The importance of context in the acoustic behaviors of marine, subtropical fish species^a)

Signaling through the production of active (i.e., intentional) sounds is widely used by fishes (Kasumyan, 2009; Looby , 2022a). Over 1000 fish species are known to produce active sounds, and thousands more are suspected to be actively soniferous (Looby , 2022a; Looby , 2022b; Looby , 2023b; Rice , 2022). Underwater acoustic cues have several advantages over other forms of cues, including high-speed information transfer, large area of spread, and locational source detection (Kasumyan, 2009). Sounds may convey valuable details about the individual producing them, such as sex, size, age, and activity (e.g., Pereira , 2020). Fish sounds may also vary spatially, temporally, or with other environmental variables that could provide ecologically relevant information (e.g., Fine and Thorson, 2008). Such acoustic signaling may be beneficial to the fishes themselves, to other organisms, and for passive acoustic monitoring applications (e.g., Gannon , 2005; Rountree , 2006; Bertucci , 2015).

Fishes produce active sounds in numerous behavioral contexts (i.e., situational purposes for which intentional sound production occurs) that can broadly be grouped by disturbance, aggression, reproduction, and other behavioral contexts (Kasumyan, 2009). For instance, some fish species may produce sounds when handled (i.e., disturbed) or during competitive feeding with conspecifics (i.e., aggression; Fish and Mowbray, 1970; Colson , 1998). Fish species may further make similar or different sounds in multiple behavioral contexts. For example, Gulf toadfish (Opsanus beta) males and females produce grunts agonistically, and males additionally have an advertisement call to attract females to their nests (Fine and Thorson, 2008). Similarly, red hind (Epinephelus guttatus) males in spawning aggregations produce low-frequency sounds during both territorial patrols and in interactions with females (Mann , 2010). Sound production may be integral to a particular behavior, such as competitive or reproductive sounds that drive responses from other conspecifics (Petersen , 2013; Forlano and Sisneros, 2016), or may be ancillary when acoustic cues are combined with other signaling modalities (Moller, 2002; Frommen, 2020). Acoustic signaling behaviors may also vary depending on the environment, such as in the wild versus in captivity, complicating their documentation and study (Bertucci , 2015; Looby , 2023a).

Despite the importance of acoustic communication in fishes, the relative occurrence of the different types of behavioral contexts associated with their sound production remains unclear. There have been several overviews of acoustic signaling behaviors in fishes (e.g., Kasumyan, 2009; Ladich , 2017) and many other reviews related to specific taxa, regions, or types of sound production behaviors (e.g., Fish and Mowbray, 1970; Ramcharitar , 2006; Colleye and Parmentier, 2012; Ladich, 2022), but these have generally been limited in scope or quantitative synthesis. Although recently there have been several efforts to coalesce fish sound production information on a global scale (e.g., Looby , 2022a; Rice , 2022), these efforts have largely focused on identifying actively soniferous fishes without data on the contexts surrounding their active sound production. This lack has led to indefinite and generalizing statements about sound production behaviors in fishes, such as that fishes mainly produce sounds in reproductive contexts (e.g., Kasumyan, 2009; Butler and Maruska, 2020; University of Rhode Island and Inner Space Center, 2021). Quantifying the variety and pervasiveness of the different circumstances in which fish species produce sound is necessary to understanding the evolutionary and ecological reasons for fishes' use of sound production in communication (Looby , 2022a; Rice , 2022) as well as potential human impacts on them (e.g., Butler and Maruska, 2020).

A systematized review was conducted on actively soniferous marine, subtropical fishes to (1) quantify the prevalence of the different behavioral contexts that may be associated with sound production among species and (2) explore how these behavioral contexts differed from research effort (i.e., the number of investigations) and among study environments and fish families. This review serves as a follow-up study to the recently published quantitative inventory of global soniferous fish diversity (Looby , 2022a) by providing data and discussion on the behavioral contexts surrounding active sound production, which were absent from the initial review. This review also centers on marine, subtropical fish species as they are among the most highly studied groups of fishes for sound production (Looby , 2022a), due to several extensive surveys (e.g., Fish and Mowbray, 1970) as well as numerous studies focused on individual species in the region (e.g., Bertucci , 2015).

