Research on avian bioacoustics in the Neotropics has surged over the last several decades due to increased interest in the large diversity of vocal behaviors and vocalization and the broader accessibility of recording equipment and software. Here, we present a synthesis of the current and past knowledge of Neotropical bird bioacoustics. This synthesis is the result of the symposium "Bioacoustics in the Neotropics", organized for the XI Neotropical Ornithological Congress in San Jose, Costa Rica, in July 2019. We covered what we consider the main topics in avian bioacoustics that have been studied in this region over the last 30 years. Our review includes repertoire descriptions, geographic variation, diversity in vocal behaviors, seasonality, duetting, genetic association, and playback experiments. Additionally, we present information for what we believe may be the main veins of investigation for the coming future in the Neotropics, considering the large diversity of species that are found in the region and the new investigations developed in other geographic areas. We expect this review to work as a summary of the current literature and a guide to stimulate future research in important areas within the field of avian bioacoustics in the Neotropics.
Habitat loss is leading to smaller fragmented populations, increasing their susceptibility to stochasticity. Quantifying the effects of demographic and environmental stochasticity on population dynamics and the contribution of selection versus drift to phenotypic change is essential to assess the potential consequences of environmental change. We examined how stochasticity influenced population growth and body mass changes over 22 years in 11 insular house sparrow (Passer domesticus) populations. Environmental stochasticity induced synchrony in growth rates across populations while also causing substantial island-specific fluctuations. Additionally, demographic stochasticity led to larger annual growth rate fluctuations in smaller populations. Although heavier individuals generally had higher fitness, we detected non-directional evolutionary change in body mass, driven by drift rather than selection. Our study provides a unique quantitative assessment of the 'small population' paradigm, highlighting the importance of theoretically driven analyses of long-term individual-based data to understand the drivers of phenotypic evolution and a population's long-term viability.
The house sparrow (Passer domesticus) is a small passerine known to be highly sedentary. Throughout a 30-year capture-mark-recapture study, we have obtained occasional reports of recoveries far outside our main metapopulation study system, documenting unusually long dispersal distances. Our records constitute the highest occurrence of long-distance dispersal events recorded for this species in Scandinavia. Such long-distance dispersals radically change the predicted distribution of dispersal distances and connectedness for our study metapopulation. Moreover, it reveals a much greater potential for colonization than formerly recorded for the house sparrow, which is an invasive species across four continents. These rare and occasional long-distance dispersal events are challenging to document but may have important implications for the genetic composition of small and isolated populations and for our understanding of dispersal ecology and evolution.
Changes in avian breeding phenology are among the most apparent responses to climate change in free-ranging populations. A key question is whether populations will be able to keep up with the expected rates of environmental change. There is a large body of research on the mechanisms by which avian lay-dates track temperature change and the consequences of (mal)adaptation on population persistence. Often overlooked is the role of males, which can influence the lay-date of their mate through their effect on the prelaying environment. We explore how social plasticity causing male indirect genetic effects can help or hinder population persistence when female genes underpinning lay-date and male genes influencing female’s timing of reproduction both respond to climate-mediated selection. We extend quantitative genetic moving optimum models to predict the consequences of social plasticity on the maximum sustainable rate of temperature change, and evaluate our model using a combination of simulated data and empirical estimates from the literature. Our results suggest that predictions for population persistence may be biased if indirect genetic effects and cross-sex genetic correlations are not considered and that the extent of this bias depends on sex differences in how environmental change affects the optimal timing of reproduction. Our model highlights that more empirical work is needed to understand sex-specific effects of environmental change on phenology and the fitness consequences for population dynamics. While we discuss our results exclusively in the context of avian breeding phenology, the approach we take here can be generalized to many different contexts and types of social interaction.
