Towards acoustic monitoring of bees: wingbeat sounds are related to species and individual traits.

Global pollinator decline urgently requires effective methods to assess their trends, distribution and behaviour. Passive acoustics is a non-invasive and cost-efficient monitoring tool increasingly employed for monitoring animal communities. However, insect sounds remain highly unexplored, hindering the application of this technique for pollinators. To overcome this shortfall and support future developments, we recorded and characterized wingbeat sounds of a variety of Iberian domestic and wild bees and tested their relationship with taxonomic, morphological, behavioural and environmental traits at inter- and intra-specific levels. Using directional microphones and machine learning, we shed light on the acoustic signature of bee wingbeat sounds and their potential to be used for species identification and monitoring. Our results revealed that frequency of wingbeat sounds is negatively related with body size and environmental temperature (between-species analysis), while it is positively related with experimentally induced stress conditions (within-individual analysis). We also found a characteristic acoustic signature in the European honeybee that supported automated classification of this bee from a pool of wild bees, paving the way for passive acoustic monitoring of pollinators. Overall, these findings confirm that insect sounds during flight activity can provide insights on individual and species traits, and hence suggest novel and promising applications for this endangered animal group. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

The potential of acoustic monitoring of aquatic insects for freshwater assessment.

Aquatic insects are a major indicator used to assess ecological condition in freshwater environments. However, current methods to collect and identify aquatic insects require advanced taxonomic expertise and rely on invasive techniques that lack spatio-temporal replication. Passive acoustic monitoring (PAM) is emerging as a non-invasive complementary sampling method allowing broad spatio-temporal and taxonomic coverage. The application of PAM in freshwater ecosystems has already proved useful, revealing unexpected acoustic diversity produced by fishes, amphibians, submerged aquatic plants, and aquatic insects. However, the identity of species producing sounds remains largely unknown. Among them, aquatic insects appear to be the major contributor to freshwater soundscapes. Here, we estimate the potential number of soniferous aquatic insects worldwide using data from the Global Biodiversity Information Facility. We found that four aquatic insect orders produce sounds totalling over 7000 species. This number is probably underestimated owing to poor knowledge of aquatic insects bioacoustics. We then assess the value of sound producing aquatic insects to evaluate ecological condition and find that they might be useful despite having similar responses in pristine and degraded environments in some cases. Both expert and automated identifications will be necessary to build international reference libraries and to conduct acoustic bioassessment in freshwaters. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

On the function of a female-like signal type in the vibrational repertoire of Enchenopa male treehoppers (Hemiptera: Membracidae).

Animals often mimic the behaviours or signals of conspecifics of the opposite sex while courting. We explored the potential functions of a novel female-like signal type in the courtship displays of male Enchenopa treehoppers. In these plant-feeding insects, males produce plant-borne vibrational advertisement signals, to which females respond with their own duetting signals. Males also produce a signal type that resembles the female duetting responses. We experimentally tested whether this signal modifies the behaviour of receivers. First, we tested whether the female-like signal would increase the likelihood of a female response. However, females were as likely to respond to playbacks with or without them. Second, we tested whether the female-like signal would inhibit competing males, but males were as likely to produce displays after playbacks with or without them. Hence, we found no evidence that this signal has an adaptive function, despite its presence in the courtship display, where sexual selection affects signal features. Given these findings, we also explored whether the behavioural and morphological factors of the males were associated with the production of the female-like signal. Males that produced this signal had higher signalling effort (longer and more frequent signals) than males that did not produce it, despite being in worse body condition. Lastly, most males were consistent over time in producing the female-like signal or not. These findings suggest that condition-dependent or motivational factors explain the presence of the female-like signal. Alternatively, this signal might not bear an adaptive function, and it could be a way for males to warm up or practice signalling, or even be a by-product of how signals are transmitted through the plant. We suggest further work that might explain our puzzling finding that a signal in the reproductive context might not have an adaptive function.

Social Plasticity Enhances Signal-Preference Codivergence.

