Background Acoustics in Terrestrial Ecology

The way in which terrestrial organisms use the acoustic realm is fundamentally important and shapes behavior, populations, and communities, but how background acoustics, or noise, influence the patterns and processes in ecology is still relatively understudied. In this review, we summarize how background acoustics have traditionally been studied from the signaling perspective, discuss what is known from a receiver\u27s perspective, and explore what is known about population- and community-level responses to noise. We suggest that there are major gaps linking animal physiology and behavior in noise to fitness; that there is a limited understanding of variation in hearing within and across species, especially in the context of real-world acoustic conditions; and that many puzzling responses to noise could be clarified with a community-level lens that considers indirect effects. Failing to consider variation in acoustic conditions, and the many ways organisms use and interact via this environmental dimension, risks a limited understanding of natural systems

Revisiting the drivers of acoustic similarities in tropical anuran assemblages

Acoustic signaling is key in mediating mate-choice, which directly impacts individual fitness. Because background noise and habitat structure can impair signal transmission, the acoustic space of mixed-species assemblages has long been hypothesized to reflect selective pressures against signal interference and degradation. However, other potential drivers that received far less attention can drive similar outputs on the acoustic space. Phylogenetic niche conservatism and allometric constraints may also modulate species acoustic features, and the acoustic space of communities could be a side-effect of ecological assembly processes involving other traits (e.g. environmental filtering). Additionally, the acoustic space can also reflect the sorting of species relying on public information through extended communication networks. Using an integrative approach, we revisit the potential drivers of the acoustic space by addressing the distribution of acoustic traits, body size, and phylogenetic relatedness in tropical anuran assemblages across gradients of environmental heterogeneity in the Pantanal wetlands. We found the overall acoustic space to be aggregated compared with null expectations, even when accounting for confounding effects of body size. Across assemblages, acoustic and phylogenetic differences were positively related, while acoustic and body size similarities were negatively related, although to a minor extent. We suggest that acoustic partitioning, acoustic adaptation, and allometric constraints play a minor role in shaping the acoustic output of tropical anuran assemblages and that phylogenetic niche conservatism and public information use would influence between-assemblage variation. Our findings highlight an overlooked multivariate nature of the acoustic dimension and underscore the importance of including the ecological context of communities to understand drivers of the acoustic space

Geographic variation in the phenotype of an African horseshoe bat species, Rhinolophus damarensis, (Chiroptera: Rhinolophidae)

