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Animals vary in the complexity and size of the signal repertoire used in communication. Often, these behavioural repertoires include multiple signal types for the same process, for instance, courtship. In Enchenopa treehoppers (Hemiptera: Membracidae) mate-searching males produce plant-borne vibrational advertisement signals. Receptive females then respond to males with their own signals. Here we describe an additional signal type in the repertoire of these males. We collected nymphs in Wisconsin, USA, and recorded the spontaneous signalling bouts of adult males and duetting signals of females using laser vibrometry. Two-thirds of males produced the additional signal type, which differed in temporal and spectral features from the main male advertisement signals, whilst resembling female duetting signals in placement and acoustic features. Our findings suggest that this might be a female mimic signal. Overall, our findings highlight the diversity in the behavioural repertoire that animals may use for reproduction.

Funder: Canon Foundation in Europe; Id: http://dx.doi.org/10.13039/100005286, Passive acoustic monitoring (PAM) has emerged as a transformative tool for applied ecology, conservation and biodiversity monitoring, but its potential contribution to fundamental ecology is less often discussed, and fundamental PAM studies tend to be descriptive, rather than mechanistic. Here, we chart the most promising directions for ecologists wishing to use the suite of currently available acoustic methods to address long‐standing fundamental questions in ecology and explore new avenues of research. In both terrestrial and aquatic habitats, PAM provides an opportunity to ask questions across multiple spatial scales and at fine temporal resolution, and to capture phenomena or species that are difficult to observe. In combination with traditional approaches to data collection, PAM could release ecologists from myriad limitations that have, at times, precluded mechanistic understanding. We discuss several case studies to demonstrate the potential contribution of PAM to biodiversity estimation, population trend analysis, assessing climate change impacts on phenology and distribution, and understanding disturbance and recovery dynamics. We also highlight what is on the horizon for PAM, in terms of near‐future technological and methodological developments that have the potential to provide advances in coming years. Overall, we illustrate how ecologists can harness the power of PAM to address fundamental ecological questions in an era of ecology no longer characterised by data limitation. Read the free Plain Language Summary for this article on the Journal blog.

Species distribution models (SDMs) are a key tool for biogeography and climate change research, although current approaches have some significant drawbacks. The use of species occurrence constrains predictions of correlative models, while there is a general lack of eco-physiological data to develop mechanistic models. Passive acoustic monitoring is an emerging technique in ecology that may help to overcome these limitations. By remotely tracking animal behaviour across species geographical ranges, researchers can estimate the climatic breadth of species activity and provide a baseline for refined predictive models. However, such integrative approach still remains to be developed., Here, we propose the following: (a) a general and transferable method to build acoustic SDMs, a novel tool combining acoustic and biogeographical information, (b) a detailed comparison with standard correlative and mechanistic models, (c) a step-by-step guide to develop aSDMs and (d) a study case to assess their effectiveness and illustrate model outputs, using a year-round monitoring of calling behaviour of the Iberian tree frog at the thermal extremes of its distribution range. This method aims at forecasting changes in environmental suitability for acoustic communication, a key and climate-dependent behaviour for a wide variety of animal taxa., SDMs identified strong associations between calling behaviour and local environmental conditions and showed robust and consistent predictive perfor mance using two alternative models (regression and boundary). Furthermore, these models better captured climatic variation than correlative models as they use observations at higher temporal resolution. These results support aSDMs as efficient tools to model calling behaviour under future climate scenarios., The proposed approach offers a promising basis to explore the capacity of vocal species to deal with climate change, supported by an innovative integration of two disciplines: bioacoustics and biogeography. aSMDs are grounded on ecologically realistic conditions and provide spatially and temporally explicit predictions on calling behaviour, with direct implications in reproduction and survival. This enables to precisely forecast shifts in breeding phenology, geographic distribution or species persistence. Our study demonstrates how acoustic monitoring may represent an increasingly valuable tool for climate change., D.L. acknowledges a post-doctoral grant provided by the Comunidad de Madrid (2020-T1/AMB-20636, Atracción de Talento Investigador, Spain), and research projects funded by the European Commission (EAVESTROP–661408, Global Marie S. Curie fellowship, program H2020, EU) and the Ministerio de Ciencia, Innovación y Universidades (CGL2017-88764-R, MINECO/AEI/FEDER, Spain). S.V.-P. acknowledges a post-doctoral grant provided by the Comunidad de Madrid (2017-T2/AMB-6035).

