Ashlee Lillis

Oyster Larvae Settle in Response to Habitat-Associated Underwater Sounds

Following a planktonic dispersal period of days to months, the larvae of benthic marine organisms must locate suitable seafloor habitat in which to settle and metamorphose. For animals that are sessile or sedentary as adults, settlement onto substrates that are adequate for survival and reproduction is particularly critical, yet represents a challenge since patchily distributed settlement sites may be difficult to find along a coast or within an estuary. Recent studies have demonstrated that the underwater soundscape, the distinct sounds that emanate from habitats and contain information about their biological and physical characteristics, may serve as broad-scale environmental cue for marine larvae to find satisfactory settlement sites. Here, we contrast the acoustic characteristics of oyster reef and off-reef soft bottoms, and investigate the effect of habitat-associated estuarine sound on the settlement patterns of an economically and ecologically important reef-building bivalve, the Eastern oyster (Crassostrea virginica). Subtidal oyster reefs in coastal North Carolina, USA show distinct acoustic signatures compared to adjacent off-reef soft bottom habitats, characterized by consistently higher levels of sound in the 1.5–20 kHz range. Manipulative laboratory playback experiments found increased settlement in larval oyster cultures exposed to oyster reef sound compared to unstructured soft bottom sound or no sound treatments. In field experiments, ambient reef sound produced higher levels of oyster settlement in larval cultures than did off-reef sound treatments. The results suggest that oyster larvae have the ability to respond to sounds indicative of optimal settlement sites, and this is the first evidence that habitat-related differences in estuarine sounds influence the settlement of a mollusk. Habitat-specific sound characteristics may represent an important settlement and habitat selection cue for estuarine invertebrates and could play a role in driving settlement and recruitment patterns in marine communities.

The Curious Acoustic Behavior of Estuarine Snapping Shrimp: Temporal Patterns of Snapping Shrimp Sound in Sub-Tidal Oyster Reef Habitat.

Ocean soundscapes convey important sensory information to marine life. Like many mid-to-low latitude coastal areas worldwide, the high-frequency (>1.5 kHz) soundscape of oyster reef habitat within the West Bay Marine Reserve (36°N, 76°W) is dominated by the impulsive, short-duration signals generated by snapping shrimp. Between June 2011 and July 2012, a single hydrophone deployed within West Bay was programmed to record 60 or 30 seconds of acoustic data every 15 or 30 minutes. Envelope correlation and amplitude information were then used to count shrimp snaps within these recordings. The observed snap rates vary from 1500–2000 snaps per minute during summer to <100 snaps per minute during winter. Sound pressure levels are positively correlated with snap rate (r = 0.71–0.92) and vary seasonally by ~15 decibels in the 1.5–20 kHz range. Snap rates are positively correlated with water temperatures (r = 0.81–0.93), as well as potentially influenced by climate-driven changes in water quality. Light availability modulates snap rate on diurnal time scales, with most days exhibiting a significant preference for either nighttime or daytime snapping, and many showing additional crepuscular increases. During mid-summer, the number of snaps occurring at night is 5–10% more than predicted by a random model; however, this pattern is reversed between August and April, with an excess of up to 25% more snaps recorded during the day in the mid-winter. Diurnal variability in sound pressure levels is largest in the mid-winter, when the overall rate of snapping is at its lowest, and the percentage difference between daytime and nighttime activity is at its highest. This work highlights our lack of knowledge regarding the ecology and acoustic behavior of one of the most dominant soniforous invertebrate species in coastal systems. It also underscores the necessity of long-duration, high-temporal-resolution sampling in efforts to understand the bioacoustics of animal behaviors and associated changes within the marine soundscape.

Soundscape manipulation enhances larval recruitment of a reef-building mollusk

Marine seafloor ecosystems, and efforts to restore them, depend critically on the influx and settlement of larvae following their pelagic dispersal period. Larval dispersal and settlement patterns are driven by a combination of physical oceanography and behavioral responses of larvae to a suite of sensory cues both in the water column and at settlement sites. There is growing evidence that the biological and physical sounds associated with adult habitats (i.e., the “soundscape”) influence larval settlement and habitat selection; however, the significance of acoustic cues is rarely tested. Here we show in a field experiment that the free-swimming larvae of an estuarine invertebrate, the eastern oyster, respond to the addition of replayed habitat-related sounds. Oyster larval recruitment was significantly higher on larval collectors exposed to oyster reef sounds compared to no-sound controls. These results provide the first field evidence that soundscape cues may attract the larval settlers of a reef-building estuarine invertebrate.

Soundscapes and Larval Settlement: Characterizing the Stimulus from a Larval Perspective.

There is growing evidence that underwater sounds serve as a cue for the larvae of marine organisms to locate suitable settlement habitats; however, the relevant spatiotemporal scales of variability in habitat-related sounds and how this variation scales with larval settlement processes remain largely uncharacterized, particularly in estuarine habitats. Here, we provide an overview of the approaches we have developed to characterize an estuarine soundscape as it relates to larval processes, and a conceptual framework is provided for how habitat-related sounds may influence larval settlement, using oyster reef soundscapes as an example.