AbstractThe social environment is often the most dynamic and fitness-relevant environment animals experience. Here we tested whether plasticity arising from variation in social environments can promote signal-preference divergence-a key prediction of recent speciation theory but one that has proven difficult to test in natural systems. Interactions in mixed social aggregations could reduce, create, or enhance signal-preference differences. In the latter case, social plasticity could establish or increase assortative mating. We tested this by rearing two recently diverged species of Enchenopa treehoppers-sap-feeding insects that communicate with plant-borne vibrational signals-in treatments consisting of mixed-species versus own-species aggregations. Social experience with heterospecifics (in the mixed-species treatment) resulted in enhanced signal-preference species differences. For one of the two species, we tested but found no differences in the plastic response between sympatric and allopatric sites, suggesting the absence of reinforcement in the signals and preferences and their plastic response. Our results support the hypothesis that social plasticity can create or enhance signal-preference differences and that this might occur in the absence of long-term selection against hybridization on plastic responses themselves. Such social plasticity may facilitate rapid bursts of diversification.

The Indirect Genetic Effect Interaction Coefficient ψ: Theoretically Essential and Empirically Neglected.

The interaction effect coefficient ψ has been a much-discussed, fundamental parameter of indirect genetic effect (IGE) models since its formal mathematical description in 1997. The coefficient simultaneously describes the form of changes in trait expression caused by genes in the social environment and predicts the evolutionary consequences of those IGEs. Here, we report a striking mismatch between theoretical emphasis on ψ and its usage in empirical studies. Surveying all IGE research, we find that the coefficient ψ has not been equivalently conceptualized across studies. Several issues related to its proper empirical measurement have recently been raised, and these may severely distort interpretations about the evolutionary consequences of IGEs. We provide practical advice on avoiding such pitfalls. The majority of empirical IGE studies use an alternative variance-partitioning approach rooted in well-established statistical quantitative genetics, but several hundred estimates of ψ (from 15 studies) have been published. A significant majority are positive. In addition, IGEs with feedback, that is, involving the same trait in both interacting partners, are far more likely to be positive and of greater magnitude. Although potentially challenging to measure without bias, ψ has critically-developed theoretical underpinnings that provide unique advantages for empirical work. We advocate for a shift in perspective for empirical work, from ψ as a description of IGEs, to ψ as a robust predictor of evolutionary change. Approaches that "run evolution forward" can take advantage of ψ to provide falsifiable predictions about specific trait interactions, providing much-needed insight into the evolutionary consequences of IGEs.

A neglected conceptual problem regarding phenotypic plasticity's role in adaptive evolution: The importance of genetic covariance and social drive.

There is tantalizing evidence that phenotypic plasticity can buffer novel, adaptive genetic variants long enough to permit their evolutionary spread, and this process is often invoked in explanations for rapid adaptive evolution. However, the strength and generality of evidence for it is controversial. We identify a conceptual problem affecting this debate: recombination, segregation, and independent assortment are expected to quickly sever associations between genes controlling novel adaptations and genes contributing to trait plasticity that facilitates the novel adaptations by reducing their indirect fitness costs. To make clearer predictions about this role of plasticity in facilitating genetic adaptation, we describe a testable genetic mechanism that resolves the problem: genetic covariance between new adaptive variants and trait plasticity that facilitates their persistence within populations. We identify genetic architectures that might lead to such a covariance, including genetic coupling via physical linkage and pleiotropy, and illustrate the consequences for adaptation rates using numerical simulations. Such genetic covariances may also arise from the social environment, and we suggest the indirect genetic effects that result could further accentuate the process of adaptation. We call the latter mechanism of adaptation social drive, and identify methods to test it. We suggest that genetic coupling of plasticity and adaptations could promote unusually rapid 'runaway' evolution of novel adaptations. The resultant dynamics could facilitate evolutionary rescue, adaptive radiations, the origin of novelties, and other commonly studied processes.

Pond Acoustic Sampling Scheme: A draft protocol for rapid acoustic data collection in small waterbodies.

Freshwater conservation is vital to the maintenance of global biodiversity. Ponds are a critical, yet often under-recognized, part of this, contributing to overall ecosystem functioning and diversity. They provide habitats for a range of aquatic, terrestrial, and amphibious life, often including rare and declining species.Effective, rapid, and accessible survey methods are needed to enable evidence-based conservation action, but freshwater taxa are often viewed as "difficult"-and few specialist surveyors are available. Datasets on ponds are therefore limited in their spatiotemporal coverage.With the advent of new recording technologies, acoustic survey methods are becoming increasingly available to researchers, citizen scientists, and conservation practitioners. They can be an effective and noninvasive approach for gathering data on target species, assemblages, and environmental variables. However, freshwater applications are lagging behind those in terrestrial and marine spheres, and as an emergent method, research studies have employed a multitude of different sampling protocols.We propose the Pond Acoustic Sampling Scheme (PASS), a simple protocol to allow a standardized minimal sample to be collected rapidly from small waterbodies, alongside environmental and methodological metadata. This sampling scheme can be incorporated into a variety of survey designs and is intended to allow access to a wide range of participants, without requiring complicated or prohibitively expensive equipment.Adoption of this sampling protocol would enable consistent sound recordings to be gathered by researchers and conservation organizations, and allow the development of landscape-scale surveys, data sharing, and collaboration within an expanding freshwater ecoacoustic community-rather than individual approaches that produce incompatible datasets. The compilation of standardized data would improve the prospects for effective research into the soundscapes of small waterbodies and aid freshwater conservation efforts.