Density dependence plays an important role in population regulation in the wild. It involves a decrease in population growth rate when the population size increases. Fifty years ago, Charlesworth introduced the concept of ‘critical age group’, denoting the age classes in which variation in the number of individuals most strongly contributes to density regulation. Since this pioneering work, this concept has rarely been used. In light of Charlesworth’s concept, we discuss the need to develop work between behavioural ecology, demography and evolutionary biology to better understand the mechanisms acting in density-regulated age-structured populations. We highlight demographic studies that explored age-specific contributions to density dependence and discuss the underlying evolutionary processes. Understanding competitive interactions among individuals is pivotal to identify the ages contributing most strongly to density regulation, highlighting the need to move towards behavioural ecology to decipher mechanisms acting in density-regulated age-structured populations. Because individual characteristics other than age can be linked to competitive abilities, expanding the concept of critical age to other structures (e.g. sex, dominance rank) offers interesting perspectives. Linking research fields based on the concept of the critical age group is key to move from a pattern-oriented view of density regulation to a process-oriented approach. This article is part of the discussion meeting issue ‘Understanding age and society using natural populations’.
Maximising reproductive success is crucial to animal production systems, particularly in meeting global demands for animal products and improving commercially important traits. However, while social interactions and mating strategies are known to influence reproductive success in wild populations, their consideration in agricultural systems remains limited. Using an interdisciplinary framework that combines concepts from behavioural ecology and quantitative genetics in an animal breeding context, we investigated the role of sperm limitation and polygynous mating strategies (female polyandry, male monopolisation of females and male polygamy) in limiting female reproductive success in farmed Pekin ducks ( Anas platyrthynchos domestica ). We assessed the impact of these behaviours on chick production and quantified their genetic and environmental (co)variance. Our results revealed that the number of dam mates positively influenced chick production in female ducks. However, contrary to our expectation, skew in chick paternity (our measure of male monopolisation) was associated with increased female chick production, challenging the hypothesis that male monopolisation limits the sperm available to females and reduces their reproductive success. We found no evidence that male polygamy led to decreased female chick production. Genetic analysis revealed that female mate number and reproductive skew exhibit genetic variance, providing opportunities for targeted selection to enhance chick production. However, there was a negative genetic association between female polyandry and skew in chick paternity, suggesting a trade-off between these traits that would need to be considered in future selection programmes. Our findings highlight how concepts from behavioural ecology can be incorporated into breeding programmes, providing new opportunities to develop effective and sustainable breeding strategies. ### Competing Interest Statement The authors have declared no competing interest.
Many group-living animals coordinate social behaviours using contact calls, which can be produced for all group members or targeted at specific individuals. In the disc-winged bat, Thyroptera tricolor , group members use ‘inquiry’ and ‘response’ calls to coordinate daily movements into new roosts (furled leaves). Rates of both calls show consistent among-individual variation, but causes of within-individual variation remain unknown. Here, we tested whether disc-winged bats produce more contact calls towards group members with higher kinship or association. In 446 experimental trials, we recorded 139 random within-group pairs of one flying bat (producing inquiry calls for roost searching) and one roosting bat (producing response calls for roost advertising). Using generalized linear mixed-effect models (GLMM), we assessed how response and inquiry calling rates varied by sender, receiver, genetic kinship and co-roosting association rate. Calling rates varied consistently across senders but not by receiver. Response calling was influenced by inquiry calling rates, but neither calling rate was higher when the interacting pair had higher kinship or association. Rather than dyadic calling rates indicating within-group relationships, our findings are consistent with the hypothesis that bats produce contact calls to maintain contact with any or all individuals within a group while collectively searching for a new roost site. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.
The causes of variation in multiple paternity (MP) in socially monogamous birds have received considerable attention. Traits like age and age-dependent morphology have been shown to be important for the distribution of MP. However, most studies fail to separate between the different processes underlying age-effects on MP, such as selective disappearance (that is, higher survival probability for certain phenotypes) versus individually plastic changes in morphology and mating behaviour with age. Using Bayesian multi-level path analysis on a long-term dataset from a house sparrow ( Passer domesticus ) metapopulation, we disentangle the effects of age on male and female MP, both independently from and through morphological traits. Age was a key determinant of MP for males when accounting for morphological traits, with males having MP more often as they get older (plastic component of age) and not due to disappearance of males unsuccessful to get MP (selective disappearance), challenging ‘good genes’ explanations for MP. Conversely, selective disappearance explained the higher levels of MP in older females, suggesting that higher quality females have MP more often than lower quality females. We show how an appropriate statistical decomposition of age-components and age-dependent processes provides insights to the biological drivers of MP.### Competing Interest StatementThe authors have declared no competing interest.
