Microorganisms uniquely capture and predict stony coral tissue loss disease and hurricane disturbance impacts on US Virgin Island reefs.

Coral reef ecosystems are now commonly affected by major climate and disease disturbances. Disturbance impacts are typically recorded using reef benthic cover, but this may be less reflective of other ecosystem processes. To explore the potential for reef water-based disturbance indicators, we conducted a 7-year time series on US Virgin Island reefs where we examined benthic cover and reef water nutrients and microorganisms from 2016 to 2022, which included two major disturbances: hurricanes Irma and Maria in 2017 and the stony coral tissue loss disease outbreak starting in 2020. The disease outbreak coincided with the largest changes in the benthic habitat, with increases in the percent cover of turf algae and Ramicrusta, an invasive alga. While sampling timepoint contributed most to changes in reef water nutrient composition and microbial community beta diversity, both disturbances led to increases in ammonium concentration, a mechanism likely contributing to observed microbial community shifts. We identified 10 microbial taxa that were sensitive and predictive of increasing ammonium concentration. This included the decline of the oligotrophic and photoautotrophic Prochlorococcus and the enrichment of heterotrophic taxa. As disturbances impact reefs, the changing nutrient and microbial regimes may foster a type of microbialization, a process that hastens reef degradation.

Frequency-dependent temporary threshold shifts in the Eastern painted turtle (Chrysemys picta picta).

Testudines are a highly threatened group facing an array of stressors, including alteration of their sensory environment. Underwater noise pollution has the potential to induce hearing loss and disrupt detection of biologically important acoustic cues and signals. To examine the conditions that induce temporary threshold shifts (TTS) in hearing in the freshwater Eastern painted turtle (Chrysemys picta picta), three individuals were exposed to band limited continuous white noise (50-1000 Hz) of varying durations and amplitudes (sound exposure levels ranged from 151 to 171 dB re 1 µPa2 s). Control and post-exposure auditory thresholds were measured and compared at 400 and 600 Hz using auditory evoked potential methods. TTS occurred in all individuals at both test frequencies, with shifts of 6.1-41.4 dB. While the numbers of TTS occurrences were equal between frequencies, greater shifts were observed at 600 Hz, a frequency of higher auditory sensitivity, compared to 400 Hz. The onset of TTS occurred at 154 dB re 1 µPa2 s for 600 Hz, compared to 158 dB re 1 µPa2 s at 400 Hz. The 400-Hz onset and patterns of TTS growth and recovery were similar to those observed in previously studied Trachemys scripta elegans, suggesting TTS may be comparable across Emydidae species.

Toward a New Era of Coral Reef Monitoring.

Coral reefs host some of the highest concentrations of biodiversity and economic value in the oceans, yet these ecosystems are under threat due to climate change and other human impacts. Reef monitoring is routinely used to help prioritize reefs for conservation and evaluate the success of intervention efforts. Reef status and health are most frequently characterized using diver-based surveys, but the inherent limitations of these methods mean there is a growing need for advanced, standardized, and automated reef techniques that capture the complex nature of the ecosystem. Here we draw on experiences from our own interdisciplinary research programs to describe advances in in situ diver-based and autonomous reef monitoring. We present our vision for integrating interdisciplinary measurements for select "case-study" reefs worldwide and for learning patterns within the biological, physical, and chemical reef components and their interactions. Ultimately, these efforts could support the development of a scalable and standardized suite of sensors that capture and relay key data to assist in categorizing reef health. This framework has the potential to provide stakeholders with the information necessary to assess reef health during an unprecedented time of reef change as well as restoration and intervention activities.

Sound sensitivity of the giant scallop (Placopecten magelanicus) is life stage, intensity, and frequency dependent.

