Correction: Hurricane impacts on a coral reef soundscape.

[This corrects the article DOI: 10.1371/journal.pone.0244599.].

Hurricane impacts on a coral reef soundscape.

Soundscape ecology is an emerging field in both terrestrial and aquatic ecosystems, and provides a powerful approach for assessing habitat quality and the ecological response of sound-producing species to natural and anthropogenic perturbations. Little is known of how underwater soundscapes respond during and after severe episodic disturbances, such as hurricanes. This study addresses the impacts of Hurricane Irma on the coral reef soundscape at two spur-and-groove fore-reef sites within the Florida Keys USA, using passive acoustic data collected before and during the storm at Western Dry Rocks (WDR) and before, during and after the storm at Eastern Sambo (ESB). As the storm passed, the cumulative acoustic exposure near the seabed at these sites was comparable to a small vessel operating continuously overhead for 1-2 weeks. Before the storm, sound pressure levels (SPLs) showed a distinct pattern of low frequency diel variation and increased high frequency sound during crepuscular periods. The low frequency band was partitioned in two groups representative of soniferous reef fish, whereas the high frequency band represented snapping shrimp sound production. Daily daytime patterns in low-frequency sound production largely persisted in the weeks following the hurricane. Crepuscular sound production by snapping shrimp was maintained post-hurricane with only a small shift (~1.5dB) in the level of daytime vs nighttime sound production for this high frequency band. This study suggests that on short time scales, temporal patterns in the coral reef soundscape were relatively resilient to acoustic energy exposure during the storm, as well as changes in the benthic habitat and environmental conditions resulting from hurricane damage.

Integrating ecosystem services considerations within a GIS-based habitat suitability index for oyster restoration.

Geospatial habitat suitability index (HSI) models have emerged as powerful tools that integrate pertinent spatial information to guide habitat restoration efforts, but have rarely accounted for spatial variation in ecosystem service provision. In this study, we utilized satellite-derived chlorophyll a concentrations for Pamlico Sound, North Carolina, USA in conjunction with data on water flow velocities and dissolved oxygen concentrations to identify potential restoration locations that would maximize the oyster reef-associated ecosystem service of water filtration. We integrated these novel factors associated with oyster water filtration ecosystem services within an existing, 'Metapopulation Persistence' focused GIS-based, HSI model containing biophysical (e.g., salinity, oyster larval connectivity) and logistical (e.g., distance to nearest restoration material stockpile site) factors to identify suitable locations for oyster restoration that maximize long-term persistence of restored oyster populations and water filtration ecosystem service provision. Furthermore, we compared the 'Water Filtration' optimized HSI with the HSI optimized for 'Metapopulation Persistence,' as well as a hybrid model that optimized for both water filtration and metapopulation persistence. Optimal restoration locations (i.e., locations corresponding to the top 1% of suitability scores) were identified that were consistent among the three HSI scenarios (i.e., "win-win" locations), as well as optimal locations unique to a given HSI scenario (i.e., "tradeoff" locations). The modeling framework utilized in this study can provide guidance to restoration practitioners to maximize the cost-efficiency and ecosystem services value of habitat restoration efforts. Furthermore, the functional relationships between oyster water filtration and chlorophyll a concentrations, water flow velocities, and dissolved oxygen applied in this study can guide field- and lab-testing of hypotheses related to optimal conditions for oyster reef restoration to maximize water quality enhancement benefits.

Oyster toadfish (Opsanus tau) boatwhistle call detection and patterns within a large-scale oyster restoration site.

During May 2015, passive acoustic recorders were deployed at eight subtidal oyster reefs within Harris Creek Oyster Sanctuary in Chesapeake Bay, Maryland USA. These sites were selected to represent both restored and unrestored habitats having a range of oyster densities. Throughout the survey, the soundscape within Harris Creek was dominated by the boatwhistle calls of the oyster toadfish, Opsanus tau. A novel, multi-kernel spectral correlation approach was developed to automatically detect these boatwhistle calls using their two lowest harmonic bands. The results provided quantitative information on how call rate and call frequency varied in space and time. Toadfish boatwhistle fundamental frequency ranged from 140 Hz to 260 Hz and was well correlated (r = 0.94) with changes in water temperature, with the fundamental frequency increasing by ~11 Hz for every 1°C increase in temperature. The boatwhistle call rate increased from just a few calls per minute at the start of monitoring on May 7th to ~100 calls/min on May 10th and remained elevated throughout the survey. As male toadfish are known to generate boatwhistles to attract mates, this rapid increase in call rate was interpreted to mark the onset of spring spawning behavior. Call rate was not modulated by water temperature, but showed a consistent diurnal pattern, with a sharp decrease in rate just before sunrise and a peak just after sunset. There was a significant difference in call rate between restored and unrestored reefs, with restored sites having nearly twice the call rate as unrestored sites. This work highlights the benefits of using automated detection techniques that provide quantitative information on species-specific call characteristics and patterns. This type of non-invasive acoustic monitoring provides long-term, semi-continuous information on animal behavior and abundance, and operates effectively in settings that are otherwise difficult to sample.

