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'.

Human Auditory Ecology: Extending Hearing Research to the Perception of Natural Soundscapes by Humans in Rapidly Changing Environments.

Research in hearing sciences has provided extensive knowledge about how the human auditory system processes speech and assists communication. In contrast, little is known about how this system processes "natural soundscapes," that is the complex arrangements of biological and geophysical sounds shaped by sound propagation through non-anthropogenic habitats [Grinfeder et al. (2022). Frontiers in Ecology and Evolution. 10: 894232]. This is surprising given that, for many species, the capacity to process natural soundscapes determines survival and reproduction through the ability to represent and monitor the immediate environment. Here we propose a framework to encourage research programmes in the field of "human auditory ecology," focusing on the study of human auditory perception of ecological processes at work in natural habitats. Based on large acoustic databases with high ecological validity, these programmes should investigate the extent to which this presumably ancestral monitoring function of the human auditory system is adapted to specific information conveyed by natural soundscapes, whether it operate throughout the life span or whether it emerges through individual learning or cultural transmission. Beyond fundamental knowledge of human hearing, these programmes should yield a better understanding of how normal-hearing and hearing-impaired listeners monitor rural and city green and blue spaces and benefit from them, and whether rehabilitation devices (hearing aids and cochlear implants) restore natural soundscape perception and emotional responses back to normal. Importantly, they should also reveal whether and how humans hear the rapid changes in the environment brought about by human activity.

Auditory discrimination of natural soundscapes.

A previous modelling study reported that spectro-temporal cues perceptually relevant to humans provide enough information to accurately classify "natural soundscapes" recorded in four distinct temperate habitats of a biosphere reserve [Thoret, Varnet, Boubenec, Ferriere, Le Tourneau, Krause, and Lorenzi (2020). J. Acoust. Soc. Am. 147, 3260]. The goal of the present study was to assess this prediction for humans using 2 s samples taken from the same soundscape recordings. Thirty-one listeners were asked to discriminate these recordings based on differences in habitat, season, or period of the day using an oddity task. Listeners' performance was well above chance, demonstrating effective processing of these differences and suggesting a general high sensitivity for natural soundscape discrimination. This performance did not improve with training up to 10 h. Additional results obtained for habitat discrimination indicate that temporal cues play only a minor role; instead, listeners appear to base their decisions primarily on gross spectral cues related to biological sound sources and habitat acoustics. Convolutional neural networks were trained to perform a similar task using spectro-temporal cues extracted by an auditory model as input. The results are consistent with the idea that humans exclude the available temporal information when discriminating short samples of habitats, implying a form of a sub-optimality.

Using acoustics and artificial intelligence to monitor pollination by insects and tree use by woodpeckers.

The collection and interpretation of field data is a prerequisite for informed conservation in protected environments. Although several techniques, including camera trapping and passive acoustic monitoring, have been developed to estimate the presence of animal species, very few attempts have been made to monitor ecological functions. Pollination by insects and wood use, including tree related foraging and intraspecific communication, by woodpeckers are key functions that need to be assessed in order to better understand and preserve forest ecosystems within the context of climate change. Here, we developed and applied for the first time an acoustic survey to monitor pollination by insects and wood use by woodpeckers in a protected Alpine forest in France. We deployed four autonomous recorders over a year, resulting in 2285 h of recordings. We trained a convolutional neural network (CNN) on spectrographic images to automatically detect the sounds of flying insects' buzzing and woodpeckers' drumming as they forage and call. We used the output of the CNN to estimate the seasonality, diel pattern, climatic breadth and distribution of both functions and their relationships with weather parameters. Our method showed that insects were flying (therefore potentially pollinating flowers) in bright, warm and dry conditions, after dawn and before dusk during spring and summer. Woodpeckers were mainly drumming around March at the time of pair formation in cool and wet conditions. Having considered the role of weather parameters, climate change might have contrasting effects on insect buzzing and woodpecker drumming, with an increase in temperature being favorable to pollination by insects but not to wood use by woodpeckers, and a concomitant increase in relative humidity being favorable to wood use but not to pollination. This study reveals that a systemic facet of biodiversity can be tracked using sound, and that acoustics provide valuable information for the environment description.

Soundscape dynamics of a cold protected forest: dominance of aircraft noise.