There is increasing concern that anthropogenic sounds have a significant impact on marine animals, but there remains insufficient data on sound sensitivities for most invertebrates, despite their ecological and economic importance. We quantified auditory thresholds (in particle acceleration levels) and bandwidth of the giant scallop (Placopecten magellanicus) and subsequently sought to discern sensitivity among two different life stages: juveniles (1 yr olds) and subadults (3 yr olds). We also leveraged a novel valvometry technique to quantify the amplitude of scallop valve gape reductions when exposed to different sound amplitudes and frequencies. Behavioral responses were obtained for lower frequencies below 500 Hz, with best sensitivity at 100 Hz. There were significant differences between the auditory thresholds of juveniles and subadults, with juveniles being more sensitive, suggesting ontogenetic differences in hearing sensitivity. Scallops showed intensity and frequency dependent responses to sounds, with higher valve closures to lower frequencies and higher sound levels. To our knowledge, these are the first data highlighting life stage, intensity, and frequency responses to sound in a marine benthic invertebrate. These results demonstrate clear sound sensitivity and underscore that the potential impacts of anthropogenic sound in valuable ecological resources, such as scallops, may be dependent on sound characteristics.

Acoustic properties and shallow water propagation distances of Caribbean spiny lobster sounds (Panulirus argus).

Marine crustaceans produce broadband sounds that are useful for passive acoustic monitoring to support conservation and management efforts. However, the propagation characteristics and detection ranges of their signals are poorly known, limiting our leveraging of these sounds. Here, we used a four-hydrophone linear array to measure source levels (SLs) and sound propagation from Caribbean spiny lobsters (Panulirus argus) of a wide range of sizes within a natural, shallow water habitat (3.3 m depth). Source level in peak-peak (SLpp) varied with body size; larger individuals produced SLpp up to 166 dB re 1 µPa. However, transmission losses (TL) were similar across all sizes, with a global fitted TL of 12.1 dB. Correspondingly, calculated detection ranges varied with body size, ranging between 14 and 364 m for small and large individuals (respectively). This increased up to 1612 m for large spiny lobsters when considering lower ambient noise levels. Despite the potential ease of tank studies, our results highlight the importance of empirical in situ sound propagation studies for marine crustaceans. Given the important ecological and economic role of spiny lobsters, these data are a key step to supporting remote monitoring of this species for fisheries management and efforts to acoustically quantify coral reefs' health.

Daytime boat sound does not affect the behavior of wild thorny oysters (Spondylus americanus): A field-based study.

There is increasing awareness of boat sound effects on coral reef assemblages. While behavioral disturbances have been found in fishes, the effects on marine invertebrates remain largely unknown. Here, the behavioral effects of recreational boat sound on thorny oysters at two coral reef habitats within the U.S. Virgin Island National Park were assessed. The "treatment" site was characterized by frequent boat traffic, which increased daytime mean particle acceleration levels (PALrms) by more than 6 dB, while mean PALrms at the "control" site were not contaminated by boat sound. Despite these contrasting soundscapes, all oysters showed the same diurnal cycle, with their valves open at night and partially closed during the day. There was no statistical evidence of behavioral responses in oysters exposed to daytime boat sound. This can be explained by low auditory sensitivity, habituation to a noisy environment due to the pervasiveness of boat sound pollution, or that boat sound may not represent an immediate concern for this species. These findings contrast with laboratory studies that have shown behavioral responses in bivalves exposed to boat sound, highlighting the need for more realistic field-based studies when evaluating potential effects of anthropogenic sounds on this group.

Temporary noise-induced underwater hearing loss in an aquatic turtle (Trachemys scripta elegans).

Noise pollution in aquatic environments can cause hearing loss in noise-exposed animals. We investigated whether exposure to continuous underwater white noise (50-1000 Hz) affects the auditory sensitivity of an aquatic turtle Trachemys scripta elegans (red-eared slider) across 16 noise conditions of differing durations and amplitudes. Sound exposure levels (SELs) ranged between 155 and 193 dB re 1 µPa2 s, and auditory sensitivity was measured at 400 Hz using auditory evoked potential methods. Comparing control and post-exposure thresholds revealed temporary threshold shifts (TTS) in all three individuals, with at least two of the three turtles experiencing TTS at all but the two lowest SELs tested, and shifts up to 40 dB. There were significant positive relationships between shift magnitude and exposure duration, amplitude, and SEL. The mean predicted TTS onset was 160 dB re 1 µPa2 s. There was individual variation in susceptibility to TTS, threshold shift magnitude, and recovery rate, which was non-monotonic and occurred on time scales ranging from < 1 h to > 2 days post-exposure. Recovery rates were generally greater after higher magnitude shifts. Sound levels inducing hearing loss were comparatively low, suggesting aquatic turtles may be more sensitive to underwater noise than previously considered.