The known acoustic behavioral contexts and sound production study environments of marine, subtropical fish species were surveyed with a systematized review (Fig. 1; Grant and Booth, 2009), following methods similar to those in Looby (2023a). Existing datasets were used to determine which publications were relevant to the review objectives and, therefore, necessitated data collection for the purposes of this review. Looby (2022a) conducted a systematized review to compile an inventory of documented sound production examinations of fish species globally that was later published online as FishSounds at FishSounds.net (Looby , 2021, 2022b; Looby , 2023b). The review considered whether and in which references species were found to make active sounds (i.e., sounds deemed by the authors of the publication to have been produced deliberately in association with a particular behavior or situation, frequently with specialized sonic organs or structures, and generally used for communication; Looby , 2022a). As the data collection for this review of behavioral contexts and study environments occurred prior to the completion of FishSounds version 1.0 (which included references published up until the year 2020; Looby , 2023b), this review instead relied on the 2018 version of the FishSounds dataset that was compiled using the same methods as Looby (2022a) but only included references published up until the year 2018 (Looby , 2021). For the purposes of this data collection, the FishSounds dataset was also restricted to only include English, peer-reviewed journal articles, with the addition of Fish and Mowbray (1970)—a book describing sound production testing for over 200 fish species (Rountree , 2002). The publications were further limited to only those that included species found to make active sounds auditorily (i.e., documenting the presence of audible active sounds through listening live or on a recording; Looby , 2022a).

Another existing database, FishBase, was used to determine which publications included marine, subtropical species (Froese and Pauly, 2023). FishBase is a global biodiversity information system encompassing about 35 000 fish species with data compiled from almost 60 000 references (Froese and Pauly, 2023). Much of the data provided on FishBase is accessible through its associated R package, rfishbase (Boettiger , 2012). For this review, taxonomic and water body information was taken from the R package rfishbase version 4.0.0 with the FishBase version set to 22.02 (Boettiger , 2012), while the species' primary climate zone was taken from the FishBase website (Froese and Pauly, 2019). Data were only collected on extant, marine, subtropical fish species as determined by these sources (Boettiger , 2012; Froese and Pauly, 2019).

The review data consisted of 450 investigations (i.e., auditory documentations of active sound production by a species in a publication)—encompassing 186 fish species studied in 194 publications. To maintain consistency and mitigate bias, the data collection was primarily conducted by a single reviewer. A second reviewer validated the data collected for over 100 of the investigations reviewed, including any that were ambiguous.

Data were collected on study environments in which the species were found to produce active sounds. Study environments were divided into four broad categories: captivity (i.e., completely artificial, human, or captive environments), semi-wild (i.e., relatively large artificial environments or natural environments with some artificial enclosures, such as human-made ponds or outdoor pens), wild (i.e., natural environments without any type of artificial enclosures), and unclear (i.e., could not be readily categorized with the information available). Species may have been found to produce active sounds in multiple study environments, either within an individual publication (e.g., a species was reported to produce active sounds in both the wild and captivity in the same study) or across multiple publications (e.g., a species was reported to produce active sounds in the wild in one study and in captivity in another study).

Data were also collected on which behavioral contexts were associated with the active sound production of marine, subtropical species. Because numerous synonyms could be used to describe similar activities, behavioral contexts were first determined based on the terms authors used to describe them. Then similar terms were combined into five broad categories: disturbance (e.g., defense, distress, escape); aggression (e.g., offense, chase, fighting); reproduction (e.g., advertisement, courtship, mating); other (e.g., coughing, yawning, choking); and unclear (i.e., could not be readily categorized with the information available). While there are existing debates over the use of some of these terms to describe fish behaviors (e.g., Ladich, 2022), the category names chosen were based on those most common in the literature and that best encompassed the various activities being described while these discussions remain ongoing. The categories may have included behaviors that did not occur naturally, such as disturbance behaviors elicited with direct handling (e.g., Fish and Mowbray, 1970) or reproductive behaviors instigated by hormonal stimulation (e.g., Bolgan , 2020).

Behavioral context categories were determined for each species in a given publication for each study environment category. Species may have been assigned to multiple behavioral context categories in the same or multiple study environments or publications (e.g., there may have been a species that made disturbance and reproductive sounds in captivity in one publication and reproductive sounds in the wild in another publication, all of which would have been differentiated in the data collection). Any behavioral contexts reported by the authors of the publication that were only speculative (e.g., a sound was only possibly associated with reproduction) or cited (e.g., a sound was associated with reproduction in a separate publication) were excluded in the data synthesis.