Juvenile social experience and practice have a switch-like influence on adult mate preferences in an insect.

Social causes of variation in animal communication systems have important evolutionary consequences, including speciation. The relevance of these effects depends on how widespread they are among animals. There is evidence for such effects not only in birds and mammals, but also frogs and some insects and spiders. Here, we analyze the social ontogeny of adult mate preferences in an insect, Enchenopa treehoppers. In these communal plant-feeding insects, individuals reared in isolation or in groups differ in their mate preferences, and the group-reared phenotype can be rescued by playbacks to isolation-reared individuals. We ask about the relative role of signaling experience and signaling practice during ontogeny on the development of adult mating preferences in Enchenopa females. Taking advantage of variation in the signal experience and signaling practice of isolation-reared individuals, we find switch-like effects for experience and practice on female mate preference phenotypes, with individuals having some experience and practice as juveniles best rescuing the group-reared preference phenotype. We discuss how understanding the nature and distribution of social-ontogenetic causes of variation in mate preferences and other sexual traits will bring new insights into how within- and between-population variation influences the evolution of communication systems.

The relationship between a combinatorial processing rule and a continuous mate preference function in an insect.

Mate choice involves processing signals that can reach high levels of complexity and feature multiple components, even in small animals with tiny brains. This raises the question of whether and how such organisms deal with this complexity. One solution involves combinatorial processing, whereby different signal elements are processed as single units. Combinatorial processing has been described in several mammals and birds, and recently in a vibrationally signalling insect, Enchenopa treehoppers. Here, we ask about the relationship between combinatorial rules and mate preferences for continuously varying signal features. Enchenopa male advertisement signals are composed of two elements: a 'whine' followed by a set of pulses. The dominant frequency of the whine and element combination both matter to females. We presented synthetic signals varying in element order (natural [whine-pulses], reverse [pulses-whine]) and in frequency to Enchenopa females and recorded their responses. The reverse combination resulted in a decrease in attractiveness of the signals, and also slightly changed the shape of the preference for frequency. We found that females could be classified into three 'types': females with both a strong preference and a strong combinatorial rule, females with both a weak preference and weak rule, and females with a strong preference but a weak rule. Our results suggest that in Enchenopa signal processing, the mate preference for a continuous signal feature 'takes precedence' over, but also interacts with, the combinatorial rule. The relationship between the preference and the rule could evolve to take different forms according to selection on mate choice decisions. We suggest that exploring the relationship between such preferences and rules in species with more complex signals will bring insight into the evolution of the multi-component communication systems.

Combinatorial Signal Processing in an Insect.

AbstractHuman language is combinatorial: phonemes are grouped into syllables, syllables are grouped into words, and so on. The capacity for combinatorial processing is present, in different degrees, in some mammals and birds. We used vibrational insects, Enchenopa treehoppers, to test the hypothesis of basic combinatorial processing against two competing hypotheses: beginning rule (where the early signal portions play a stronger role in acceptability) and no ordering rule (where the order of signal elements plays no role in signal acceptability). Enchenopa males use plant-borne vibrational signals that consist of a whine followed by pulses. We tested the above hypotheses with vibrational playback experiments in which we presented Enchenopa females with stimuli varying in signal element combinations. We monitored female responses to these playbacks with laser vibrometry. We found strong support for combinatorial processing in Enchenopa: in brief, females preferred natural-combination signals regardless of the beginning element and discriminated against reverse-order signals or individual elements. Finding support for the combinatorial rule hypothesis in insects suggests that this capability represents a common solution to the problems presented by complex communication.

Signalling interactions during ontogeny are a cause of social plasticity in Enchenopa treehoppers (Hemiptera: Membracidae).