Studies involving geographic variation in the phenotypes of bats help scientists to explain why these mammals are the most species rich mammalian order second only to rodents, with well more than 1 300 species occurring worldwide. Such species richness or high diversity is the manifestation of the generation of biodiversity through the splitting of lineages within bat species. A lineage of bat species can diversify into several lineages which then differentiate from each other in allopatry. Thus, the spatial separation of a lineage into several lineages could be attributed to geographical, ecological and environmental factors across the distributional range of the species. Similarly, vicariant events may also play a role in separating lineages within species. The Damara horseshoe bat species, Rhinolophus damarensis, is widely distributed but restricted to the western half of southern Africa, where it occurs across several major biomes. Formerly regarded as the subspecies, R. darlingi damarensis, it was elevated to full species status on the basis of genetic and phenotypic differences between it and R. darlingi darlingi. Rhinolophus damarensis is itself made up of two ecologically separated genetic lineages. A total of 106 individuals of R. damarensis were sampled from seven localities across its distributional range, with a view to determining and documenting the extent of geographic variation in body size, echolocation parameters, wing parameters, cranial shape and postcranial morphology of individuals from populations of R. damarensis across the distributional range of the species. Firstly, an investigation into geographic variation in resting echolocation frequency (RF) of the horseshoe bat species, R. damarensis was carried out in the western half of southern Africa (Chapter 2). Three hypotheses were tested. The first one, James’Rule (JR), states that individuals occurring in hot humid environments generally have smaller body sizes than conspecifics that occur in cooler, dryer environments, and the largest are expected to occur in cool, dry areas. On this basis and because of the known relationship between body size and RF, it was predicted that there should be a correlation between body size and climatic factors and between body size and RF. The second hypothesis was Isolation by Environment (IbE) mediated through sensory drive, which proposes that diversification of lineage may be driven by environmentally-mediated differences in sensory systems. Under this hypothesis, it was predicted that call frequency variation should be correlated with climatic variables. The third hypothesis was that Isolation by Distance (IbD) can influence phenotypic trait variation by restricting gene flow between populations. Under the Isolation by Distance (IbD) Hypothesis, it was predicted that call frequency variation should be partitioned in accordance with geographic distance between populations. To investigate the probability of the JR, IbE and IbD, the Akaike’s information criterion AICc candidate models were evaluated with different combinations of environmental (annual mean temperature and relative humidity), spatial (latitude and region) and biological (forearm as a proxy for body size) predictor variables to determine their influence on resting frequency (RF) across the distributional range of R. damarensis. Linear mixed effects models (LMEs) were employed to analyse the relationship between the response variable (RF) and the environmental, spatial and biological predictor variables. The influence of prey detection range and atmospheric attenuation was also investigated. The results showed no evidence for JR or for random genetic drift. Body size was neither correlated with RF nor environmental variables, suggesting that variation in RF was not the result of concomitant variation in body size as proposed by JR. Similarly, the Mantel test showed no IbD effect and there was therefore no evidence that genetic drift was responsible for the variation in RFs. In contrast, the LMEs showed that there was support for IbE in the form of an association between RF and region (in the form of the variable “Reg”) which was based on the two geographically separated genetic lineages. Furthermore, RF variation was also associated with the climatic variable AMT. The taxonomic status of R. damarensis was investigated using ecological traits and phenotypic characters including skulls, wings and echolocation (Chapter 3) and three dimensional (3D) scanned skulls and mandibles (Chapter 4). The main objective (Chapter 3 and Chapter 4) was to test whether previously reported genetic divergence between the two R. damarensis lineages was associated with phenotypic divergence. Morphometric and echolocation measurements were taken from hand held individual bats in the field, and skull measurements were taken from field collected voucher specimens as well as museum specimens. Discriminant Function Analyses (DFA) revealed that there was geographic variation among populations and lineages of R. damarensis. Multivariate Linear Regressions (MLV) and Linear models (LM) on the basal parts of bacula revealed significant differences between the southern and northern lineages of R. damarenis. The bacula of the two lineages of R. damarensis appear to have different shapes. Diversification through shape analyses (Chapter 4) was investigated using three dimensional (3D) geometric morphometric analyses based on X-ray microcomputed tomography (µCT) scanning of dried skulls and mandibles of R. damarensis. Procrustes Anova results of both mandibles and skulls indicated that there were no significant differences between sexes but that the shape of skulls and mandibles varied across different localities (Chapter 4). Canonical Variate Analysis (CVA) suggested that geographic variation in R. damarensis mandibles was based on the shape and thickness of the alveolar bone. Geographic variation in the skulls was based on changes in the rostrum, anterior medial swelling and brain case. Some populations had slightly deeper rostra, slightly larger anterior medial swellings and smaller braincases, whilst others had slightly shallower rostra, slightly smaller anterior medial swellings and larger braincases. The northern lineage was found to be separated from the southern lineage based on the changes in skull and mandible shape. Therefore, separation of lineages within R. damarensis (Chapter 4) could be associated with the foraging and feeding behaviour of the species under different ecological conditions due to ecological opportunity. Overall, differences in the RF were found to be associated with Isolation by Environment mediated through sensory drive and this has led to the formation of two regional (northern and southern) groupings in RF (Chapter 2). The two lineages were supported by both the phenotypic divergence (Chapter 3) and shape variation within R. damarensis skulls and mandibles (Chapter 4). Thus, phenotypic differences corresponded to genetic differences between the two lineages and provide support for IbE