Sound production patterns of big-clawed snapping shrimp (Alpheus spp.) are influenced by time-of-day and social context

Snapping shrimp are perhaps the most pervasive sources of biological sound in the ocean. The snapping sounds of cryptic shrimp colonies in shallow coastal habitats worldwide create a near-continuous crackling with high spatiotemporal variability, yet the underlying acoustic ecology is not well understood. This study investigated sound production rates and acoustic behavior of snapping shrimp species common in the Western Atlantic Ocean and Gulf of Mexico (Alpheus heterochaelis and Alpheus angulosus). Snap rates were measured in a controlled laboratory setting under natural light, temperature, and substrate conditions for shrimp held individually, in pairs, and in a ten-shrimp mesocosm, to test hypotheses that acoustic activity varies with time-of-day and social context. Spontaneous snapping was observed for 81 out of 84 solitary shrimp monitored. Time-of-day influenced snap output for individuals and same-sex pairs-higher rates occurred during dusk and night, compared to daylight hours, but this pattern was inconsistent for opposite-sex pairs and a mixed-sex group. These laboratory results provide insight into behavioral rhythms that may influence snapping patterns in natural populations, and underscore the limited understanding of a major sound source in marine environments.

Larval settlement in response to estuarine soundscapes

Ambient underwater sound has the potential to be an important orientation and settlement cue for marine invertebrate larvae, yet larval responses to relevant sound patterns are largely unknown. In estuaries of the Southeastern United States, oyster reefs are patchy productive habitats that harbor many soniferous fish and invertebrates, creating distinct sound characteristics. This habitat-related sound could provide a useful cue for the planktonic larvae of obligate reef dwellers and facilitate encounter with suitable settlement substrate. To investigate sound as a settlement cue in this system, larval settlement responses to oyster reef and soft-bottom sounds, as well as a no-sound control were tested for the Eastern oyster, Crassostrea virginica. Laboratory and field experiments suggest that sound has a significant effect on oyster settlement rates: higher numbers of larvae settled in the presence of oyster reef sounds than in soft-bottom sound or silent control treatments. Improved understanding of the...

Multiscale spatio-temporal patterns of boat noise on U.S. Virgin Island coral reefs

Sound-sensitive organisms are abundant on coral reefs. Accordingly, experiments suggest that boat noise could elicit adverse effects on coral reef organisms. Yet, there are few data quantifying boat noise prevalence on coral reefs. We use long-term passive acoustic recordings at nine coral reefs and one sandy comparison site in a marine protected area to quantify spatio-temporal variation in boat noise and its effect on the soundscape. Boat noise was most common at reefs with high coral cover and fish density, and temporal patterns reflected patterns of human activity. Boat noise significantly increased low-frequency sound levels at the monitored sites. With boat noise present, the peak frequencies of the natural soundscape shifted from higher frequencies to the lower frequencies frequently used in fish communication. Taken together, the spectral overlap between boat noise and fish communication and the elevated boat detections on reefs with biological densities raises concern for coral reef organisms.

Variability in coral reef soundscapes, spatiotemporal differences, biophysical and behavioral drivers, and associations with local biota

Coral reefs harbor some of the highest biodiversity on the planet. Their rich ecoacoustic soundscape may provide a way to track both animal activities and community level structure. To do so, it is critical to identify how reef soundscapes are influenced by biotic and abiotic parameters, and establish how soundscapes change over time and across habitats. Here we present results from 18 coral reefs in the U.S. Virgin Islands and Maui, Hawaii, with the overall goals to quantify soundscape variability across multiple spatial and temporal scales (days to years), test how soundscape parameters relate to local biological communities, and address how biophysical parameters (light, temperature, and rugosity) influence these eco-soundscapes. Acoustic measurements were made in-tandem with benthic and fish visual surveys. Analyses were carried out using high and low-frequency bands corresponding to the primary soniferous taxa on reefs, snapping shrimp and fish. Overall, these results indicate that certain acoustic metrics can be linked to visual survey results. Snapping shrimp exhibit complex spatiotemporal patterns, with strong diel rhythms shifting over time and varying substantially over short spatial scales. Furthermore, long-term recordings are necessary to provide a robust baseline measurement of acoustic variability and better quantify changes in coral reef ecosystems.Coral reefs harbor some of the highest biodiversity on the planet. Their rich ecoacoustic soundscape may provide a way to track both animal activities and community level structure. To do so, it is critical to identify how reef soundscapes are influenced by biotic and abiotic parameters, and establish how soundscapes change over time and across habitats. Here we present results from 18 coral reefs in the U.S. Virgin Islands and Maui, Hawaii, with the overall goals to quantify soundscape variability across multiple spatial and temporal scales (days to years), test how soundscape parameters relate to local biological communities, and address how biophysical parameters (light, temperature, and rugosity) influence these eco-soundscapes. Acoustic measurements were made in-tandem with benthic and fish visual surveys. Analyses were carried out using high and low-frequency bands corresponding to the primary soniferous taxa on reefs, snapping shrimp and fish. Overall, these results indicate that certain acoustic m...

The snapping shrimp conundrum: Spatial and temporal complexity of snapping sounds on coral reefs

Snapping shrimp are abundant crevice-dwelling crustaceans worldwide. The short-duration broadband “snap” generated by the collapse of a cavitation bubble upon the rapid closure of their specialized claw is among the loudest bioacoustic sound in the sea. Because these shrimp form large high density aggregations, their colonies create a pervasive crackling in many coastal environments, and variation in shrimp acoustic activity substantially alters ambient sound levels at a given location or time. Despite their fundamental contribution to the soundscape of coral reefs, and probable influence on sound-receptive organisms, relatively little is known about snapping shrimp sound production patterns, and the underlying behavioural ecology or environmental factors. Recent advances in recording capacity and efforts to sample habitat soundscapes at high spatiotemporal resolution have provided datasets that reveal complex dynamics in snapping shrimp sound production. Our analyses of soundscape data from coral reefs s...