Assessing the biological relevance of variance components estimated using MCMC-based mixed-effects models is not straightforward. Variance estimates are constrained to be greater than zero and their posterior distributions are often asymmetric. Different measures of central tendency for these distributions can therefore be very different, and credible intervals cannot overlap zero, making it difficult to assess the the size and statistical support for among-group variance. This is often done through visual inspection of the whole posterior distribution, and so relies on subjective decisions for interpretation. We use simulations to demonstrate the difficulties of summarising the posterior distributions of variance estimates from MCMC-based models. We compare commonly used summary statistics of posterior distributions of variance components showing that the posterior median is predominantly the least biased. We also describe different methods for generating null distributions (i.e. a distribution of effect sizes that would be obtained if there was no among-group variance) that can be used to aid in the interpretation of variance estimates. We further show how null distributions could be used to derive a p-value that provides complimentary information to the commonly presented measures of central tendency and uncertainty and also facilitates the implementation of power analyses within an MCMC framework.
Telomeres, the nucleotide sequences that protect the ends of eukaryotic chromosomes, shorten with each cell division and telomere loss may be influenced by environmental factors. Telomere length (TL) decreases with age in several species, but little is known about the sources of genetic and environmental variation in the change in TL (∆TL) in wild animals. In this study, we tracked changes in TL throughout the natural lifespan (from a few months to almost 9 years) of free-living house sparrows (Passer domesticus) in two different island populations. TL was measured in nestlings and subsequently up to four times during their lifetime. TL generally decreased with age (senescence), but we also observed instances of telomere lengthening within individuals. We found some evidence for selective disappearance of individuals with shorter telomeres through life. Early-life TL positively predicted later-life TL, but the within-individual repeatability in TL was low (9.2%). Using genetic pedigrees, we found a moderate heritability of ∆TL (h2 = 0.21), which was higher than the heritabilities of early-life TL (h2 = 0.14) and later-life TL measurements (h2 = 0.15). Cohort effects explained considerable proportions of variation in early-life TL (60%), later-life TL (53%), and ∆TL (37%), which suggests persistent impacts of the early-life environment on lifelong telomere dynamics. Individual changes in TL were independent of early-life TL. Finally, there was weak evidence for population differences in ∆TL that may be linked to ecological differences in habitat types. Combined, our results show that individual telomere biology is highly dynamic and influenced by both genetic and environmental variation in natural conditions.
Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits.
Closer integration between behavioral ecology and quantitative genetics has resulted in a recent increase in studies partitioning sources of variation in labile traits. Repeatable between-individual differences are commonly documented, and their existence is generally explained using adaptive arguments, implying that selection has shaped variation at the among- and within-individual level. However, predicting the expected pattern of non-adaptive phenotypic variation around an optimal phenotypic value is difficult, hampering our ability to provide quantitative assessments of the adaptive nature of observed patterns of phenotypic variation within a population. We argue that estimating the strength of selection on trait variation among and within individuals provides a way to test adaptive theory concerned with phenotypic variation. To achieve this aim, we describe a nonlinear selection analysis that enables the study of the selective pressures on trait means and their among- and within-individual variation. By describing an integrative approach for studying the strength of selection on phenotypic variation at different levels, we hope to stimulate empirical studies investigating the ecological factors that can shape the repeatability, heritability, and coefficients of variation of labile and other repeatedly expressed traits.
Social evolution and the dynamics of social interactions have previously been studied under the frameworks of quantitative genetics and behavioural ecology. In quantitative genetics, indirect genetic effects of social partners on the socially plastic phenotypes of focal individuals typically lack crucial detail already included in treatments of social plasticity in behavioural ecology. Specifically, whilst focal individuals (e.g. receivers) may show variation in their 'responsiveness' to the social environment, individual social partners (e.g. signallers) may have a differential 'impact' on focal phenotypes. Here we propose an integrative framework, that highlights the distinction between responsiveness versus impact in indirect genetic effects for a range of behavioural traits. We describe impact and responsiveness using a reaction norm approach and provide statistical models for the assessment of these effects of focal and social partner identity in different types of social interactions. By providing such a framework, we hope to stimulate future quantitative research investigating the causes and consequences of social interactions on phenotypic evolution.