Soundscapes as heard by invertebrates and fishes: Particle motion measurements on coral reefs.

Coral reef soundscapes are increasingly studied for their ecological uses by invertebrates and fishes, for monitoring habitat quality, and to investigate effects of anthropogenic noise pollution. Few examinations of aquatic soundscapes have reported particle motion levels and variability, despite their relevance to invertebrates and fishes. In this study, ambient particle acceleration was quantified from orthogonal hydrophone arrays over several months at four coral reef sites, which varied in benthic habitat and fish communities. Time-averaged particle acceleration magnitudes were similar across axes, within 3 dB. Temporal trends of particle acceleration corresponded with those of sound pressure, and the strength of diel trends in both metrics significantly correlated with percent coral cover. Higher magnitude particle accelerations diverged further from pressure values, potentially representing sounds recorded in the near field. Particle acceleration levels were also reported for boat and example fish sounds. Comparisons with particle acceleration derived audiograms suggest the greatest capacity of invertebrates and fishes to detect soundscape components below 100 Hz, and poorer detectability of soundscapes by invertebrates compared to fishes. Based on these results, research foci are discussed for which reporting of particle motion is essential, versus those for which sound pressure may suffice.

Tank acoustics substantially distort broadband sounds produced by marine crustaceans.

Marine crustaceans produce broadband sounds that have been mostly characterized in tanks. While tank physical impacts on such signals are documented in the acoustic community, they are overlooked in the bioacoustic literature with limited empirical comparisons. Here, we compared broadband sounds produced at 1 m from spiny lobsters (Panulirus argus) in both tank and in situ conditions. We found significant differences in all sound features (temporal, power, and spectral) between tank and in situ recordings, highlighting that broadband sounds, such as those produced by marine crustaceans, cannot be accurately characterized in tanks. We then explained the three main physical impacts that distort broadband sounds in tanks, respectively known as resonant frequencies, sound reverberation, and low frequency attenuation. Tank resonant frequencies strongly distort the spectral shape of broadband sounds. In the high frequency band (above the tank minimum resonant frequency), reverberation increases sound duration. In the low frequency band (below the tank minimum resonant frequency), low frequencies are highly attenuated due to their longer wavelength compared to the tank size and tank wall boundary conditions (zero pressure) that prevent them from being accurately measured. Taken together, these results highlight the importance of understanding tank physical impacts when characterizing broadband crustacean sounds.

Sound detection by the American lobster (Homarus americanus).

Although many crustaceans produce sounds, their hearing abilities and mechanisms are poorly understood, leaving uncertainties regarding whether or how these animals use sound for acoustic communication. Marine invertebrates lack gas-filled organs required for sound pressure detection, but some of them are known to be sensitive to particle motion. Here, we examined whether the American lobster (Homarus americanus) could detect sound and subsequently sought to discern the auditory mechanisms. Acoustic stimuli responses were measured using auditory evoked potential (AEP) methods. Neurophysiological responses were obtained from the brain using tone pips between 80 and 250 Hz, with best sensitivity at 80-120 Hz. There were no significant differences between the auditory thresholds of males and females. Repeated controls (recordings from deceased lobsters, moving electrodes away from the brain and reducing seawater temperature) indicated the evoked potentials' neuronal origin. In addition, AEP responses were similar before and after antennules (including statocysts) were ablated, demonstrating that the statocysts, a long-proposed auditory structure in crustaceans, are not the sensory organs responsible for lobster sound detection. However, AEPs could be eliminated (or highly reduced) after immobilizing hairfans, which cover much of lobster bodies. These results suggest that these external cuticular hairs are likely to be responsible for sound detection, and imply that hearing is mechanistically possible in a wider array of invertebrates than previously considered. Because the lobsters' hearing range encompasses the fundamental frequency of their buzzing sounds, it is likely that they use sound for intraspecific communication, broadening our understanding of the sensory ecology of this commercially vital species. The lobsters' low-frequency acoustic sensitivity also underscores clear concerns about the potential impacts of anthropogenic noise.

