The role of freshwater bioacoustics in ecological research

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TAXONOMIC FOCUS OF FRESHWATER BIOACOUSTIC STUDIES

Biodiversity and ecosystem functions are closely linked, and monitoring biological diversity and abundance is essential for developing an understanding of ecosystem condition and processes (McGrady-Steed, Harris, & Morin, 1997). Many methods used to estimate biodiversity such as quadrats (Stevens, Dise, Mountford, & Gowing, 2004) and camera traps (Silveira, Jacomo, & Diniz-Filho, 2003) can underestimate the diversity of fauna present in a habitat. In particular, the number of individuals sampled, and the number, size and distribution of sampling areas can have a strong influence on values of estimated biodiversity (Gotelli & Colwell, 2011). Furthermore, biodiversity estimates are often extrapolated over large temporal and spatial scales to compensate for the logistical difficulties associated with sampling large areas for long periods of time (Gasc, Pavoine, Lellouch, Grandcolas, & Sueur, 2015). In freshwater systems conventional methodologies used to estimate biodiversity, such as kick sampling, fyke netting and trapping, are nonselective and invasive, sometimes leading to the capture of vulnerable species.

Moreover, these methods can necessitate substantial manual labor as field sites must be visited frequently to deploy and check equipment, and there can be requirements for laboratory processing and species identification. In addition, if used in multiple waterways, traps and nets may present a biosecurity risk to other freshwater ecosystems by spreading disease or invasive species. Passive acoustic monitoring, the noninvasive recording of environmental sounds, has been shown to effectively survey biodiversity in terrestrial (Blumstein et al., 2011; Fristrup & Mennitt, 2012; Llusia, Márquez, & Bowker, 2011; Sugai, Silva, Ribeiro Jr, & Llusia, 2018) and marine (Croll et al., 2002; di Sciara & Gordon, 1997; Montgomery & Radford, 2017; Ramcharitar, Gannon, & Popper, 2006) ecosystems. Despite this, soundscapes (i.e., representations of all the acoustic signals in an environment; Table) of freshwater ecosystems remain largely unexplored (Linke et al., 2018). In a recent review, Linke et al. (2018) identified 2,740 freshwater bioacoustics articles by entering the search terms “freshwater + bioacoustics” into Google Scholar on the 28th of August 2017.

In total 124 papers met the selection criteria, 72 papers from the 2,756 papers initially listed from our search of the Web of Science database, and 52 papers from an additional survey of the reference literature and our own personal archives. Thirteen papers (11%) reported recordings of underwater soundscapes, and thus did not focus on any particular taxonomic group. Most studies identified by this review, however, reported descriptions of sounds produced by a single taxonomic group, of which “fish” was the most commonly represented (44% of papers; Figure). In total, 80 species of fish within 13 orders and 20 families were studied within these papers. Perciformes (perch-like fishes) have been the most well represented order, with 31 species from six families represented by 23 papers, 16 of which were Cichlidae (Table). Salmoniformes (salmonids; four species in one family), Cypriniformes (carps, minnows and loaches; eight species in two families) and Acipenseriformes (sturgeons and paddlefishes; four species in one family) were also well represented.

Specifically, Rountree, Bolgan, et al. (2018) and Rountree, Juanes, et al. (2018) reported that 68 species of fish in 12 orders have been studied, including 28 species of Cypriniformes in four families, 18 species of Perciformes in five families, 11 species of Salmoniformes in one family, and 11 species of Acipenseriformes in one family. The large number of studies orientated towards fish is perhaps in part due to the familiarity that researchers from different disciplines have with fish husbandry. Animal behavior and ecotoxicology laboratories possess the expertise and equipment required to keep fish in captivity (Lynn, Egar, Walker, Sperry, & Ramenofsky, 2007), which can easily be adapted for use in bioacoustics studies. Furthermore, both P. martensii and T. vittata are straightforward to obtain for research purposes as the former is a common species that occupies very shallow water (<0.5 m; Lugli et al., 2003) in southern Europe, and the latter is a popular aquarium fish frequently traded around the world (Courtenay & Stauffer, 1990).

Freshwater fish species can possess significant economic, ecological and cultural value (Linke et al., 2018). One such species, the Arctic charr Salvelinus alpinus, has recently become extinct in multiple locations in the UK and Ireland and could benefit from conservation interventions (Maitland, Winfield, McCarthy, & Igoe, 2007). The species was represented by two studies in this review (Bolgan, O’Brien, Rountree, and Gammell, 2016; Bolgan et al., 2018), with one study using passive acoustic monitoring to successfully identify spawning sounds produced by Arctic charr disturbing gravel in order to assess breeding behavior and aide conservation efforts (Bolgan et al., 2018). Passive acoustic monitoring was also used by Straight et al. (2014, 2015) on a larger scale to detect spawning behavior of the river redhorse Moxostoma carinatum and robust redhorse Moxostoma robustum. In total, several hundred spawning events were recorded in multiple rivers in north Georgia (United States).

The spawning events were identified by characterizing the unique pattern of dominant frequencies, amplitude variation and duration of the spawning event audio signal. These data were then integrated into an automated detection software, which was capable of identifying 80–82% of known spawning events (Straight et al., 2014). Research papers investigating 33 species of amphibian in nine families (two orders: Anura and Caudata) were identified by this review. Anura was the most represented order, within which Pipidae was the most represented family, with 20 species represented by five studies (Kwong-Brown et al., 2019; Ringeis, Krumscheid, Bishop, De Vries, & Elepfandt, 2017; Tobias, Corke, Korsh, Yin, & Kelley, 2010; Vignal & Kelley, 2007; Yager, 1992). Kwong-Brown et al. (2019) filmed the larynx of 18 Xenopus (Pipidae) frogs as they produced sound in order to identify the mechanisms behind sound production underwater. Xenopus are well known to researchers as model organisms in fields such as vertebrate embryology and genomics (Hellsten et al., 2010), which may explain their notable presence in the literature.