Applications in bioacoustics and its sister discipline ecoacoustics have increased exponentially over the last decade. However, despite knowledge about aquatic bioacoustics dating back to the times of Aristotle and a vast amount of background literature to draw upon, freshwater applications of ecoacoustics have been lagging to date. In this special issue, we present nine studies that deal with underwater acoustics, plus three acoustic studies on water‐dependent birds and frogs. Topics include automatic detection of freshwater organisms by their calls, quantifying habitat change by analysing entire soundscapes, and detecting change in behaviour when organisms are exposed to noise. We identify six major challenges and review progress through this special issue. Challenges include characterisation of sounds, accessibility of archived sounds as well as improving automated analysis methods. Study design considerations include characterisation analysis challenges of spatial and temporal variation. The final key challenge is the so far largely understudied link between ecological condition and underwater sound. We hope that this special issue will raise awareness about underwater soundscapes as a survey tool. With a diverse array of field and analysis tools, this issue can act as a manual for future monitoring applications that will hopefully foster further advances in the field.

1. Passive acoustic monitoring is gaining momentum as a viable alternative method to surveying freshwater ecosystems. As part of an emerging field, the spatio‐temporal replication levels of these sampling methods need to be standardised. However, in shallow waters, acoustic spatio‐temporal patchiness remains virtually unexplored. 2. In this paper, we specifically investigate the spatial heterogeneity in underwater sounds observed within and between waterholes of an ephemeral river at different times of the day and how it could affect sampling in passive acoustic monitoring. 3. We recorded in the Einasleigh River, Queensland in August 2016, using a linear transect of hydrophones mounted on frames. We recorded four times a day: at dawn, midday, dusk, and midnight. To measure different temporal and spectral attributes of the recorded sound, we investigated the mean frequency spectrum and computed acoustic indices. 4. Both mean frequency spectrum and index analyses revealed that the site and diel activity patterns significantly influenced the sounds recorded, even for adjacent sites with similar characteristics along a single river. We found that most of the variation was due to temporal patterns, followed by between‐site differences, while within‐site differences had limited influence. 5. This study demonstrates high spatio‐temporal acoustic variability in freshwater environments, linked to different species or species groups. Decisions about sampling design are vital to obtain adequate representation. This study thus emphasises the need to tailor spatio‐temporal settings of a sampling design to the aim of the study, the species and the habitat.

Passive acoustic monitoring (PAM) is increasingly popular in ecological research and conservation programs, with high‐volume and long‐term data collection provided by automatized acoustic sensors offering unprecedented opportunities for faunal and ecosystem surveys. Practitioners and newcomers interested in PAM can easily find technical specifications for acoustic sensors and microphones, but guidelines on how to plan survey designs are largely scattered over the literature. Here, we (i) review spatial and temporal sampling designs used in passive acoustic monitoring, (ii) provide a synthesis of the crucial aspects of PAM survey design and (iii) propose a workflow to optimize recording autonomy and recording schedules. From 1992 to 2018, most of the 460 studies applying PAM in terrestrial environments have used a single recorder per site, covered broad spatial scales and rotated recorders between sites to optimize sampling effort. Continuous recording of specific diel periods was the main recording procedure used. When recording schedules were applied, a larger number of recordings per hour was generally associated with a smaller recording length. For PAM survey design, we proposed to (i) estimate memory/battery autonomy and associated costs, (ii) assess signal detectability to optimize recording schedules in order to recover maximum biological information and (iii) evaluate cost‐benefit scenarios between sampling effort and budget to address potential biases from a given PAM survey design. Establishing standards for PAM data collection will improve the quality of inferences over the broad scope of PAM research and promote essential standardization for cross‐scale research to understand long‐term biodiversity trends in a changing world.