A field study of auditory sensitivity of the Atlantic puffin, Fratercula arctica.

Hearing is vital for birds as they rely on acoustic communication with parents, mates, chicks and conspecifics. Amphibious seabirds face many ecological pressures, having to sense cues in air and underwater. Natural noise conditions have helped shape this sensory modality but anthropogenic noise is increasingly impacting seabirds. Surprisingly little is known about their hearing, despite their imperiled status. Understanding sound sensitivity is vital when we seek to manage the impacts of man-made noise. We measured the auditory sensitivity of nine wild Atlantic puffins, Fratercula arctica, in a capture-and-release setting in an effort to define their audiogram and compare these data with the hearing of other birds and natural rookery noise. Auditory sensitivity was tested using auditory evoked potential (AEP) methods. Responses were detected from 0.5 to 6 kHz. Mean thresholds were below 40 dB re. 20 µPa from 0.75 to 3 kHz, indicating that these were the most sensitive auditory frequencies, similar to other seabirds. Thresholds in the 'middle' frequency range 1-2.5 kHz were often down to 10-20 dB re. 20 µPa. The lowest thresholds were typically at 2.5 kHz. These are the first in-air auditory sensitivity data from multiple wild-caught individuals of a deep-diving alcid seabird. The audiogram was comparable to that of other birds of similar size, thereby indicating that puffins have fully functioning aerial hearing despite the constraints of their deep-diving, amphibious lifestyles. There was some variation in thresholds, yet animals generally had sensitive ears, suggesting aerial hearing is an important sensory modality for this taxon.

Ontogenetic variation in the auditory sensitivity of black sea bass (Centropristis striata) and the implications of anthropogenic sound on behavior and communication.

Black sea bass (Centropristis striata) is an important fish species in both commercial and recreational fisheries of southern New England and the mid-Atlantic Bight. Due to the intense urbanization of these waters, this species is subject to a wide range of anthropogenic noise pollution. Concerns that C. striata are negatively affected by pile driving and construction noise predominate in areas earmarked for energy development. However, as yet, the hearing range of C. striata is unknown, making it hard to evaluate potential risks. This study is a first step in understanding the effects of anthropogenic noise on C. striata by determining the auditory detection bandwidth and thresholds of this species using auditory evoked potentials, creating pressure and acceleration audiograms. These physiological tests were conducted on wild-caught C. striata in three size/age categories. Results showed that juvenile C. striata had the significantly lowest thresholds, with auditory sensitivity decreasing in the larger size classes. Furthermore, C.striata has fairly sensitive sound detection relative to other related species. Preliminary investigations into the mechanisms of their sound detection ability were undertaken with gross dissections and an opportunistic micro-computed tomography image to address the auditory structures including otoliths and swim bladder morphology. Crucially, the auditory detection bandwidth of C. striata, and their most sensitive frequencies, directly overlap with high-amplitude anthropogenic noise pollution such as shipping and underwater construction.

The common murre (Uria aalge), an auk seabird, reacts to underwater sound.

Marine mammals have fine-tuned hearing abilities, which makes them vulnerable to human-induced sounds from shipping, sonars, pile drivers, and air guns. Many species of marine birds, such as penguins, auks, and cormorants, find their food underwater where light is often limited, suggesting sound detection may play a vital role. Yet, for most marine birds, it is unknown whether they are using, and can thereby be affected by, underwater sound. The authors conducted a series of playback experiments to test whether Alcid seabirds responded to and were disrupted by, underwater sound. Underwater broadband sound bursts and mid-frequency naval 53 C sonar signals were presented to two common murres (Uria aalge) in a quiet pool. The received sound pressure levels varied from 110 to 137 dB re 1 µPa. Both murres showed consistent reactions to sounds of all intensities, as compared to no reactions during control trials. For one of the birds, there was a clearly graded response, so that more responses were found at higher received levels. The authors' findings indicate that common murres may be affected by, and therefore potentially also vulnerable to, underwater noise. The effect of man-made noise on murres, and possibly other marine birds, requires more thorough consideration.