Geographic Variation in Rock Wren (Salpinctes Obsoletus) Song Complexity

Birds sing to advertise for mates and repel rivals, but there is enormous variety in how they do this. One of the best-studied and most intriguing questions in the field is how song varies in complexity from one bird to the next, at all taxonomic levels. Several studies have found associations between migratory behavior or latitudinal gradients and song complexity, but it remains unclear how universal this pattern is or what factors may be driving it. This small body of literature suffers from several problems, perhaps the most glaring of which is the lack of systematic, population-level studies. The main goals of this dissertation were to determine what evidence there is for the hypothesis that song complexity is influenced by latitude and/or migratory behavior and whether such a pattern can be detected in a single species, the rock wren (Salpinctes obsoletus). I recorded rock wren song at 11 sites in a latitudinal transect with both migratory and sedentary populations, and used morphological measurements and genome-level SNP scans to test my classification scheme of migratory versus sedentary populations. Song repertoire size was larger in sedentary rock wrens but did not vary with latitude, while migratory wrens had smaller mean repertoire sizes which increased with increasing latitude. Morphological measurements differed between migratory and sedentary populations, suggesting life history differences between these two groups. Population genetic structure was only apparent using outlier loci, but the resulting structure was not concordant with migratory behavior or site membership. Taken together, these results suggest migration does not pose a barrier to gene flow between migratory and sedentary populations, and that migratory and sedentary behavior is associated with differences in song complexity and morphology, although in a way inconsistent with any previously published hypotheses

Measuring communicative complexity across modalities: a new framework in the context of the “social complexity hypothesis” and its application in true lemurs