Disturbance was the most common behavioral context associated with sound production in marine, subtropical fish species and across investigations (Fig. 2; supplemental Tables SI and SII¹). When documentations were combined by species irrespective of study environment, disturbance was the most common behavioral context associated with active sound production (n = 140 species), followed by aggression (n = 46 species), reproduction (n = 34 species), and then other [n = 8 species; Fig. 2(a)]. Disturbance was also the most common behavioral context reported among investigations as associated with active sound production (n = 219 investigations). Reproduction was the next most common (n = 116 investigations), followed by aggression (n = 67 investigations) and then other [n = 9 investigations; Fig. 2(b)].

Species frequently were found to produce active sounds in multiple identifiable (i.e., not unclear) behavioral contexts. Specifically, 39 species produced active sounds in two behavioral contexts, 11 species in three behavioral contexts, and two species in all four behavioral contexts. Of the 140 species that produced sound during disturbance contexts, 48 also produced active sounds associated with at least one other behavioral context. Additionally, of the 46 species that produced sounds during aggression, 35 also produced sounds during disturbance, and of the 34 species that produced sounds during reproduction, 22 also produced sounds during disturbance. Eighty of the 450 investigations documented more than one behavioral context associated with active sound production as well.

Some of the prevalence in behavioral contexts among species and investigations varied by study environment (Fig. 3; supplemental Tables SI and SII¹). For example, among species tested in the wild, reproduction was more common (n = 23 species), followed by disturbance (n = 18 species) and then aggression [n = 12 species; Fig. 3(a)]. Also, many investigations did not clearly document behavioral contexts [n = 98 investigations; Fig. 2(b)] or the study environments in which active sound production was observed [n = 22 investigations; Fig. 3(b)].

The prevalence of behavioral contexts associated with sound production among species also varied somewhat by fish family (Fig. 4, supplemental Table SIII¹). The 186 marine, subtropical fish species included in the review belonged to 56 fish families. Among these families, 45 had at least one species documented to produce active sound associated with disturbance, 22 with aggression, 11 with reproduction, five with other, and 33 with unclear behavioral contexts. Twenty-four families had species documented to produce active sounds associated with more than one behavioral context. Disturbance was also the most common behavioral category among species within most families, especially when excluding unclear behaviors. Nonetheless, 13 families had a higher occurrence of aggression, reproduction, or other behaviors among species compared to disturbance.

Disturbance was the most common behavioral context associated with documented active sound production in marine, subtropical fish species. Active sound production associated with aggression was also very common, while less so with reproduction. This review's results contrast with some assumptions that fish sound production is more commonly associated with reproduction—in fact, less than a fifth of the marine, subtropical fish species from only about a fifth of the fish families included in the review have been documented producing sounds associated with reproduction. These findings are nonetheless supported by a separate although similar synthesis in the gray literature, which found more reports of fishes producing sounds associated with agonistic and disturbance contexts than with chorusing and reproduction (Ladich , 2017). This discrepancy in the assumed importance of reproduction may be related to its increased relative occurrence in investigations as a metric of research effort compared to species. Additional potential factors include study environment, fish family, or biases associated with the data assessed.

Most fish families had more species documented to produce active sound associated with disturbance than any other behavioral contexts. These include families, such as Carangidae, that contain species that make sounds during escape, when held on a hook, or during other mechanical stimulation (Fish and Mowbray, 1970). Only 11 of the 56 fish families included in the review had no species yet reported to make sounds associated with disturbance contexts, and those 11 families all had fewer than four species included in the review. Some families, however, did have as many or more species documented to produce active sound associated with aggression and reproduction. For example, some species in the Pomacentridae family make sounds aggressively during territorial defense (Colleye and Parmentier, 2012). Other families, such as Batrachoididae, are frequently studied for their advertisement calls and choruses (Edds-Walton , 2002; Fine and Thorson, 2008; Maruska and Mensinger, 2009; McIver , 2014).

There was some but not substantial overlap between behavioral contexts among species and investigations. Only 52 of the 186 species and 80 of the 450 investigations included in the review had active sound production associated with more than one identifiable behavioral context. The majority (92%) of species that produce active sounds in multiple behavioral contexts did so during disturbance in addition to at least one of the other categories. For example, the clownfish Amphiprion frenatus may produce either aggressive or disturbance sounds during agonistic interactions (Colleye and Parmentier, 2012). Additionally, both the lined seahorse (Hippocampus erectus) and the oyster toadfish (Opsanus tau) produced sounds in all the behavioral categories considered (Tower, 1908; Fish and Mowbray, 1970; Colson , 1998; Edds-Walton , 2002; Anderson, 2009; Maruska and Mensinger, 2009). Not all species that produce sounds during non-disturbance behaviors, however, were found to produce sounds during disturbance behaviors. There is, therefore, still limited evidence to indicate that fishes that make active sounds during certain behavioral contexts (e.g., disturbance) could always be expected to do so during other behavioral contexts (e.g., aggression).