Biodiversity in freshwater habitats is decreasing faster than in any other type of environment, mostly as a result of human activities. Monitoring these losses can help guide mitigation efforts. In most studies, sampling strategies predominantly rely on collecting animal and vegetal specimens. Although these techniques produce valuable data, they are invasive, time‐consuming and typically permit only limited spatial and temporal replication. There is need for the development of complementary methods. As observed in other ecosystems, freshwater environments host animals that emit sounds, either to communicate or as a by‐product of their activity. The main freshwater soniferous groups are amphibians, fish, and macroinvertebrates (mainly Coleoptera and Hemiptera, but also some Decapoda, Odonata, and Trichoptera). Biophysical processes such as flow or sediment transport also produce sounds, as well as human activities within aquatic ecosystems. Such animals and processes can be recorded, remotely and autonomously, and provide information on local diversity and ecosystem health. Passive acoustic monitoring (PAM) is an emerging method already deployed in terrestrial environments that uses sounds to survey environments. Key advantages of PAM are its non‐invasive nature, as well as its ability to record autonomously and over long timescales. All these research topics are the main aims of ecoacoustics, a new scientific discipline investigating the ecological role of sounds. In this paper, we review the sources of sounds present in freshwater environments. We then underline areas of research in which PAM may be helpful emphasising the role of PAM for the development of ecoacoustics. Finally, we present methods used to record and analyse sounds in those environments. Passive acoustics represents a potentially revolutionary development in freshwater ecology, enabling continuous monitoring of dynamic bio‐physical processes to inform conservation practitioners and managers.

In humans and some other mammals and birds, the development of communication systems requires social feedback. How do such systems evolve from ancestral states featuring innate developmental mechanisms? We report evidence of a novel form of social ontogeny in the communication system of Enchenopa treehoppers that suggests an answer to this question. These insects use plant-borne vibrational signals throughout their lives. Signal repertoires of nymphs and adults differed and showed sexually dimorphic ontogenetic trajectories; individual differences projected into some of the features of adult signals and mate preferences. Signals and mate preferences differed between adults reared in isolation and adults reared in groups, but even individuals reared in isolation developed species-typical signals. In this type of social ontogeny, peer inputs cause variation in signals and preferences. Thus, even innate communication systems can be socially malleable. This may set the stage for the evolution of obligate social feedbacks in communication: the starting point is already socially plastic and does not require learning to arise de novo.

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., New acoustic survey methods are becoming increasingly available to researchers, citizen scientists, and conservation practitioners. We propose a Pond Acoustic Sampling Scheme (PASS), to allow standardized individual audio samples to be collected rapidly from small waterbodies, alongside environmental and survey metadata. This will allow a wide range of participants, without complicated/expensive equipment, to contribute to collaborative data collection projects, and enable the development of the consistent datasets often missing from ecoacoustics research.

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 analyse 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 signalling experience and signalling practice during ontogeny on the development of adult mating preferences in Enchenopa females. Taking advantage of variation in the signal experience and signalling 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. This article is protected by copyright. All rights reserved.

Human 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. Publisher PDF

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.