Density-dependent role of an invasive marsh grass, Phragmites australis, on ecosystem service provision.

Invasive species can positively, neutrally, or negatively affect the provision of ecosystem services. The direction and magnitude of this effect can be a function of the invaders' density and the service(s) of interest. We assessed the density-dependent effect of an invasive marsh grass, Phragmites australis, on three ecosystem services (plant diversity and community structure, shoreline stabilization, and carbon storage) in two oligohaline marshes within the North Carolina Coastal Reserve and National Estuarine Research Reserve System (NCNERR), USA. Plant species richness was equivalent among low, medium and high Phragmites density plots, and overall plant community composition did not vary significantly by Phragmites density. Shoreline change was most negative (landward retreat) where Phragmites density was highest (-0.40 ± 0.19 m yr-1 vs. -0.31 ± 0.10 for low density Phragmites) in the high energy marsh of Kitty Hawk Woods Reserve and most positive (soundward advance) where Phragmites density was highest (0.19 ± 0.05 m yr-1 vs. 0.12 ± 0.07 for low density Phragmites) in the lower energy marsh of Currituck Banks Reserve, although there was no significant effect of Phragmites density on shoreline change. In Currituck Banks, mean soil carbon content was approximately equivalent in cores extracted from low and high Phragmites density plots (23.23 ± 2.0 kg C m-3 vs. 22.81 ± 3.8). In Kitty Hawk Woods, mean soil carbon content was greater in low Phragmites density plots (36.63 ± 10.22 kg C m-3) than those with medium (13.99 ± 1.23 kg C m-3) or high density (21.61 ± 4.53 kg C m-3), but differences were not significant. These findings suggest an overall neutral density-dependent effect of Phragmites on three ecosystem services within two oligohaline marshes in different environmental settings within a protected reserve system. Moreover, the conceptual framework of this study can broadly inform an ecosystem services-based approach to invasive species management.

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.

Soundscapes and Larval Settlement: Larval Bivalve Responses to Habitat-Associated Underwater Sounds.

We quantified the effects of habitat-associated sounds on the settlement response of two species of bivalves with contrasting habitat preferences: (1) Crassostrea virginicia (oyster), which prefers to settle on other oysters, and (2) Mercenaria mercenaria (clam), which settles on unstructured habitats. Oyster larval settlement in the laboratory was significantly higher when exposed to oyster reef sound compared with either off-reef or no-sound treatments. Clam larval settlement did not vary according to sound treatments. Similar to laboratory results, field experiments showed that oyster larval settlement in "larval housings" suspended above oyster reefs was significantly higher compared with off-reef sites.

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.

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.

Timing and route of migration of mature female blue crabs in a tidal estuary.

Information on migration patterns is critical to using no-take migratory corridors and marine reserves to protect the spawning stock of commercially exploited species. Both active and passive acoustic tracking methods quantified movement of commercially and ecologically important blue crabs in the White Oak River estuary, NC, USA. We targeted post-mating female crabs migrating down-estuary to oceanic spawning grounds. Crabs travelled approximately 14.1 km mainly in deeper channels and over 12-26 days from mating areas to spawning grounds. No crabs were detected migrating down-estuary in the autumn and only 30% were detected migrating down-estuary in spring. None of the crabs detected near spawning grounds were detected or recaptured back up-estuary, suggesting that they either (i) do not return to the estuary after a one to two week period in the spawning area or (ii) were captured by fishermen. The results from this study demonstrate that (1) acoustic transmitters coupled with passive acoustic receivers provided reliable and valuable data on migration patterns of mature female blue crabs and (2) mature female blue crabs are capable of migrating primarily within deep channels to spawning grounds shortly after insemination.

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.

Molecular keys unlock the mysteries of variable survival responses of blue crabs to hypoxia.

Hypoxia is a major stressor in coastal ecosystems, yet generalizing its impacts on fish and shellfish populations across hypoxic events is difficult due to variability among individuals in their history of exposure to hypoxia and related abiotic variables, and subsequent behavioral and survival responses. Although aquatic animals have diverse physiological responses to cope with hypoxia, we know little about how inter-individual variation in physiological state affects survival and behavioral decisions under hypoxic conditions. Laboratory experiments coupled with molecular techniques determined how extrinsic factors (e.g., water body and temperature) and respiratory physiology (hemocyanin concentration and structure) affected survival and behavior of adult blue crabs (Callinectes sapidus) exposed to different levels of hypoxia over a 30-h time period. Nearly 100% of crabs survived the 1.3 mg dissolved oxygen (DO) l(-1) treatment (18.4% air saturation), suggesting that adult blue crabs are tolerant of severe hypoxia. Probability of survival decreased with increasing hypoxic exposure time, lower DO, and increasing temperature. Individual-level differences in survival correlated with water body and crab size. Crabs collected from the oligo/mesohaline and hypoxic Neuse River Estuary (NRE), North Carolina, USA survived hypoxic exposures longer than crabs from the euhaline and normoxic Bogue and Back Sounds, North Carolina. Furthermore, small NRE crabs survived longer than large NRE crabs. Hemocyanin (Hcy) concentration did not explain these individual-level differences, however, hypoxia-tolerant crabs had Hcy structures indicative of a high-O(2)-affinity form of Hcy, suggesting Hcy "quality" (i.e., structure) may be more important for hypoxia survival than Hcy "quantity" (i.e., concentration). The geographic differences in survival we observed also highlight the importance of carefully selecting experimental animals when planning to extrapolate results to the population level.