Audiogram of a Cook Inlet beluga whale (Delphinapterus leucas).

Noise is a stressor to wildlife, yet the precise sound sensitivity of individuals and populations is often unknown or unmeasured. Cook Inlet, Alaska belugas (CIBs) are a critically endangered and declining marine mammal population. Anthropogenic noise is a primary threat to these animals. Auditory evoked potentials were used to measure the hearing of a wild, stranded CIB as part of its rehabilitation assessment. The beluga showed broadband (4-128 kHz) and sensitive hearing (<80 dB) for a wide-range of frequencies (16-80 kHz), reflective of a healthy odontocete auditory system. Data were similar to healthy, adult belugas from the comparative Bristol Bay population (the only other published data set of healthy, wild marine mammal hearing). Repeated October and December 2017 measurements were similar, showing continued auditory health of the animal throughout the rehabilitation period. Hearing data were compared to pile-driving and container-ship noise measurements made in Cook Inlet, two sources of concern, suggesting masking is likely at ecologically relevant distances. These data provide the first empirical hearing data for a CIB allowing for estimations of sound-sensitivity in this population. The beluga's sensitive hearing and likelihood of masking show noise is a clear concern for this population struggling to recover.

Augmenting biologging with supervised machine learning to study in situ behavior of the medusa Chrysaora fuscescens.

Zooplankton play critical roles in marine ecosystems, yet their fine-scale behavior remains poorly understood because of the difficulty in studying individuals in situ Here, we combine biologging with supervised machine learning (ML) to propose a pipeline for studying in situ behavior of larger zooplankton such as jellyfish. We deployed the ITAG, a biologging package with high-resolution motion sensors designed for soft-bodied invertebrates, on eight Chrysaora fuscescens in Monterey Bay, using the tether method for retrieval. By analyzing simultaneous video footage of the tagged jellyfish, we developed ML methods to: (1) identify periods of tag data corrupted by the tether method, which may have compromised prior research findings, and (2) classify jellyfish behaviors. Our tools yield characterizations of fine-scale jellyfish activity and orientation over long durations, and we conclude that it is essential to develop behavioral classifiers on in situ rather than laboratory data.

Quantifying the swimming gaits of veined squid (Loligo forbesii) using bio-logging tags.

Squid are mobile, diverse, ecologically important marine organisms whose behavior and habitat use can have substantial impacts on ecosystems and fisheries. However, as a consequence in part of the inherent challenges of monitoring squid in their natural marine environment, fine-scale behavioral observations of these free-swimming, soft-bodied animals are rare. Bio-logging tags provide an emerging way to remotely study squid behavior in their natural environments. Here, we applied a novel, high-resolution bio-logging tag (ITAG) to seven veined squid, Loligo forbesii, in a controlled experimental environment to quantify their short-term (24 h) behavioral patterns. Tag accelerometer, magnetometer and pressure data were used to develop automated gait classification algorithms based on overall dynamic body acceleration, and a subset of the events were assessed and confirmed using concurrently collected video data. Finning, flapping and jetting gaits were observed, with the low-acceleration finning gaits detected most often. The animals routinely used a finning gait to ascend (climb) and then glide during descent with fins extended in the tank's water column, a possible strategy to improve swimming efficiency for these negatively buoyant animals. Arms- and mantle-first directional swimming were observed in approximately equal proportions, and the squid were slightly but significantly more active at night. These tag-based observations are novel for squid and indicate a more efficient mode of movement than suggested by some previous observations. The combination of sensing, classification and estimation developed and applied here will enable the quantification of squid activity patterns in the wild to provide new biological information, such as in situ identification of behavioral states, temporal patterns, habitat requirements, energy expenditure and interactions of squid through space-time in the wild.

Field-based hearing measurements of two seabird species.

