What’s all that racket! Soundscapes, phenology, and biodiversity in estuaries

(Troglodytes pacificus), and ruby-crowned kinglet (Regulus calendula) due to an earlier winter to spring transition at Glacier Bay National Park, Alaska, USA [8]. Studies have shown that common frogs (Rana temporaria) tend to breed earlier in warmer ponds, while 78 songbird species in North America shifted their spring arrival earlier from overwintering grounds due to rising spring temperatures [33, 34]. In marine ecosystems, passive acoustics offers an auton- omous, technology-based approach to track spawning behaviors and migratory arrivals of spe- cies that produce sounds, which is particularly useful in underwater habitats where visibility can be limited (e.g. estuaries) and access can be challenging (e.g. deep ocean). With the advent of newer, affordable recording systems and increased computational power, underwater sound data can be collected and visualized at short time intervals (e.g. continuously, 20 min, or 60 min) and over long-term scales (i.e. years and decades) providing excellent temporal cover- age to detect changes in phenology. Soundscape and biodiversity Many of the sound-producing fish species collected in haul seines were young-of-the-year, and the ability of this life stage to produce sound is questionable. In the May River estuary, adult male oyster toadfish, silver perch, spotted seatrout, and red drum are the major sound-produc- ing species that produce courtship calls and choruses associated with spawning [16, 17, 18, 28]. All of these fish to some degree contribute to sound pressure levels in the low frequency band-

width [28]. In the May River, oyster toadfish, black drum, silver perch, and spotted seatrout are residents in estuaries year-round, while adult red drum may move offshore in the colder winter months; none of these fish produces sound in the cold, winter months from November to February [18, 28]. Louder habitats may correlate with higher species richness and abundance [11, 12]. In the present study, we showed that higher species diversity and abundance occurred during sea- sonal periods (i.e. spring and summer) when biological sound levels in the low and high fre- quency bandwidths were the highest. Furthermore, biologically louder areas of the tidal river had higher diversity and abundance of invertebrates and fish. It is possible that the soundscape could provide organisms with information about habitat quality, resources, and potential predators [6]. It is also possible that the myriad of snapping shrimp and fish vocalizations guide organisms (e.g. larva, fish, and marine mammals) into and within the estuary. Recent laboratory and field playback experiments conducted in St. Johns, US Virgin Islands and Pam- lico Sound, North Carolina, USA have reported that larva utilize sound cues to find coral / oys- ter reefs based on the biogenic sound production of organisms occupying these habitats [35– 37]. The May River is a salt marsh estuary bordered by extensive patches of smooth cordgrass Spartina alterniflora and oyster reefs comprised of the eastern oyster Crassostrea virginica. Pas-

sive acoustic recorders were placed on the bottom, close to the sides of the estuary, where live and dead oyster patches were common. Habitat-specific sound characteristics may reflect an important selection cue in driving settlement and recruitment patterns in marine communi- ties, leading to higher biodiversity and potentially healthier habitats [36, 38]. While our study investigated temporal changes of the soundscape and diversity over a rela- tively short timeframe (~ six years), this approach provides a blueprint for implementation over longer time scales [3]. Listening to soundscapes has the potential to provide insight into the response and resiliency of individual species and their behaviors. Integrating long-term soundscape characterization into coastal marine observatory networks would be powerful because of its utility in providing acoustic behavior measurements at multiple levels of biologi- cal complexity (i.e. from snapping shrimp to fish to marine mammals) at time scales that range from minutes to years. This approach allows us to eavesdrop on key behaviors that can PLOS ONE Estuarine soundscapes and biodiversity PLOS ONE | https://doi.org/10.1371/journal.pone.0236874 September 3, 2020 8 / 18