The results of the review were likely influenced by the greater ease with which some behaviors and species can be studied in different environments (Looby , 2023a). Some fishes and behaviors may be much more easily studied in captivity, such as species that are small or easily acquired and disturbance behaviors that can be easily induced through artificial stimulation techniques (Fish and Mowbray, 1970). Other species' sound production behaviors may be more easily observed in the wild, such as toadfishes that loudly chorus to advertise for females (Tower, 1908; Fine and Thorson, 2008), or may only be observable in the wild, such as the growls cautiously attributed to the dusky grouper Epinephelus marginatus (Bertucci , 2015). In contrast, species such as the meagre (Argyrosomus regius) may produce similar sounds in both captivity and the wild (Pereira , 2020), and plainfin midshipman (Porichthys notatus) sounds are frequently studied in captivity, semi-wild, and wild environments (Brantley and Bass, 1994; Petersen , 2013; McIver , 2014; Brown , 2021; Woods , 2022). As certain behaviors may be more easily observed in one study environment over others, combinations of multiple environments and other variables may be required to comprehensively document the behavioral contexts in which any individual species produces sound (Bertucci , 2021; Looby , 2023a). Despite the value in varied testing methodologies, however, only about a quarter of the marine, subtropical species reviewed have documentations of active sound production in multiple study environments—an ongoing challenge in fish bioacoustics research (Looby , 2023a).

Because of potentially substantial biases introduced by the methods used to study fish sound production, the relative occurrence of these behaviors in natural contexts remains in question. For example, as disturbance sounds are so frequently induced through some form of manipulation by humans, the ability to relate these sounds to natural predation remains hindered (Ladich, 2022). Even in species that have been tested extensively for sound production, it can be difficult to confidently declare sound production absent from species or behaviors, as fish sound production can be specific to certain ages, seasons, situations, or other factors (Brantley , 1993; Lowerre-Barbieri , 2013; McIver , 2014; Morgan and Fine, 2020; Looby , 2022a). For example, although blue catfish (Ictalurus furcatus) produce stridulatory sounds when held by predators or humans, they were not found to use these sounds in conspecific competition or during spawning in the wild (Bosher , 2006; Ghahramani , 2014; Morgan, 2014; Morgan and Fine, 2020). The occurrence of these stridulatory sounds during agonistic or reproduction behaviors, nevertheless, still cannot be ruled out (Morgan and Fine, 2020). As such, the data presented in this review are meant to primarily highlight what has been found within scientific studies so far and may not be indicative of the full extent of naturally occurring sound production behavioral contexts.

This review and its results have some other limitations. Much remains unknown about active fish sound production, as only about 4% of extant fish species have been examined for sound production, and active sound production has evolved independently multiple times across fish taxa with potential for secondary loss (Looby , 2022a; Rice , 2022). The review only focused on marine, subtropical species that had been studied for sound production in the scientific literature. Thus, the review results may not be applicable to other regions or fishes that have not been examined for sound production. Additionally, many studies did not clearly identify behaviors or study environments, which may have impacted the numbers reported. To address these limitations, data collection on a wider variety of fish species and contexts, more complex meta-analyses, and surveys of fish species irrespective of suspected sound production would be beneficial in further understanding acoustic behaviors in fishes.

This review provides a quantitative synthesis of the behavioral contexts associated with known active sound production in marine, subtropical fishes. Disturbance was the most common behavioral context reported among species, followed by aggression, reproduction, and other behaviors. This trend was not entirely reflected in research effort, assessed by the number of investigations studying acoustic behaviors. Behavioral prevalence also varied within some study environments and fish families. These results demonstrate the need to consider potential biases when researching and generalizing about acoustic communication behaviors in fishes.

A Mitacs Globalink Research Internship funded undergraduate assistance, and the University of Florida School of Forest, Fisheries, and Geomatics Sciences funded graduate assistance in the project. We thank the University of Florida George A. Smathers Libraries, their interlibrary loan system, and the libraries' staff for their assistance.