CONTEXT: One mainstay of soundscape ecology is to understand acoustic pattern changes, in particular the relative balance between biophony (biotic sounds), geophony (abiotic sounds), and anthropophony (human-related sounds). However, little research has been pursued to automatically track these three components. OBJECTIVES: Here, we introduce a 15-year program that aims at estimating soundscape dynamics in relation to possible land use and climate change. We address the relative prevalence patterns of these components during the first year of recording. METHODS: Using four recorders, we monitored the soundscape of a large coniferous Alpine forest at the France-Switzerland border. We trained an artificial neural network (ANN) with mel frequency cepstral coefficients to systematically detect the occurrence of silence and sounds coming from birds, mammals, insects (biophony), rain (geophony), wind (geophony), and aircraft (anthropophony). RESULTS: The ANN satisfyingly classified each sound type. The soundscape was dominated by anthropophony (75% of all files), followed by geophony (57%), biophony (43%), and silence (14%). The classification revealed expected phenologies for biophony and geophony and a co-occurrence of biophony and anthropophony. Silence was rare and mostly limited to night time. CONCLUSIONS: It was possible to track the main soundscape components in order to empirically estimate their relative prevalence across seasons. This analysis reveals that anthropogenic noise is a major component of the soundscape of protected habitats, which can dramatically impact local animal behavior and ecology. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10980-021-01360-1.

Acoustic biodiversity.

Jérôme Sueur and colleagues introduce the acoustic components of biodiversity.

Hay meadow vibroscape and interactions within insect vibrational community.

Our experiences shape our knowledge and understanding of the world around us. The natural vibrational environment (vibroscape) is hidden to human senses but is nevertheless perceived and exploited by the majority of animals. Here, we show that the vibroscape recorded on plants in a temperate hay meadow is a dynamic low-frequency world, rich in species-specific vibrational signals. The overall vibroscape composition changed throughout the season and also depended on the plant species, as well as on the spatial position of individual plants within the meadow. Within the studied community, vibrationally signaling species sharing this communication channel avoided interference primarily by partitioning vibrational space on a fine temporal scale. The vibroscape is a reliable source of information in the environment and expands our understanding of ecological and evolutionary processes.

Climatic breadth of calling behaviour in two widespread Neotropical frogs: Insights from humidity extremes.

Climate change is severely altering precipitation regimes at local and global scales, yet the capacity of species to cope with these changes has been insufficiently examined. Amphibians are globally endangered and particularly sensitive to moisture conditions. For mating, most amphibian species rely on calling behaviour, which is a key weather-dependent trait. Using passive acoustics, we monitored the calling behaviour of two widespread Neotropical frogs in 12 populations located at the humidity extremes but thermal mean of the species distribution. Based on 2,554 hr of recordings over a breeding season, we found that both the aquatic species Pseudis paradoxa and the arboreal species Boana raniceps exhibited calling behaviour at a wide range of relative humidity. Calling humidity was significantly lower in conspecific populations subjected to drier conditions, while calling temperature did not differ between populations or species. Overall, no variation in climatic breadth was observed between large and small choruses, and calling behaviour was scarcely detected during the driest, hottest and coldest potential periods of breeding. Our results showed that calling humidity of the studied species varies according to the precipitation regime, suggesting that widespread Neotropical anurans may have the capacity to exhibit sexual displays in different climatic environments. Regardless of the underlying mechanism (plasticity or local adaptation), which should be determined by common garden experiments, a wide and population-specific climatic breadth of calling behaviour may assist species to deal with changing humidity conditions. To our knowledge, this is the first study to explore the response capacity of anurans to perform calling behaviour under contrasting precipitation regimes.

Climate Change Is Breaking Earth's Beat.

Forests, deserts, rivers, and oceans are filled with animal vocalizations and geological sounds. We postulate that climate change is changing the Earth's natural acoustic fabric. In particular, we identify shifts in acoustic structure that all sound-sensitive organisms, marine and terrestrial, may experience. Only upstream solutions might mitigate these acoustic changes.

Explosive breeding in tropical anurans: environmental triggers, community composition and acoustic structure.

BACKGROUND: Anurans largely rely on acoustic communication for sexual selection and reproduction. While multiple studies have focused on the calling activity patterns of prolonged breeding assemblages, species that concentrate their reproduction in short-time windows, explosive breeders, are still largely unknown, probably because of their ephemeral nature. In tropical regions, multiple species of explosive breeders may simultaneously aggregate leading to massive, mixed and dynamic choruses. To understand the environmental triggers, the phenology and composition of these choruses, we collected acoustic and environmental data at five ponds in French Guiana during a rainy season, assessing acoustic communities before and during explosive breeding events. RESULTS: We detected in each pond two explosive breeding events, lasting between 24 and 70 h. The rainfall during the previous 48 h was the most important factor predicting the emergence of these events. During explosive breeding events, we identified a temporal factor that clearly distinguished pre- and mid-explosive communities. A common pool of explosive breeders co-occurred in most of the events, namely Chiasmocleis shudikarensis, Trachycephalus coriaceus and Ceratophrys cornuta. Nevertheless, the species composition was remarkably variable between ponds and for each pond between the first and the second events. The acoustic structure of explosive breeding communities had outlying levels of amplitude and unexpected low acoustic diversity, significantly lower than the communities preceding explosive breeding events. CONCLUSIONS: Explosive breeding communities were tightly linked with specific rainfall patterns. With climate change increasing rainfall variability in tropical regions, such communities may experience significant shifts in their timing, distribution and composition. In structurally similar habitats, located in the same region without obvious barriers, our results highlight the variation in composition across explosive breeding events. The characteristic acoustic structure of explosive breeding events stands out from the circadian acoustic environment being easily detected at long distance, probably reflecting behavioural singularities and conveying heterospecific information announcing the availability of short-lived breeding sites. Our data provides a baseline against which future changes, possibly linked to climate change, can be measured, contributing to a better understanding on the causes, patterns and consequences of these unique assemblages.