Estimating the genetic variation underpinning a trait is crucial to understanding and predicting its evolution. A key statistical tool to estimate this variation is the animal model . Typically, the environment is modelled as an external variable independent of the organism, affecting the focal phenotypic trait via phenotypic plasticity. We studied what happens if the environment is not independent of the organism because it chooses or adjusts its environment, potentially creating non‐zero genotype–environment correlations. We simulated a set of biological scenarios assuming the presence or absence of a genetic basis for a focal phenotypic trait and/or the focal environment (treated as an extended phenotype), as well as phenotypic plasticity (the effect of the environment on the phenotypic trait) and/or ‘environmental plasticity’ (the effect of the phenotypic trait on the local environment). We then estimated the additive genetic variance of the phenotypic trait and/or the environment by applying five animal models which differed in which variables were fitted as the dependent variable and which covariates were included. We show that animal models can estimate the additive genetic variance of the local environment (i.e. the extended phenotype) and can detect environmental plasticity. We show that when the focal environment has a genetic basis, the additive genetic variance of a phenotypic trait increases if there is phenotypic plasticity. We also show that phenotypic plasticity can be mistakenly inferred to exist when it is actually absent and instead environmental plasticity is present. When the causal relationship between the phenotype and the environment is misunderstood, it can lead to severe misinterpretation of the genetic parameters, including finding ‘phantom’ genetic variation for traits that, in reality, have none. We also demonstrate how using bivariate models can partly alleviate these issues. Finally, we provide the mathematical equations describing the expected estimated values. This study highlights that not taking gene–environment correlations into account can lead to erroneous interpretations of additive genetic variation and phenotypic plasticity estimates. If we aim to understand and predict how organisms adapt to environmental change, we need a better understanding of the mechanisms that may lead to gene–environment correlations.
An animal’s behavioral phenotype comprises several traits, which are hierarchically structured in functional units. This is manifested in measured behaviors often being correlated, partly reflecting the need of a coordinated functional response. Unfortunately, we still have limited understanding whether consistent differences in animal behaviors are due to underlying physiological constraints or a result of plastic adaptation to their current environment. Therefore, characterizing the spatial distribution of behaviors can provide important insights into causes and consequences of behavioral variation. In the present study, we quantified behaviors in a wild, free-ranging population of the Neotropical frog Allobates femoralis . We investigated how these behaviors were linked to the frogs’ natural and social environment and quantified the extent to which these behaviors consistently differed among individuals (i.e., animal personality). We assessed levels of aggressiveness, exploration, and boldness by measuring several underlying behaviors expressed in a set of experimental assays, and found evidence for consistent among-individual differences along these axes. Contrary to our expectation, there was no relationship between individual behaviors and their natural environment, but we found a plastic response of males to changes in female density, which might reflect how individuals cope with their socio-ecological environment. Significance statement How are behavioral phenotypes distributed across space? Here, we studied an entire free-ranging population of poison frogs, and investigated if the personality traits aggressiveness, exploration, and boldness are linked to the frogs’ natural or social environment. We found that behavioral traits were non-randomly distributed across the population, suggesting that the spatial arrangement of behavioral traits reflects how individuals cope with their complex natural and social environment.
Intra-specific aggressive interactions play a prominent role in the life of many animals. While studies have found evidence for repeatability in boldness, activity, and exploration in amphibians, we know relatively little about consistent among-individual variation in aggressiveness, despite its importance for male-male competition and territoriality. Amphibians, and Neotropical poison frogs (Dendrobatidae) in particular, are highly suitable for investigating among-individual variation in aggressiveness, as most species exhibit strong territoriality in at least one of the sexes. In the present study, we aimed to fill this gap in knowledge, by investigating within- and between-individual variation in territorial aggression in a semi-natural population of the Neotropical poison frog Allobates femoralis (Dendrobatidae) in French Guiana. We conducted repeated, standardized behavioral tests to assess if the level of territorial aggression is consistent within and different between individuals. Further, we tested a possible link between body size and level of territorial aggression. We found moderate repeatability in territorial aggressiveness, but no link to age and/or body size. In conclusion, our study represents the first documentation of repeatable aggressive behavior in a territorial context in amphibians.