Mesurer la complexité communicationnelle à travers les modalités : un nouveau cadre dans le contexte de l'"hypothèse de la complexité sociale" et son application chez les lémuriens. Les animaux présentent une étonnante diversité de systèmes de communication, avec des variations substantielles tant dans la nature que dans le nombre de signaux qu'ils produisent. La variation de la complexité communicationnelle a été conceptuellement et empiriquement attribuée à la complexité sociale et formulée comme "l'hypothèse de la complexité sociale" (SCHCC pour “Social-Complexity Hypothesis for Communicative Complexity”). En effet, les animaux vivant en groupe sont confrontés à des environnements sociaux complexes où ils s'engagent dans un large éventail d'interactions avec différents partenaires sociaux, ce qui rend nécessaire la transmission d'une plus grande diversité de messages. Dans le chapitre I (Peckre et al. 2019), je passe en revue la littérature sur les tests actuels de la SCHCC, en soulignant et en discutant ce que j'ai identifié comme les principales lacunes dans l'état de l'art. Plus précisément, trois questions clés sont ressorties de mon analyse. La première question concerne la définition opérationnelle des variables principales, complexité sociale et communicationnelle. Notamment, pour définir la complexité communicative, la plupart des tests empiriques de la SCHCC se concentrent sur une seule modalité (par exemple, acoustique, visuelle, olfactive) alors qu'il existe plusieurs bonnes raisons de reconnaître la nature multimodale des signaux et des systèmes communicatifs dans ce cadre. Au niveau du système, se concentrer sur une seule modalité peut conduire à une sur- ou sous-estimation de la relation entre la complexité sociale et communicative. La deuxième question concerne le fait que, si de nombreuses études ont mis en évidence un lien entre la complexité sociale et communicative, leur nature corrélative ne permet pas de conclure sur la direction de cette causalité. En effet, des hypothèses alternatives impliquant des facteurs anatomiques, phylogénétiques ou écologiques ont également été proposées pour expliquer l'évolution de formes de communication plus complexes. Enfin, je note que les chercheurs se penchent rarement sur la nature réelle des liens par lesquels les facteurs sociaux affectent directement la variation de l’expression des signaux. En effet, les mécanismes sous-jacents à ces liens sont généralement laissés inexplorés, ne permettant pas de mettre en lumière l'attribut spécifique de la communication qui évoluerait conjointement avec des aspects spécifiques de la socialité. Je plaide donc en faveur d'une extension des tests de la SCHCC en termes 1) d'étendue (approche systématique à travers les différentes modalités de communication) et 2) de profondeur (caractérisation des relations observées), car je pense que cela pourrait faire progresser de manière significative notre compréhension des liens complexes entre socialité et communication animales. Pour aborder le point 1), je propose dans le chapitre II une approche globale des systèmes de communication intermodale de deux espèces cousines de lémuriens, ayant une morphologie similaire, vivant dans des habitats similaires, mais différant dans leurs systèmes sociaux. J'ai étudié des Eulemur rufifrons et des E. mongoz en liberté à Madagascar, respectivement dans les forêts de Kirindy et d'Ankatsabe pendant 12 mois. Je décris un nouveau cadre analytique pour évaluer la complexité des systèmes de signalisation à travers les différentes modalités de communication. L'application d'une approche multimodale peut aider à mettre en lumière les différentes pressions sélectives agissant sur le système de communication et à mieux comprendre les fonctions adaptatives qui pourraient être invisibles par l'étude indépendante de ses composants séparés. E. rufifrons, l'espèce ayant le système social le plus complexe, avait également un système de communication globalement plus complexe que celui d'E. mongoz. Le choix minutieux des espèces à comparer pour limiter l'effet d'éventuelles pressions sélectives supplémentaires et l'exploration de la fonction sociale des signaux non-homologues permettent de conclure que cette complexité accrue du système de communication chez E. rufifrons est très probablement associée à des pressions sélectives sociales. J'ai développé ce nouveau cadre analytique, en partie basé sur l'utilisation d'une approche de réseau inter-modalités, dans l'optique de faciliter les comparaisons inter-taxonomiques. De plus, cette approche peut être combinée avec de nouvelles approches multidimensionnelles de la complexité sociale et contribuer à une approche plus holistique des tests de la SCHCC. Ainsi, nous devrions être en mesure de dériver de nouvelles hypothèses testables qui contribueraient à mieux comprendre le cours des événements qui ont conduit à l'évolution de la diversité de la communication dans ses différentes dimensions. Dans le chapitre III, j'aborde le point 2) en étudiant les impacts de la socialité sur l'expression d'un signal multimodal, le comportement de marquage olfactif anogénital chez les lémuriens à front roux. J'ai spécifiquement étudié les effets de l'audience intragroupe sur les comportements de marquage olfactif anogénital dans une population de lémuriens à front roux en liberté, en particulier si les mâles et les femelles diffèrent dans cet aspect et si ces différences peuvent révéler des différences fonctionnelles associées au marquage olfactif anogénital entre les sexes. J'ai trouvé un effet d'audience intragroupe chez les mâles mais pas chez les femelles. Les mâles déposaient moins souvent des marques anogénitales lorsque qu’un plus grand nombre de mâles étaient présents dans un rayon de trois mètres (mais pas de cinq ou dix mètres). Les mâles pourraient préférer réduire le risque de contact physique en évitant de marquer près d'autres mâles, et/ou donner la priorité aux autres mâles pour marquer. Avec ces résultats, je fournis des informations importantes sur la signification fonctionnelle du marquage olfactif anogénital chez les lémuriens à front roux et je soutiens l'idée de pressions sociales intragroupe plus importantes associées au marquage olfactif anogénital chez les mâles que chez les femelles chez les espèces égalitaires. L'étude de la flexibilité de l'utilisation des signaux complexes (par exemple, l'occurrence ou les modifications structurelles) en fonction des contextes sociaux (audiences) devrait permettre d'identifier les différentes caractéristiques sociales individuelles qui peuvent susciter ou limiter l'expression de signaux complexes. Ces caractéristiques peuvent ensuite constituer des pressions sociales agissant pour ou contre l'évolution de ces comportements de signalisation complexes. Dans les chapitres IV et V, j'aborde également les questions éthiques liées à ce projet et la manière dont j'ai essayé de m'adapter et d'assumer au mieux mes responsabilités en matière de bien-être animal. Dans le chapitre IV, j'expose certains détails techniques et les problèmes éthiques rencontrés lors du choix de mes sites de terrain. Dans le chapitre V (Buil and Peckre et al. 2019), je présente un système de collier détachable à distance développé en collaboration avec le Laboratoire de neurobiologie (Centre allemand des primates, Göttingen, Allemagne) dans le but de fournir un outil permettant de réduire de manière significative le nombre de captures dans les études utilisant le bio-logging pour les espèces de mammifères de taille moyenne. Globalement, en soulignant l'importance de la nature multimodale des systèmes de communication et du contexte social dans lequel les signaux sont échangés, j'espère stimuler le développement de nouveaux tests de la SCHCC basés sur ce cadre élargi. En outre, j'insiste sur l'importance de regarder à travers les domaines de recherche, car des parallèles frappants peuvent être observés entre le comportement animal et la recherche linguistique lorsqu'on aborde les origines de la complexité de la communication, que ce soit sous la forme du langage humain ou de la communication animale