Hearing is a primary sensory modality for birds. For seabirds, auditory data is challenging to obtain and hearing data are limited. Here, we present methods to measure seabird hearing in the field, using two Alcid species: the common murre Uria aalge and the Atlantic puffin Fratercula arctica Tests were conducted in a portable semi-anechoic crate using physiological auditory evoked potential (AEP) methods. The crate and AEP system were easily transportable to northern Iceland field sites, where wild birds were caught, sedated, studied and released. The resulting data demonstrate the feasibility of a field-based application of an established neurophysiology method, acquiring high quality avian hearing data in a relatively quiet setting. Similar field methods could be applied to other seabirds, and other bird species, resulting in reliable hearing data from a large number of individuals with a modest field effort. The results will provide insights into the sound sensitivity of species facing acoustic habitat degradation.

Acoustic recordings of rough-toothed dolphin (Steno bredanensis) offshore Eastern Sicily (Mediterranean Sea).

Rough-toothed dolphin's abundance and distribution is largely unknown worldwide and evaluation of its conservation status in the Mediterranean Sea is necessary. A rough-toothed dolphin was sighted offshore Eastern Sicily (Mediterranean Sea) in July 2017 and acoustic data were acquired in the same area of Watkins, Tyack, Moore, and Notarbartolo di Sciara [(1987). Mar. Mamm. Sci. 3, 78-82]. An automatic detection algorithm was developed to identify the echolocation clicks recorded within both datasets and a recurrent inter-click interval value was identified during the new encounter. Distinctive whistle classes were also identified with similar contour shapes within both datasets.

Variation in hearing within a wild population of beluga whales (Delphinapterus leucas).

Documenting hearing abilities is vital to understanding a species' acoustic ecology and for predicting the impacts of increasing anthropogenic noise. Cetaceans use sound for essential biological functions such as foraging, navigation and communication; hearing is considered to be their primary sensory modality. Yet, we know little regarding the hearing of most, if not all, cetacean populations, which limits our understanding of their sensory ecology, population level variability and the potential impacts of increasing anthropogenic noise. We obtained audiograms (5.6-150 kHz) of 26 wild beluga whales to measure hearing thresholds during capture-release events in Bristol Bay, AK, USA, using auditory evoked potential methods. The goal was to establish the baseline population audiogram, incidences of hearing loss and general variability in wild beluga whales. In general, belugas showed sensitive hearing with low thresholds (<80 dB) from 16 to 100 kHz, and most individuals (76%) responded to at least 120 kHz. Despite belugas often showing sensitive hearing, thresholds were usually above or approached the low ambient noise levels measured in the area, suggesting that a quiet environment may be associated with hearing sensitivity and that hearing thresholds in the most sensitive animals may have been masked. Although this is just one wild population, the success of the method suggests that it should be applied to other populations and species to better assess potential differences. Bristol Bay beluga audiograms showed substantial (30-70 dB) variation among individuals; this variation increased at higher frequencies. Differences among individual belugas reflect that testing multiple individuals of a population is necessary to best describe maximum sensitivity and population variance. The results of this study quadruple the number of individual beluga whales for which audiograms have been conducted and provide the first auditory data for a population of healthy wild odontocetes.

Loudness-dependent behavioral responses and habituation to sound by the longfin squid (Doryteuthis pealeii).

Sound is an abundant cue in the marine environment, yet we know little regarding the frequency range and levels which induce behavioral responses in ecologically key marine invertebrates. Here we address the range of sounds that elicit unconditioned behavioral responses in squid Doryteuthis pealeii, the types of responses generated, and how responses change over multiple sound exposures. A variety of response types were evoked, from inking and jetting to body pattern changes and fin movements. Squid responded to sounds from 80 to 1000 Hz, with response rates diminishing at the higher and lower ends of this frequency range. Animals responded to the lowest sound levels in the 200-400 Hz range. Inking, an escape response, was confined to the lower frequencies and highest sound levels; jetting was more widespread. Response latencies were variable but typically occurred after 0.36 s (mean) for jetting and 0.14 s for body pattern changes; pattern changes occurred significantly faster. These results demonstrate that squid can exhibit a range of behavioral responses to sound include fleeing, deimatic and protean behaviors, all of which are associated with predator evasion. Response types were frequency and sound level dependent, reflecting a relative loudness concept to sound perception in squid.