Environmental and physiological controls of blue crab avoidance behavior during exposure to hypoxia.

Generalizing the impacts of hypoxia on aquatic animal populations is difficult due to differences in behavioral and physiological responses among individuals as well as varying hydrodynamics of hypoxic events. Information on which environmental cues animals use to avoid hypoxia and how abiotic covariates and physiology influence avoidance behavior is lacking. Our laboratory flume studies quantified the interacting effects of hydrography (dissolved oxygen [DO], temperature, and salinity), hydrodynamics (rate of DO decline and current speed), and physiological state on avoidance behaviors of blue crabs (Callinectes sapidus). Changes in DO stimulated increased rates of movement, regardless of whether the change resulted in hypoxia. Increased rates of DO decline stimulated faster movement rates under hypoxic conditions because crabs spent less time in hypoxia compared to crabs under conditions of slow rate of DO decline. Blue crabs that had hemocyanin structures with a high affinity for O(2) (hypoxia-tolerant) were less active under hypoxic conditions than conspecifics with hemocyanins with a low O(2) affinity, suggesting that physiological state influences behavioral responses to stressors. These results provide a mechanistic understanding of how physiological acclimation and hypoxia hydrodynamics may influence population dynamics.

Functional response of sport divers to lobsters with application to fisheries management.

Fishery managers must understand the dynamics of fishers and their prey to successfully predict the outcome of management actions. We measured the impact of a two-day exclusively recreational fishery on Caribbean spiny lobster in the Florida Keys, USA, over large spatial scales (>100 km) and multiple years and used a theoretical, predator-prey functional response approach to identify whether or not sport diver catch rates were density-independent (type I) or density-dependent (type II or III functional response), and if catch rates were saturated (i.e., reached an asymptote) at relatively high lobster densities. We then describe how this predator-prey framework can be applied to fisheries management for spiny lobster and other species. In the lower Keys, divers exhibited a type-I functional response, whereby they removed a constant and relatively high proportion of lobsters (0.74-0.84) across all pre-fishing-season lobster densities. Diver fishing effort increased in a linear manner with lobster prey densities, as would be expected with a type-I functional response, and was an order of magnitude lower in the upper Keys than lower Keys. There were numerous instances in the upper Keys where the density of lobsters actually increased from before to after the fishing season, suggesting some type of "spill-in effect" from surrounding diver-disturbed areas. With the exception of isolated reefs in the upper Keys, the proportion of lobsters removed by divers was density independent (type-I functional response) and never reached saturation at natural lobster densities. Thus, recreational divers have a relatively simple predatory response to spiny lobster, whereby catch rates increase linearly with lobster density such that catch is a reliable indicator of abundance. Although diver predation is extremely high (approximately 80%), diver predation pressure is not expected to increase proportionally with a decline in lobster density (i.e., a depensatory response), which could exacerbate local extinction. Furthermore, management actions that reduce diver effort should have a concomitant and desired reduction in catch. The recreational diver-lobster predator-prey construct in this study provides a useful predictive framework to apply to both recreational and commercial fisheries, and on which to build as management actions are implemented.

Environmentally-controlled, density-dependent secondary dispersal in a local estuarine crab population.

The mechanisms driving the pelagic secondary dispersal of aquatic organisms following initial settlement to benthic habitats are poorly characterized. We examined the physical environmental (wind, diel cycle, tidal phase) and biological (ontogenetic, density-dependent) factors that contribute to the secondary dispersal of a benthic marine invertebrate, the blue crab (Callinectes sapidus) in Pamlico Sound, NC, USA. Field studies conducted in relatively large (0.05 km2) seagrass beds determined that secondary dispersal is primarily undertaken by the earliest juvenile blue crab instar stages (J1 crabs). These crabs emigrated pelagically from seagrass settlement habitats using nighttime flood tides during average wind conditions (speed approximately 5 m s-1). Moreover, the secondary dispersal of J1 crabs was density-dependent and regulated by intra-cohort (J1) crab density in seagrass. Our results suggest that dispersal occurs rapidly following settlement, and promotes blue crab metapopulation persistence by redistributing juveniles from high-density settlement habitats to areas characterized by low postlarval supply. Collectively, these data indicate that blue crab secondary dispersal is an active process under behavioral control and can alter initial distribution patterns established during settlement. This study highlights the necessity of considering secondary dispersal in ecological studies to improve our understanding of population dynamics of benthic organisms.