Funding: J.G. was supported by a NERC GW4+ FRESH CDT PhD studentship (NE/R011524/1). C.D. was supported by a grant from the Ministerio de Economía, Industria y Competitividad (CGL2017-88764-R, MINECO/AEI/FEDER, Spain). Conventional methodologies used to estimate biodiversity in freshwater ecosystems can be nonselective and invasive, sometimes leading to capture and potential injury of vulnerable species. Therefore, interest in noninvasive surveying techniques is growing among freshwater ecologists. Passive acoustic monitor-ing, the noninvasive recording of environmental sounds, has been shown to effectively survey biota in terrestrial and marine ecosystems. However, knowl-edge of the sounds produced by freshwater species is relatively scarce. Further-more, little is known about the representation of different freshwater taxonomic groups and habitat types within the literature. Here we present results of a systematic review of research literature on freshwater bioacoustics and identify promising areas of future research. The review showed that fish are the focal taxonomic group in 44% of published studies and were studied pri-marily in laboratory aquaria and lotic habitats. By contrast, lentic habitats and other taxonomic groups have received relatively little research interest. It is par-ticularly striking that arthropods are only represented by 26% of studies, despite their significant contributions to freshwater soundscapes. This indicates a mis-match between the representation of taxonomic groups within the freshwater bioacoustic literature and their relative acoustic contribution to natural freshwater soundscapes. In addition, the review indicates an ongoing shift from behavioral studies, often with focus on a single taxonomic group, towards field-based studies using ecoacoustic approaches. On the basis of this review we suggest that future freshwater bioacoustics research should focus on passive acoustic monitoring and arthropod sound, which would likely yield novel insights into freshwater ecosystem function and condition. This article is categorized under: Water and Life > Nature of Freshwater Ecosystems Water and Life > Conservation, Management, and Awareness Water and Life > Methods. Publisher PDF

International audience; Acoustic population monitoring is a noninvasive method that can be deployed continuously over long periods of time and at large spatial scales. One of the newly discovered threats acting on biological diversity is anthropogenic noise. High levels of anthropogenic noise occur in aquatic environments, yet their effects on animals living in freshwater habitats have very rarely been investigated.Here, we used acoustic monitoring and automatic detection to assess the acoustic activity of a population of a soniferous freshwater insect.The sounds emitted by the corixid Micronecta scholtzi were recorded in a Mediterranean pond with an array of 12 hydrophones. An automatic analysis based on a measure of the amplitude found in the frequency band of M. scholtzi was developed to assess the level of acoustic activity. We used functional linear models, accounting for the periodicity of the calling behaviour, to estimate the possible effect of temperature, vegetation and a noise due to an immersed engine.The automatic analysis was validated as an efficient method to measure the acoustic activity. The monitoring revealed a clear 24‐hr pattern in the acoustic activity of M. scholtzi and three peaks of activity during the morning. Functional linear models revealed negative effects of both temperature and vegetation and showed that an engine noise, played back for 2 hr during the night, elicited an increase in the level of acoustic activity of the population. Moreover, a cross‐correlation procedure showed that noise delayed the acoustic activity of the population.Our results suggest that acoustic survey and automatic detection are efficient methods to monitor the acoustic activity of an insect population especially in response to an anthropogenic disturbance.

Funding: SL was supported by ARC DECRA DE130100565. ED was supported by a Griffith University IPRS scholarship. CD was supported by a ENS PhD grant. Ecoacoustic methods are increasingly used to monitor the state of populations and ecosystems. In freshwater environments, they present the clear advantages of being non-invasive, reducing bias, and providing continuous observations instead of only limited sampling snapshots in time. However, similar to standard bioassessment methods, temporal variation and choice of indicators can greatly influence ecoacoustic assessments, highlighting the importance of sampling and analysis design. In this study, we quantified diurnal variation in underwater sound and its effect on sampling regimes for two waterholes in the Einasleigh River, Northern Australia. Recording continuously for 6 days, and subsampling 5 s every 10 min, we found 22 distinct sounds that were emitted by fish, Hemiptera and Coleoptera as well as another 22 of abiotic or unknown origin. Through rarefaction analyses, we found that subsampling the data to 60% of the recorded sound events resulted in capture of most of the 44 identified sound types. Temporal heterogeneity—patchy sound events through time—needs to be considered when maximising detected sound events. Reducing the sampling interval from every 10 min to half-hourly or hourly had a much greater effect on capturing all sound types compared to the number of days recorded or the length of the recording. Overall, only 10–20% of the sound events need to be annotated for most sound types to be described; for example, restricting analysis of the days recorded to only three and the recording interval to 0.5–1 s. Acoustic indices were dominated by three main event types—a diurnally flowing creek, a nocturnal chorus of Hemiptera, as well as a dawn chorus of terapontid fishes. We conclude with two key messages: First, a select group of informative signals can be monitored using very simple methods—namely, converting an audio stream into indices using freely available software. Second, however, to detect less acoustically dominant sound events, manual annotation or single call processing will still be needed. While these findings are encouraging, similar analysis will need to be conducted within other freshwater ecosystems before general conclusions about optimal sampling regimes can be drawn. Postprint

