The Role of Freshwater Bioacoustics In Ecological Research

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The Role of Freshwater Bioacoustics In Ecological Research

TAXONOMIC FOCUS OF FRESHWATER BIOACOUSTIC STUDIES

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 taxonomy 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. 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. 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.

The Padanian goby Padogobius martensii was the most studied fish species, appearing in three papers (Lugli, Yan, and Fine, 2003; Lugli, Pavan, & Torricelli, 1996; Lugli, Torricelli, et al., 1996; Torricelli et al., 1986). P. martensii sound production has been subject to extensive study in the laboratory (Lugli et al., 2003), often with a focus on courtship behavior (Lugli et al., 2003; Torricelli et al., 1986).

The round goby Neogobius melanostomus (Rollo, Andraso, Janssen, and Higgs, 2007; Rollo & Higgs, 2008), the croaking gourami Trichopsis vittata (Ladich, 2007; Ladich & Schleinzer, 2015), the burbot Lota lota (Cott et al., 2014; Grabowski et al., 2020), and the Arno goby Padogobius nigricans (Lugli, Pavan, & Torricelli, 1996; Lugli, Torricelli, et al., 1996; Malavasi et al., 2008) were represented by two studies. Rountree, Bolgan, et al. (2018) and Rountree, Juanes, et al. (2018) also report the most acoustically well-studied orders of temperate freshwater fish, with qualitatively similar results to those from this systematic review.

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 occupy 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).

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.

This research suggests that arthropods produce species-specific sounds that may be cataloged. Knowledge of these sounds could in the future be used with passive acoustic monitoring to identify macroinvertebrates in the natural environment and infer ecosystem conditions.

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. Rivers were the most studied natural habitat, being the research focus of 32 papers (24%).

The majority of research conducted in rivers focused on the topics of “Behaviour” (15 papers) or “Ecoacoustics” (10 papers), while the remaining studies focused on aspects of the physiology of sound production. Lake and pond habitat types, however, were only a research focus of 15 papers each. Notably, the soundscapes of temperate freshwater ponds were not investigated until when Desjonquères et al. (2015) used passive acoustic monitoring to record the soundscapes of three ponds in Chevreuse (France) for 1 min every 15 min over an 84-day period.

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 conducted 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 the 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. An increased flow rate was shown to produce higher sound pressure level values over most frequency bands. Such data offer a novel quantification of habitat

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: Jack A. Greenhalgh | Martin J. Genner | Gareth Jones | Camille Desjonquères

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