Five papers focused on freshwater mammal bioacoustics covering four species within four families, the most studied of which was the common hippopotamus Hippopotamus amphibius (Barklow, 1997, 2004; Maust-Mohl et al., 2018). Other species included the Amazon river dolphin Inia geoffrensis and the tucuxi Sotalia fluivatilis (Table). Four papers reported investigations of underwater reptile sounds, which focussed on three species, the Arrau turtle Podocnemis expansa (Ferrara et al., 2012, 2014), the American alligator Alligator mississippiensis (Reber et al., 2017) and the Northern snake-necked turtle Chelodina oblonga (Giles, Davis, McCauley, & Kuchling, 2009). Only four papers identified by the search terms of this review investigated freshwater arthropod sounds. Of these only two (Sueur et al., 2011; Wilson, Flinn, West, & Hereford, 2015) included underwater recordings of biological sound. However, an additional 30 papers were added from surveying the cited literature of reference reviews in the field of freshwater bioacoustics and our own personal literature archives.

FOCAL HABITATS OF FRESHWATER BIOACOUSTIC STUDIES

In total 71 papers (53%) identified by this review were conducted in a laboratory. Such studies benefit from the ability to reduce background noise and make detailed physiological observations while controlling environmental parameters that influence acoustic behavior, such as water temperature (Torricelli et al., 1990). However, interpretations of acoustic behavior from recordings conducted in a laboratory may be influenced by the unnatural absorption and scattering of soundwaves inside small aquaria (Akamatsu, Okumura, Novarini, & Yan, 2002), and the cut-off phenomenon (Urick, 1967), which can cause low frequencies to quickly decay and therefore be undetected by a hydrophone while higher resonant frequencies of the aquarium are amplified.

Each pond was shown to possess unique daily patterns of acoustic activity and composition, indicating that the ponds contained high levels of acoustic diversity. Furthermore, Bolgan et al. (2018) recorded the first underwater soundscape of Arctic charr spawning grounds in Lake Windermere (United Kingdom) using three passive acoustic monitoring stations. They identified three distinct sound groups: fish air passage sounds; macroinvertebrate sounds and gravel sounds (spawning activity). Passive acoustic monitoring studies are often only conduced in rivers and frequently overlook lentic habitats, which are often more species rich (Dehling, Hof, Brändle, & Brandl, 2010). Wysocki, Amoser, and Ladich (2007) demonstrated that environments with flowing water possess higher levels of background noise due to the movement of water and sediment, often present above 1 kHz which has the effect of masking sounds produced by most fish species. In lentic environments however, sounds produced by fish species are only partly masked.

In contrast to exclusively investigating sounds produced by animals, Tonolla, Lorang, Heutschi, Gotschalk, and Tockner (2011) investigated abiotic sounds in rivers. They suspended a hydrophone from an inflatable cataraft to investigate physical characteristics of underwater sound along stretches of five hydro-geomorphologically different river segments in Switzerland, Italy and the United States in order to characterize the spatial distributions of habitat types along ;a river segment. Each river segment was identifiable by the sound pressure level, sound variability and the spatial organization of the acoustic signal (31.5 Hz to 16 kHz). Abiotic sound sources, such as turbulence or streambed sediment transport along each river segment influenced spatial soundscape diversity.

A SHIFT TOWARDS ECOACOUSTICS

Most papers were focused on behavior (48%) while fewer studies addressed ecoacoustic (16%) or physiological (12%) research questions. Several papers focused on a combination of two main topics (behavior and physiology; behavior and ecoacoustics; ecoacoustics and physiology). Interestingly, more papers focused on a combination of behavior and physiology (16%) than on physiology only. Only three studies (Lara & Vasconcelos, 2018; Scholik & Yan, 2002a, 2002b) focused both on physiology and ecoacoustics (2%; Figure 3). Lara and Vasconcelos (2018) characterized the soundscapes of natural (river) and artificial (laboratory aquarium) zebrafish Danio rerio environments and found that the soundscapes of artificial environments possessed high noise levels, potentially causing auditory masking. Scholik and Yan (2002a, 2002b) studied the effect of anthropogenic sound (a small boat) on the hearing capabilities of zebrafish and fathead minnow Pimephales promelas in a laboratory.

Traditionally, bioacoustics studies have focussed on behavioral and physiological aspects of sound production (Yager, 1992) and have only recently sought to describe biological sound at a soundscape scale and address ecological research questions in the form of ecoacoustics using passive acoustic monitoring (Desjonquères et al., 2018). The results of this systematic review confirm this shift from behavioral studies, often with a focus on a single taxonomic group, towards an approach orientated towards ecoacoustics and conservation biology. Since 2000, the number of ecoacoustics articles has grown dramatically (2001–2005: 1 article, 2006–2010: 2, 2011–2015: 6 and 2016–2020: 16) while the number of behavioral studies remained stable with an average of 14 papers every five years.

Author: A. Greenhalgh , Martin J. Genner  , Gareth Jones , Camille Desjonquères