Copyright by the Ecological Society of America Passive acoustic monitoring is gaining popularity in ecology as a practical and non-invasive approach to surveying ecosystems. This technique is increasingly being used to monitor terrestrial systems, particularly bird populations, given that it can help to track temporal dynamics of populations and ecosystem health without the need for expensive resampling. We suggest that underwater acoustic monitoring presents a viable, non-invasive, and largely unexplored approach to monitoring freshwater ecosystems, yielding information about three key ecological elements of aquatic environments – (1) fishes, (2) macroinvertebrates, and (3) physicochemical processes – as well as providing data on anthropogenic noise levels. We survey the literature on this approach, which is substantial but scattered across disciplines, and call for more cross-disciplinary work on recording and analysis techniques. We also discuss technical issues and knowledge gaps, including background noise, spatiotemporal variation, and the need for centralized reference collection repositories. These challenges need to be overcome before the full potential of passive acoustics in dynamic detection of biophysical processes can be realized and used to inform conservation practitioners and managers.

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.

A major challenge in water quality assessment is to identify suitable indicators to monitor and assess the effects of anthropogenic stressors on the ecological status of freshwater ecosystems. Passive acoustic monitoring is a novel approach that could potentially be used to detect invertebrate species and ecological processes such as dissolved oxygen dynamics in freshwater environments. The aim of the present study was to evaluate to what extent sounds can be used for water quality assessment. We performed a field study to relate acoustic indices to the intensity of several stressors, the invertebrate community composition and the dissolved oxygen dynamics in 20 temperate lowland streams and drainage ditches impacted to a varying degree by agricultural activities and discharges from waste water treatment plants. Our results showed that the recorded acoustic patterns were primarily associated with the fluctuation in dissolved oxygen saturation, while specific frequency bands could be related to the sound-producing invertebrate community. We observed that acoustic indices do not allow to detect the adverse effects of anthropogenic stressors on the invertebrate community composition, presumably due to the prevalence of Heteroptera which are relatively insensitive to stressors, but make a lot of sounds. A strong relation between acoustic indices and oxygen fluctuation indicate that passive acoustic monitoring may be used to estimate metabolism in water bodies. We suggest that the next step in freshwater ecoacoustics will be to precisely characterise each source of sound emitted during the processes of primary production, respiration and re-aeration, in order to distinguish these parameters. This may overcome some of the challenges encountered in the estimation of metabolism from diel dissolved oxygen curves.

International audience; Biodiversity in freshwater habitats is decreasing faster than in any other environment, mostly due to human activities. Monitoring these losses can help guide mitigation efforts. In most comparative or focal studies, sampling strategies predominantly rely on collecting animal and vegetal specimens. Although these techniques have produced valuable data, they are invasive, time-consuming, and typically have limited spatial and temporal replication. There is therefore a need for the development of complementary methods. As with other ecosystems and landscapes, freshwater environments host animals producing sounds, either to communicate or as a byproduct of their life activity. Animals and processes can be recorded, remotely, by unattended equipment and provide global information on local diversity and ecosystem health. We review practical examples of progress in experimentally addressing six main challenges that freshwater ecoacoustic monitoring faces: (1) associating each sound to its emitter, (2) estimating intra-specific sound variations, (3) evaluating diurnal variation, (4) modeling sound propagation, (5) deriving links between ecological condition and sounds, and (6) developing a repository for freshwater sounds. Passive acoustics represents a potentially revolutionary development in freshwater ecology, enabling dynamic monitoring of biophysical processes to inform conservation practitioners and managers.