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.

Bioadhesive interface for marine sensors on diverse soft fragile species.

Marine animals equipped with sensors provide vital information for understanding their ecophysiology and collect oceanographic data on climate change and for resource management. Existing methods for attaching sensors to marine animals mostly rely on invasive physical anchors, suction cups, and rigid glues. These methods can suffer from limitations, particularly for adhering to soft fragile marine species such as squid and jellyfish, including slow complex operations, unreliable fixation, tissue trauma, and behavior changes of the animals. However, soft fragile marine species constitute a significant portion of ocean biomass (>38.3 teragrams of carbon) and global commercial fisheries. Here we introduce a soft hydrogel-based bioadhesive interface for marine sensors that can provide rapid (time <22 s), robust (interfacial toughness >160 J m-2), and non-invasive adhesion on various marine animals. Reliable and rapid adhesion enables large-scale, multi-animal sensor deployments to study biomechanics, collective behaviors, interspecific interactions, and concurrent multi-species activity. These findings provide a promising method to expand a burgeoning research field of marine bio-sensing from large marine mammals and fishes to small, soft, and fragile marine animals.

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.

Soundscape enrichment increases larval settlement rates for the brooding coral Porites astreoides.

Coral reefs, hubs of global biodiversity, are among the world's most imperilled habitats. Healthy coral reefs are characterized by distinctive soundscapes; these environments are rich with sounds produced by fishes and marine invertebrates. Emerging evidence suggests these sounds can be used as orientation and settlement cues for larvae of reef animals. On degraded reefs, these cues may be reduced or absent, impeding the success of larval settlement, which is an essential process for the maintenance and replenishment of reef populations. Here, in a field-based study, we evaluated the effects of enriching the soundscape of a degraded coral reef to increase coral settlement rates. Porites astreoides larvae were exposed to reef sounds using a custom solar-powered acoustic playback system. Porites astreoides settled at significantly higher rates at the acoustically enriched sites, averaging 1.7 times (up to maximum of seven times) more settlement compared with control reef sites without acoustic enrichment. Settlement rates decreased with distance from the speaker but remained higher than control levels at least 30 m from the sound source. These results reveal that acoustic enrichment can facilitate coral larval settlement at reasonable distances, offering a promising new method for scientists, managers and restoration practitioners to rebuild coral reefs.

Global inventory of species categorized by known underwater sonifery.

A working group from the Global Library of Underwater Biological Sounds effort collaborated with the World Register of Marine Species (WoRMS) to create an inventory of species confirmed or expected to produce sound underwater. We used several existing inventories and additional literature searches to compile a dataset categorizing scientific knowledge of sonifery for 33,462 species and subspecies across marine mammals, other tetrapods, fishes, and invertebrates. We found 729 species documented as producing active and/or passive sounds under natural conditions, with another 21,911 species deemed likely to produce sounds based on evaluated taxonomic relationships. The dataset is available on both figshare and WoRMS where it can be regularly updated as new information becomes available. The data can also be integrated with other databases (e.g., SeaLifeBase, Global Biodiversity Information Facility) to advance future research on the distribution, evolution, ecology, management, and conservation of underwater soniferous species worldwide.

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.

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.

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.

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.

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.

Pile driving repeatedly impacts the giant scallop (Placopecten magellanicus).

Large-scale offshore wind farms are a critical component of the worldwide climate strategy. However, their developments have been opposed by the fishing industry because of concerns regarding the impacts of pile driving vibrations during constructions on commercially important marine invertebrates, including bivalves. Using field-based daily exposure, we showed that pile driving induced repeated valve closures in different scallop life stages, with particularly stronger effects for juveniles. Scallops showed no acclimatization to repetitive pile driving across and within days, yet quickly returned to their initial behavioral baselines after vibration-cessation. While vibration sensitivity was consistent, daily pile driving did not disrupt scallop circadian rhythm, but suggests serious impacts at night when valve openings are greater. Overall, our results show distance and temporal patterns can support future mitigation strategies but also highlight concerns regarding the larger impact ranges of impending widespread offshore wind farm constructions on scallop populations.