We recently discovered that there is a social ontogeny of signals and preferences in Enchenopa treehoppers. Nymphs signalled throughout their development; some signal features changed gradually and in sexually dimorphic ways throughout ontogeny; and some adult male signal features and female mate preferences differed between individuals reared in isolation or groups. In this paper, we investigate whether signalling interactions during ontogeny are a cause of plasticity in mating signals and preferences. We subjected Enchenopa nymphs to treatments of either: rearing in aggregations (the natural condition), in isolation, or in isolation with playbacks of nymph signals. We then described variation in the signals and mating preferences of individuals that developed in those conditions. The playback treatments partially "rescued" the signal and preference phenotypes, resulting in phenotypes either similar to those that result from rearing in aggregations, or intermediate between those that result from rearing in isolation or in aggregations. These results pin-point signalling interactions during ontogeny as an important cause of plasticity in signals and mate preferences.

Acoustic communities reflects lateral hydrological connectivity in riverine floodplain similarly to macroinvertebrate communities.

Recent studies revealed that information on ecological patterns and processes can be investigated using sounds emanating from animal communities. In freshwater environments, animal communities are strongly shaped by key ecological factors such as lateral connectivity and temperature. We predict that those ecological factors are linked to acoustic communities formed by the collection of sounds emitted underwater. To test this prediction, we deployed a passive acoustic monitoring during 15 days in six floodplain channels of the European river Rhône. The six channels differed in their temperature and level of lateral connectivity to the main river. In parallel, we assessed the macroinvertebrate communities of these six channels using classical net sampling methods. A total of 128 sound types and 142 animal taxa were inventoried revealing an important underwater diversity. This diversity, instead of being randomly distributed among the six floodplain channels, was site-specific. Generalized mixed-effects models demonstrated a strong effect of both temperature and lateral connectivity on acoustic community composition. These results, congruent with macroinvertebrate community composition, suggest that acoustic communities reflect the interactions between animal communities and their environment. Overall our study strongly supports the perspectives offered by acoustic monitoring to describe and understand ecological patterns in freshwater environments.

First description of underwater acoustic diversity in three temperate ponds.

The past decade has produced an increased ecological interest in sonic environments, or soundscapes. However, despite this rise in interest and technological improvements that allow for long-term acoustic surveys in various environments, some habitats' soundscapes remain to be explored. Ponds, and more generally freshwater habitats, are one of these acoustically unexplored environments. Here we undertook the first long term acoustic monitoring of three temperate ponds in France. By aural and visual inspection of a selection of recordings, we identified 48 different sound types, and according to the rarefaction curves we calculated, more sound types are likely present in one of the three ponds. The richness of sound types varied significantly across ponds. Surprisingly, there was no pond-to-pond daily consistency of sound type richness variation; each pond had its own daily patterns of activity. We also explored the possibility of using six acoustic diversity indices to conduct rapid biodiversity assessments in temperate ponds. We found that all indices were sensitive to the background noise as estimated through correlations with the signal-to-noise ratio (SNR). However, we determined that the AR index could be a good candidate to measure acoustic diversities using partial correlations with the SNR as a control variable. Yet, research is still required to automatically compute the SNR in order to apply this index on a large data set of recordings. The results showed that these three temperate ponds host a high level of acoustic diversity in which the soundscapes were variable not only between but also within the ponds. The sources producing this diversity of sounds and the drivers of difference in daily song type richness variation both require further investigation. Such research would yield insights into the biodiversity and ecology of temperate ponds.

Cannibalism in the pea aphid, Acyrthosiphon pisum.

Previous observations of cannibalism have been made in the aphid Acyrthosiphon pisum (L.): this article seeks to quantify factors contributing to such behaviors. We observed and quantified the responses of a number of clones and life stages to varying levels of starvation, in the form of increasingly desiccated Vica faba L. plants (receiving 50, 25, or 10 mL every second day) or a complete absence of host plant. We found that, while the longest incidences of cannibalism are carried out by juveniles (F = 3.45, P = 0.019, df = 3) and targeted at adults, the starvation treatments had the most significant effect on the prevalence of cannibalism in mature A. pisum (F = 2.24, P = 0.025, df = 9). Furthermore, there was no difference between the prevalence or duration of cannibalistic activities within and between different clones (P ≥ 0.05 in all cases), though juveniles were more likely to target unrelated aphids (V = 6 112, P = 0.011), and spent more time feeding on aphids from the same culture (V = 6 062, P = 0.018).