Acoustic Communication in Colonial Seabirds: Individual, Sexual, and Species-Specific Variation in Acoustic Signals of Pterodroma Petrels

Acoustic communication is an integral component of social interactions in procellariid seabirds (petrels), and a substantial amount of research has been devoted to the vocalizations and vocal behavior in this family. This work has shown that petrels' calls contain information about the species, sex, and identity of the caller. Experiments have confirmed that these features are used to recognize conspecifics, mates, and other individuals in many species. Relatively little is known, however, about vocalizations in the genus Pterodroma, which contains 40% of the species in the family. My research on Pterodroma externa in the Islas Juan Fernández confirmed sexual dimorphism in the calls of this species and showed that their burrow calls differ among individuals. Both Linear Discriminant Functions and Probabilistic Neural Nets classified individuals by their calls with high accuracy. Acoustic censuses in a mixed colony of Pterodroma externa and P. longirostris showed that both of these nocturnal species increased vocal activity on nights with moonlight. Different tradeoffs between the risk of predation and the risk of collision in the dark might explain differences in the timing of their nocturnal activity. In addition, I compared aerial vocalizations in a closely related group of Pterodroma species in the subgenus Cookilaria. The similarities in the calls produced by these species suggest that vocalizations can provide useful information for understanding the phylogenetic relationships of species in this genus. Differences among the calls and activity patterns of these species, on the other hand, suggest a range of adaptations to the different environments they inhabit. One implication of these findings is that each colony of seabirds on remote islands might have an optimal pattern of activity that differs from those of colonies elsewhere. If immigrant individuals cannot adjust, these colony-specific patterns of activity could contribute to reproductive isolation between populations and thus to speciation in these birds

Acoustic indices as proxies for biodiversity: a meta-analysis

As biodiversity decreases worldwide, the development of effective techniques to track changes in ecological communities becomes an urgent challenge. Together with other emerging methods in ecology, acoustic indices are increasingly being used as novel tools for rapid biodiversity assessment. These indices are based on mathematical formulae that summarise the acoustic features of audio samples, with the aim of extracting meaningful ecological information from soundscapes. However, the application of this automated method has revealed conflicting results across the literature, with conceptual and empirical controversies regarding its primary assumption: a correlation between acoustic and biological diversity. After more than a decade of research, we still lack a statistically informed synthesis of the power of acoustic indices that elucidates whether they effectively function as proxies for biological diversity. Here, we reviewed studies testing the relationship between diversity metrics (species abundance, species richness, species diversity, abundance of sounds, and diversity of sounds) and the 11 most commonly used acoustic indices. From 34 studies, we extracted 364 effect sizes that quantified the magnitude of the direct link between acoustic and biological estimates and conducted a meta-analysis. Overall, acoustic indices had a moderate positive relationship with the diversity metrics (r = 0.33, CI [0.23, 0.43]), and showed an inconsistent performance, with highly variable effect sizes both within and among studies. Over time, studies have been increasingly disregarding the validation of the acoustic estimates and those examining this link have been progressively reporting smaller effect sizes. Some of the studied indices [acoustic entropy index (H), normalised difference soundscape index (NDSI), and acoustic complexity index (ACI)] performed better in retrieving biological information, with abundance of sounds (number of sounds from identified or unidentified species) being the best estimated diversity facet of local communities. We found no effect of the type of monitored environment (terrestrial versus aquatic) and the procedure for extracting biological information (acoustic versus non-acoustic) on the performance of acoustic indices, suggesting certain potential to generalise their application across research contexts. We also identified common statistical issues and knowledge gaps that remain to be addressed in future research, such as a high rate of pseudoreplication and multiple unexplored combinations of metrics, taxa, and regions. Our findings confirm the limitations of acoustic indices to efficiently quantify alpha biodiversity and highlight that caution is necessary when using them as surrogates of diversity metrics, especially if employed as single predictors. Although these tools are able partially to capture changes in diversity metrics, endorsing to some extent the rationale behind acoustic indices and suggesting them as promising bases for future developments, they are far from being direct proxies for biodiversity. To guide more efficient use and future research, we review their principal theoretical and practical shortcomings, as well as prospects and challenges of acoustic indices in biodiversity assessment. Altogether, we provide the first comprehensive and statistically based overview on the relation between acoustic indices and biodiversity and pave the way for a more standardised and informed application for biodiversity monitoringThis study was supported by a research project funded by the Comunidad de Madrid and the European Social Fund (PEJ2018-AI/AMB-9957, to D. L.). We thank Camille Desjonquères for her valuable comments on the study design, Alison Cooper for her exhaustive and insightful revision of the manuscript, and anonymous reviewers for their significant contribution. I. A. and L. S. M. S. acknowledge research grants provided by the Comunidad de Madrid (PEJ-2018-AI/ AMB-9957, to D. L.) and the Ministerio de Economía, Industria y Competitividad of Spain (PEJ-2018-004603-A, to D. L.), respectively, together with the support of the European Social Fund. H. L. was supported by the FPI program of the Ministerio de Ciencia e Innovacion of Spain (grant CGL2017-86926-P). D. L. also acknowledges a postdoctoral grant provided by the Comunidad de Madrid (2020-T1/AMB-20636, Atraccion de Talento Investigador, Spain) and a research project funded by the Ministerio de Economía, Industria y Competitividad (CGL2017-88764-R, MINECO/AEI/FEDER, Spain