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.

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.

Changes in feeding behavior of longfin squid (Doryteuthis pealeii) during laboratory exposure to pile driving noise.

Anthropogenic noise can cause diverse changes in animals' behaviors, but effects on feeding behaviors are understudied, especially for key invertebrate taxa. With the offshore wind industry expanding, concern exists regarding potential impacts of pile driving noise on squid and other commercially and ecologically vital taxa. We investigated changes in feeding and alarm (defense) behaviors of squid, Doryteuthis pealeii, predating on killifish, Fundulus heteroclitus, during playbacks of pile driving noise recorded from wind farm construction within squids' habitat. Fewer squid captured killifish during noise exposure compared to controls. Squid had more failed predation attempts when noise was started during predation sequences. Alarm responses to noise were similar whether or not squid were hunting killifish, indicating similar vigilance to threat stimuli in these contexts. Additionally, novel hearing measurements on F. heteroclitus confirmed they could detect the noise. These results indicate noise can disrupt feeding behaviors of a key invertebrate species, and will leverage future studies on how noise may disrupt squids' vital ecological interactions.

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.

Listening forward: approaching marine biodiversity assessments using acoustic methods.

Ecosystems and the communities they support are changing at alarmingly rapid rates. Tracking species diversity is vital to managing these stressed habitats. Yet, quantifying and monitoring biodiversity is often challenging, especially in ocean habitats. Given that many animals make sounds, these cues travel efficiently under water, and emerging technologies are increasingly cost-effective, passive acoustics (a long-standing ocean observation method) is now a potential means of quantifying and monitoring marine biodiversity. Properly applying acoustics for biodiversity assessments is vital. Our goal here is to provide a timely consideration of emerging methods using passive acoustics to measure marine biodiversity. We provide a summary of the brief history of using passive acoustics to assess marine biodiversity and community structure, a critical assessment of the challenges faced, and outline recommended practices and considerations for acoustic biodiversity measurements. We focused on temperate and tropical seas, where much of the acoustic biodiversity work has been conducted. Overall, we suggest a cautious approach to applying current acoustic indices to assess marine biodiversity. Key needs are preliminary data and sampling sufficiently to capture the patterns and variability of a habitat. Yet with new analytical tools including source separation and supervised machine learning, there is substantial promise in marine acoustic diversity assessment methods.

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.

Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae.

Ocean acidification (OA) and warming seas are significant concerns for coastal systems and species. The Atlantic longfin squid, Doryteuthis pealeii, a core component of the Northwest Atlantic trophic web, has demonstrated impacts, such as reduced growth and delayed development, under high chronic exposure to acidification (2200 ppm), but the combined effects of OA and warming have not been explored in this species. In this study, D. pealeii egg capsules were reared under a combination of several acidification levels (400, 2200, and 3500 ppm) and temperatures (20 and 27°C). Hatchlings were measured for a range of metrics [dorsal mantle length (DML), yolk sac volume (YV), malformation, and hatching success] in three trials over the 2016 breeding season (May - October). Although notable resistance to stressors was seen, highlighting variability within and between clutches, reduced DML and malformation of the embryos occurred at the highest OA exposure. Surprisingly, increased temperatures did not appear to exacerbate OA impacts, although responses were variable. Time to hatching, which increased with acidification, decreased much more drastically under warming and, further, decreased or removed delays caused by acidification. Hatching success, while variable by clutch, showed consistent patterns of greater late stage loss of embryos under acidification and greater early stage loss under warming, highlighting the potential difference in timing between these stressors for this system, i.e., that acidification stress builds up and causes impacts over time within the egg capsule as the embryos grow and respire. High OA-exposed hatchlings from the warmer conditions often showed reduced impacts compared to those reared in ambient temperatures. This may be due to the increased developmental rate and subsequently reduced OA exposure time of embryos in the higher temperature treatment. These results indicate a substantive potential plasticity to multiple stressors during the embryonic development of this species of squid, but do not predict how this species would fare under these future ocean scenarios.

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.