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.

Biodiversity sampling using a global acoustic approach: contrasting sites with microendemics in New Caledonia.

New Caledonia is a Pacific island with a unique biodiversity showing an extreme microendemism. Many species distributions observed on this island are extremely restricted, localized to mountains or rivers making biodiversity evaluation and conservation a difficult task. A rapid biodiversity assessment method based on acoustics was recently proposed. This method could help to document the unique spatial structure observed in New Caledonia. Here, this method was applied in an attempt to reveal differences among three mountain sites (Mandjélia, Koghis and Aoupinié) with similar ecological features and species richness level, but with high beta diversity according to different microendemic assemblages. In each site, several local acoustic communities were sampled with audio recorders. An automatic acoustic sampling was run on these three sites for a period of 82 successive days. Acoustic properties of animal communities were analysed without any species identification. A frequency spectral complexity index (NP) was used as an estimate of the level of acoustic activity and a frequency spectral dissimilarity index (Df ) assessed acoustic differences between pairs of recordings. As expected, the index NP did not reveal significant differences in the acoustic activity level between the three sites. However, the acoustic variability estimated by the index Df , could first be explained by changes in the acoustic communities along the 24-hour cycle and second by acoustic dissimilarities between the three sites. The results support the hypothesis that global acoustic analyses can detect acoustic differences between sites with similar species richness and similar ecological context, but with different species assemblages. This study also demonstrates that global acoustic methods applied at broad spatial and temporal scales could help to assess local biodiversity in the challenging context of microendemism. The method could be deployed over large areas, and could help to compare different sites and determine conservation priorities.

So small, so loud: extremely high sound pressure level from a pygmy aquatic insect (Corixidae, Micronectinae).

To communicate at long range, animals have to produce intense but intelligible signals. This task might be difficult to achieve due to mechanical constraints, in particular relating to body size. Whilst the acoustic behaviour of large marine and terrestrial animals has been thoroughly studied, very little is known about the sound produced by small arthropods living in freshwater habitats. Here we analyse for the first time the calling song produced by the male of a small insect, the water boatman Micronecta scholtzi. The song is made of three distinct parts differing in their temporal and amplitude parameters, but not in their frequency content. Sound is produced at 78.9 (63.6-82.2) SPL rms re 2.10(-5) Pa with a peak at 99.2 (85.7-104.6) SPL re 2.10(-5) Pa estimated at a distance of one metre. This energy output is significant considering the small size of the insect. When scaled to body length and compared to 227 other acoustic species, the acoustic energy produced by M. scholtzi appears as an extreme value, outperforming marine and terrestrial mammal vocalisations. Such an extreme display may be interpreted as an exaggerated secondary sexual trait resulting from a runaway sexual selection without predation pressure.

Attack or retreat: contrasted defensive tactics used by Cyprian honeybee colonies under attack from hornets.

This study describes the tactics used by Cyprian honeybees (Apis mellifera cypria) to defend their colonies against hornet (Vespa orientalis orientalis) attacks. We use simulated hornet attacks and a combination of video recordings and image analysis to reveal, for the first time, contrasted intra-subspecies defensive tactics that operate at the colony level during predation. In some colonies, when attacked, the numbers of guards at the hive entrance increases rapidly to attack, engulf, and kill invading hornets. In other colonies, guards avoid conflicts with hornets by retreating gradually and by forming a defensive line of honeybees at the hive entrance. Retreater colonies have propolis walls at the hive entrances with small apertures that are too narrow to allow the hornet to access the hive and that therefore reinforces entrance protection. On the contrary, attacker colonies have propolis walls with large openings through which the hornet can pass; these bees block the hornet's access by intensively guarding the hive entrance. We experimentally destroy propolis walls to test whether colonies consistently rebuild walls with the same intrinsic characteristics and we also monitor the survival rate of each anti-predator tactic after massive natural predation by hornets.