Environmental conditions during early-life development can have lasting effects shaping individual heterogeneity in fitness and fitness-related traits. The length of telomeres, the DNA sequences protecting chromosome ends, may be affected by early-life conditions, and telomere length (TL) has been associated with individual performance within some wild animal populations. Thus, knowledge of the mechanisms that generate variation in TL, and the relationship between TL and fitness, is important in understanding the role of telomeres in ecology and life-history evolution. Here, we investigate how environmental conditions and morphological traits are associated with early-life blood TL and if TL predicts natal dispersal probability or components of fitness in 2746 wild house sparrow (Passer domesticus) nestlings from two populations sampled across 20 years (1994-2013). We retrieved weather data and we monitored population fluctuations, individual survival, and reproductive output using field observations and genetic pedigrees. We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non-dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success. Our study showed how early-life TL is shaped by effects of growth, weather conditions, and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, shorter telomeres may be associated with a faster pace-of-life, as individuals with higher dispersal rates and annual reproduction tended to have shorter early-life TL.
Generation time determines the pace of key demographic and evolutionary processes. Quantified as the weighted mean age at reproduction, it can be studied as a life-history trait that varies within and among populations and may evolve in response to ecological conditions. We combined quantitative genetic analyses with age- and density-dependent models to study generation time variation in a bird metapopulation. Generation time was heritable, and males had longer generation times than females. Individuals with longer generation times had greater lifetime reproductive success but not a higher expected population growth rate. Density regulation acted on recruit production, suggesting that longer generation times should be favoured when populations are closer to carrying capacity. Furthermore, generation times were shorter when populations were growing and longer when populations were closer to equilibrium or declining. These results support classic theory predicting that density regulation is an important driver of the pace of life-history strategies.
Dispersal has a crucial role determining ecoevolutionary dynamics through both gene flow and population size regulation. However, to study dispersal and its consequences, one must distinguish immigrants from residents. Dispersers can be identified using telemetry, capture‐mark‐recapture (CMR) methods, or genetic assignment methods. All of these methods have disadvantages, such as high costs and substantial field efforts needed for telemetry and CMR surveys, and adequate genetic distance required in genetic assignment. In this study, we used genome‐wide 200K Single Nucleotide Polymorphism data and two different genetic assignment approaches (GSI_SIM, Bayesian framework; BONE, network‐based estimation) to identify the dispersers in a house sparrow ( Passer domesticus ) metapopulation sampled over 16 years. Our results showed higher assignment accuracy with BONE. Hence, we proceeded to diagnose potential sources of errors in the assignment results from the BONE method due to variation in levels of interpopulation genetic differentiation, intrapopulation genetic variation and sample size. We show that assignment accuracy is high even at low levels of genetic differentiation and that it increases with the proportion of a population that has been sampled. Finally, we highlight that dispersal studies integrating both ecological and genetic data provide robust assessments of the dispersal patterns in natural populations.
Anthropogenic noise (≤ 3 kHz) can affect key features of birds’ acoustic communication via two different processes: (1) song‐learning, because songbirds need to hear themselves and other birds to crystallize their song, and (2) avoidance of song elements that overlap with anthropogenic noise. In this study we tested whether anthropogenic noise reduces the number of song elements in the repertoire of House Wren Troglodytes aedon , an urban species. Additionally, we tested whether the proportion of high‐frequency elements (i.e. elements where the minimum frequency is above 3 kHz) is related to anthropogenic noise levels, and how the frequencies and duration of shared elements between males change with different levels of anthropogenic noise. We recorded 29 House Wren males exposed to different anthropogenic noise levels (36.50–79.50 dB) during two consecutive breeding seasons from four locations. We recorded each male on 2 days during each season continuously for 50 min (we collected 104 h of recordings) and measured anthropogenic noise levels every 10 min inside each male territory during the recording period. In general, individuals inhabiting noisier territories had smaller repertoires. However, only in two locations with anthropogenic noise levels between 38.60 and 79.50 dB did males inhabiting noisier territories have smaller repertoires. In the other two locations with lower anthropogenic noise (36.50–66.50 dB), the anthropogenic noise inside each territory was not related to the repertoire size. Individuals inhabiting the noisiest location showed a tendency to include more high‐frequency elements in their songs. In 26% of the elements, the anthropogenic noise affected their frequency features. Our results showed that not all House Wrens inhabiting urban environments modify their songs at the highest level of organization (i.e. repertoire) to reduce the masking effect of anthropogenic noise on acoustic communication.