific calls in the same order, thus adding an argument for the productivity of the relevant rules. We consider the details of these arguments for animal syntax and compositionality and argue that, with one important exception (Japanese tit ABC-D sequences), they currently remain ambiguous: there are reasonable alternatives on which each call is a separate utterance and is interpreted as such (‘trivial compositionality’). More generally, we propose that future studies should argue for animal syntax and compositionality by explicitly pitting the target theory against two deflationary analyses: the ‘only one expression’ hypothesis posits that there is no combination in the first place, for example just a simplex ABCD call; while the ‘separate utterances’ hypothesis posits that there are separate expressions (e.g. ABC and D), but that they form separate utterances and are neither syntactically nor semantically combined.     

Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

Accumulating evidence suggests that within‐individual plasticity of behavioural and physiological traits is limited, resulting in stable among‐individual differences in these aspects of the phenotype. Furthermore, these traits often covary within individuals, resulting in a continuum of correlated phenotypic variation among individuals within populations and species. This heterogeneity, in turn, affects individual fitness and can have cross‐generational effects. Patterns of trait covariation, among‐individual differences, and subsequent fitness consequences have long been recognized in reptiles. Here, we provide a test of patterns of among‐individual heterogeneity in behaviour and physiology and subsequent effects on reproduction and offspring fitness in the garter snake Thamnophis elegans. We find that measures of activity levels vary among individuals and are consistent within individuals in reproductive female snakes, indicating stable behavioural phenotypes. Blood hormone and glucose concentrations are not as stable within individuals, indicating that these traits do not describe consistent physiological phenotypes. Nonetheless, the major axes of variation in maternal traits describe behavioural and physiological phenotypes that interact to predict offspring body condition and mass at birth. This differential allocation of energy to offspring, in turn, strongly influences subsequent offspring growth and survival. This pattern suggests the potential for strong selection on phenotypes defined by behaviour–physiology interactions.     

Heterozygosity and its unexpected correlations with hybrid sterility

In general, heterozygosity is considered to be advantageous, primarily because it masks the effects of deleterious recessive alleles. However, there is usually a reduction in fitness in individuals that are heterozygous due to the pairing of two species (heterospecific). Because the parental alleles arose along separate evolutionary paths, they may not function properly when brought together within an individual. The formation of these unfit interspecies hybrids is one of the mechanisms that maintains species isolation. Interestingly, it has been observed that later-generation individuals resulting from a backcross to one parent are more often sterile than those resulting from a backcross to the other parent, but the mechanism underlying this trend is unknown. Here, I show that one direction of backcross produces offspring with more heterospecific genome, and that this is correlated with the directionality seen in backcross hybrid sterility. Therefore, the directionality in sterility is likely due to the different amounts of heterospecific genome present in the two backcrosses. Surprisingly, in spite of the potential fitness consequences, I also find that interspecies laboratory backcrosses in general yield an excess of heterospecific individuals, and that this trend is consistent across multiple taxa.     

Long‐Distance Calling by the Willow Tit,Poecile montanus,Facilitates Formation of Mixed‐Species Foraging Flocks

The occurrence of mixed‐species foraging flocks is a worldwide phenomenon in terrestrial bird communities. Previous studies suggest that individuals participating in flocks might derive benefits in terms of improved feeding efficiency and/or reduced risk of predation. However, very little is known about how individuals establish mixed‐species flocks. Here, I provide the first experimental evidence that long‐distance calling by the willow tit, Poecile montanus, facilitates the establishment of mixed‐species flocks at a foraging patch. Observations at experimental foraging patches showed that willow tits that find a food source produce long‐distance calls, particularly when they are isolated from conspecific flockmates. The probability of long‐distance calling was negatively correlated with the number of heterospecific foraging individuals near the food source. A playback experiment confirmed that calls attract both conspecific and heterospecific members of foraging flocks. This study demonstrates that willow tits use long‐distance calls to attract conspecific flockmates to foraging patches, and these calls can also facilitate the formation of mixed‐species flocks on patches.     

Social phenotype extended to communities: Expanded multilevel social selection analysis reveals fitness consequences of interspecific interactions

In social species, fitness consequences are associated with both individual and social phenotypes. Social selection analysis has quantified the contribution of conspecific social traits to individual fitness. There has been no attempt, however, to apply a social selection approach to quantify the fitness implications of heterospecific social phenotypes. Here, we propose a novel social selection based approach integrating the role of all social interactions at the community level. We extended multilevel selection analysis by including a term accounting for the group phenotype of heterospecifics. We analyzed nest activity as a model social trait common to two species, the lesser kestrel (Falco naumanni) and jackdaw (Corvus monedula), nesting in either single‐ or mixed‐species colonies. By recording reproductive outcome as a measure of relative fitness, our results reveal an asymmetric system wherein only jackdaw breeding performance was affected by the activity phenotypes of both conspecific and heterospecific neighbors. Our model incorporating heterospecific social phenotypes is applicable to animal communities where interacting species share a common social trait, thus allowing an assessment of the selection pressure imposed by interspecific interactions in nature. Finally, we discuss the potential role of ecological limitations accounting for random or preferential assortments among interspecific social phenotypes, and the implications of such processes to community evolution.