Rapid acoustic survey for biodiversity appraisal.

Biodiversity assessment remains one of the most difficult challenges encountered by ecologists and conservation biologists. This task is becoming even more urgent with the current increase of habitat loss. Many methods-from rapid biodiversity assessments (RBA) to all-taxa biodiversity inventories (ATBI)-have been developed for decades to estimate local species richness. However, these methods are costly and invasive. Several animals-birds, mammals, amphibians, fishes and arthropods-produce sounds when moving, communicating or sensing their environment. Here we propose a new concept and method to describe biodiversity. We suggest to forego species or morphospecies identification used by ATBI and RBA respectively but rather to tackle the problem at another evolutionary unit, the community level. We also propose that a part of diversity can be estimated and compared through a rapid acoustic analysis of the sound produced by animal communities. We produced alpha and beta diversity indexes that we first tested with 540 simulated acoustic communities. The alpha index, which measures acoustic entropy, shows a logarithmic correlation with the number of species within the acoustic community. The beta index, which estimates both temporal and spectral dissimilarities, is linearly linked to the number of unshared species between acoustic communities. We then applied both indexes to two closely spaced Tanzanian dry lowland coastal forests. Indexes reveal for this small sample a lower acoustic diversity for the most disturbed forest and acoustic dissimilarities between the two forests suggest that degradation could have significantly decreased and modified community composition. Our results demonstrate for the first time that an indicator of biological diversity can be reliably obtained in a non-invasive way and with a limited sampling effort. This new approach may facilitate the appraisal of animal diversity at large spatial and temporal scales.

Sexual dimorphism in auditory mechanics: tympanal vibrations of Cicada orni.

In cicadas, the tympanum is anatomically intricate and employs complex vibrations as a mechanism for auditory frequency analysis. Using microscanning laser Doppler vibrometry, the tympanal mechanics of Cicada orni can be characterized in controlled acoustical conditions. The tympanum of C. orni moves following a simple drum-like motion, rather than the travelling wave found in a previous study of Cicadatra atra. There is a clear sexual dimorphism in the tympanal mechanics. The large male tympanum is unexpectedly insensitive to the dominant frequency of its own calling song, possibly a reflection of its dual purpose as a sound emitter and receiver. The small female tympanum appears to be mechanically sensitive to the dominant frequency of the male calling song and to high-frequency sound, a capacity never suspected before in these insects. This sexual dimorphism probably results from a set of selective pressures acting in divergent directions, which are linked to the different role of the sexes in sound reception and production. These discoveries serve to indicate that there is far more to be learnt about the development of the cicada ear, its biomechanics and evolution, and the cicada's acoustic behaviour.

Dispersive and non-dispersive waves through plants: implications for arthropod vibratory communication.

Vibratory communication in arthropods is a widespread phenomenon. Arthropods living on plants have been reported to use only dispersive bending waves in the context of prey-predator, competition, social and sexual interactions. Differences in signal structure have also been postulated to work as species recognition mechanisms and speciation agents. Using two identical laser Doppler vibrometers and a wavelet analysis, we quantified the wave propagation modes in rush stems (Juncus effusus) over the whole range of frequencies used by arthropods. A non-dimensionalized analysis shows that mechanical waves propagate not only as dispersive bending waves, but also as non-dispersive waves. Our analysis implies that an arthropod can communicate through non-dispersive bending waves by either producing signals of high frequencies or by choosing large stems, two widely different options tapping into the physiological and the behavioural repertoires, respectively. Non-dispersive waves, unreported so far in insect vibratory communication in plants, present serious advantages over dispersive bending waves in terms of signal integrity and may well be much more widely used than anticipated, in particular for species recognition.

Tuning the drum: the mechanical basis for frequency discrimination in a Mediterranean cicada.

Cicadas are known to use sound to find a mate. While the mechanism employed by male cicadas to generate loud calling songs has been described in detail, little information exists to explain how their ears work. Using microscanning laser Doppler vibrometry, the tympanal vibrations in the cicada Cicadatra atra are measured in response to acoustic playbacks. The topographically accurate optical measurements reveal the vibrational behaviour of the anatomically complex tympanal membrane. Notably, the tympanal ridge, a distinct structural element of the tympanum that is a link to the receptor cells, undergoes mechanical vibrations reminiscent of a travelling wave. In effect, the frequency for which the maximum deflection amplitude is observed regularly decreases from the apex to the base of the ridge. It is also shown that whilst female ears are mechanically tuned to the male's song, the male's tympanum is only partially tuned to its own song. This study establishes the presence of a peripheral auditory mechanism that can potentially process auditory frequency analysis. In view of the importance of acoustic signalling in cicadas, this unconventional tympanal mechanism may be employed in the context of species recognition and sexual selection.