Methodological approaches for sound training in underepresented learners: a case study with american toads (anaxyrus americanus)

efforts to better understand the minds of animals have been flourishing, with methodological breakthroughs and a remarkable increase in the number of publications dealing with a wide variety of non-model species. The growing interest in species that are distantly related to humans in the field of comparative physiology and cognition was confirmed with the general reviewed performed in this dissertation. Yet, the progress is unbalanced among the ectothermic vertebrates (fish, reptiles, and amphibians), with almost no research on amphibians. Many animals remain unstudied, even though they may possess unique and powerful adaptations to respond to environmental stimuli that can be useful for learning and cognition research. Inspired by the efforts to increase species representation in studies of learning and cognition, this dissertation also explored two methods of spatial learning to train American toads to respond to tone burst cues in order to find the reward. As frogs and toads have been able to acquire maze task associated to visual cues and mating calls, I predicted that a protocol based on these previously successful methods could be reliable in testing toads to associate and discriminate tone bursts of different frequencies (HZ). None of the methods were effective in demonstrate learning abilities in American toads, but the results pointed to important challenges to calibrate methods for future studies. Aspects to consider such as sex effects on side bias and can be used to reflect behavioral plasticity as a metric for the process of learning, such as time latency (longer it takes a toad to succeed, the more likely they will be successful) and the behavior displayed during the task as an indication of behavioral flexibility for decision making. Besides these aspects of the procedure, there are physiological and evolutionary aspects that might make toads unable to interact with non-mating sounds. These aspects and the level of hearing constraints that can affect learning assessment in toads are critical to answer broad questions on anuran auditory role beyond mating purposes

Multi-modal signal evolution in birds: re-examining a standard proxy for sexual selection

Sexual selection is proposed to be an important driver of speciation and phenotypic diversification in animal systems. However, previous phylogenetic tests have produced conflicting results, perhaps because they have focused on a single signalling modality (visual ornaments), whereas sexual selection may act on alternative signalling modalities (e.g. acoustic ornaments). Here, we compile phenotypic data from 259 avian sister species pairs to assess the relationship between visible plumage dichromatism-a standard index of sexual selection in birds-and macroevolutionary divergence in the other major avian signalling modality: song. We find evidence for a strong negative relationship between the degree of plumage dichromatism and divergence in song traits, which remains significant even when accounting for other key factors, including habitat type, ecological divergence and interspecific interactions. This negative relationship is opposite to the pattern expected by a straightforward interpretation of the sexual selection-diversification hypothesis, whereby higher levels of dichromatism indicating strong sexual selection should be related to greater levels of mating signal divergence regardless of signalling modality. Our findings imply a 'trade-off' between the elaboration of visual ornaments and the diversification of acoustic mating signals, and suggest that the effects of sexual selection on diversification can only be determined by considering multiple alternative signalling modalities