Sound detection and production mechanisms in aquatic decapod and stomatopod crustaceans.

The sensory systems of crustaceans (aquatic decapods and stomatopods) have adapted to a diverse range of aquatic ecosystems. Sound production in aquatic crustaceans is more widespread than previously thought, and has been shown to play a major role in many of their life-history strategies; however, there are still many gaps in our understanding of their sound reception abilities. Crustaceans have three main sensory receptors for sound - the statocyst, superficial hair cells and chordotonal organs - which are all sensitive to the particle motion component of the sound field, rather than the pressure component. Our current understanding of these receptors is that they are sensitive to low-frequency sounds (<2000 Hz). There are a wide variety of sound-producing mechanisms employed by these animals, ranging from stridulation to implosive cavitation (see Glossary). These signals are used for a range of social behaviours, such as courtship, territorial defence and assessing 'resource guarding'. Furthermore, there are examples of sound signals that exceed their hearing range, highlighting a mismatch in our understanding of their hearing systems. This mismatch provides weight to the suggestion that another sound transmission channel - substrate-borne vibrations - might be at play, particularly because most crustaceans live on or near the seafloor. Finally, suggestions are made regarding potential future work that is needed to fill the substantial gaps in our understanding of how crustaceans hear and produce sound.

Monitoring spatial and temporal soundscape features within ecologically significant U.S. National Marine Sanctuaries.

The U.S. National Oceanic and Atmospheric Administration's Office of National Marine Sanctuaries manages a system of marine protected areas encompassing more than 2,000,000 km2 . U.S. National Marine Sanctuaries (NMS) have been designated to provide protection for their conservation, recreational, ecological, historical, scientific, cultural, archaeological, educational, or aesthetic qualities. Due to the large variability of attributes among NMS, designing coordinated system-wide monitoring to support diverse resource protection goals can be challenging. Underwater sound monitoring is seeing increasing application to marine protected area management because it is able to support this wide variety of information needs. Passive acoustics are providing invaluable autonomous information regarding habitat associations, identifying species spatial and temporal use, and highlighting patterns in conditions that are otherwise difficult to survey. Using standardized equipment and analysis methods this study collected ambient underwater sound data and derived measurements to investigate temporal changes in sound pressure levels and power spectral density, identify presence of select species of importance and support within and among site comparison of ambient underwater sound among eight sites within four U.S. NMS. Broadband sound pressure levels of ambient sound (10-24,000 Hz) varied as much as 24 dB re 1 µPa (max difference 100-124 dB re 1 µPa) among the recording sites, sanctuaries, and seasons. Biotic signals, such as snapping shrimp snaps and vocalizations of fishes, exhibited distinct diel and seasonal patterns and showed variation among sites. Presence of anthropogenic signals, such as vessel passage, also varied substantially among sites, ranging from on average 1.6-21.8 h/d. The study identified measurements that effectively summarized baseline soundscape attributes and prioritized future opportunities for integrating non-acoustic and acoustic variables in order to inform area-specific management questions within four ecologically varying U.S. National Marine Sanctuaries.

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.

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.

Impulsive pile driving noise elicits alarm responses in squid (Doryteuthis pealeii).

Pile driving occurs during construction of marine platforms, including offshore windfarms, producing intense sounds that can adversely affect marine animals. We quantified how a commercially and economically important squid (Doryteuthis pealeii: Lesueur 1821) responded to pile driving sounds recorded from a windfarm installation within this species' habitat. Fifteen-minute portions of these sounds were played to 16 individual squid. A subset of animals (n = 11) received a second exposure after a 24-h rest period. Body pattern changes, inking, jetting, and startle responses were observed and nearly all squid exhibited at least one response. These responses occurred primarily during the first 8 impulses and diminished quickly, indicating potential rapid, short-term habituation. Similar response rates were seen 24-h later, suggesting squid re-sensitized to the noise. Increased tolerance of anti-predatory alarm responses may alter squids' ability to deter and evade predators. Noise exposure may also disrupt normal intraspecific communication and ecologically relevant responses to sound.

Underwater sound from vessel traffic reduces the effective communication range in Atlantic cod and haddock.

Stellwagen Bank National Marine Sanctuary is located in Massachusetts Bay off the densely populated northeast coast of the United States; subsequently, the marine inhabitants of the area are exposed to elevated levels of anthropogenic underwater sound, particularly due to commercial shipping. The current study investigated the alteration of estimated effective communication spaces at three spawning locations for populations of the commercially and ecologically important fishes, Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus). Both the ambient sound pressure levels and the estimated effective vocalization radii, estimated through spherical spreading models, fluctuated dramatically during the three-month recording periods. Increases in sound pressure level appeared to be largely driven by large vessel activity, and accordingly exhibited a significant positive correlation with the number of Automatic Identification System tracked vessels at the two of the three sites. The near constant high levels of low frequency sound and consequential reduction in the communication space observed at these recording sites during times of high vocalization activity raises significant concerns that communication between conspecifics may be compromised during critical biological periods. This study takes the first steps in evaluating these animals' communication spaces and alteration of these spaces due to anthropogenic underwater sound.

Reef Sound as an Orientation Cue for Shoreward Migration by Pueruli of the Rock Lobster, Jasus edwardsii.

The post-larval or puerulus stage of spiny, or rock, lobsters (Palinuridae) swim many kilometres from open oceans into coastal waters where they subsequently settle. The orientation cues used by the puerulus for this migration are unclear, but are presumed to be critical to finding a place to settle. Understanding this process may help explain the biological processes of dispersal and settlement, and be useful for developing realistic dispersal models. In this study, we examined the use of reef sound as an orientation cue by the puerulus stage of the southern rock lobster, Jasus edwardsii. Experiments were conducted using in situ binary choice chambers together with replayed recording of underwater reef sound. The experiment was conducted in a sandy lagoon under varying wind conditions. A significant proportion of puerulus (69%) swam towards the reef sound in calm wind conditions. However, in windy conditions (>25 m s-1) the orientation behaviour appeared to be less consistent with the inclusion of these results, reducing the overall proportion of pueruli that swam towards the reef sound (59.3%). These results resolve previous speculation that underwater reef sound is used as an orientation cue in the shoreward migration of the puerulus of spiny lobsters, and suggest that sea surface winds may moderate the ability of migrating pueruli to use this cue to locate coastal reef habitat to settle. Underwater sound may increase the chance of successful settlement and survival of this valuable species.

Vessel Noise Promotes Hull Fouling.

Fouling of submerged vessel hulls due to the rapid settlement of algae and invertebrates is a longstanding and costly problem. It is widely thought that the presence of extensive vacant surfaces on vessel hulls is responsible for the rapid attachment and growth of biofouling. We investigated whether noise from vessels in port could also be involved in promoting the settlement and growth of common biofouling organisms on vessel hulls. Three important biofouling species exhibited significantly faster development and settlement and better survival when exposed to vessel noise compared with control species. The extent of these responses appeared to vary in relation to the intensity of the vessel noise and may help to explain differences in biofouling observed on vessel hulls.

Inducers of settlement and moulting in post-larval spiny lobster.

The rapid and often remote location of suitable habitats used by migrating organisms is often critical to their subsequent recruitment, fitness and survival, and this includes in the marine environment. However, for the non-feeding post-larval stage of spiny lobsters, effective settlement cues for habitat selection are critical to their success but are poorly described. Therefore, the current study examined whether acoustic and substrate cues have the potential to shorten the time to moulting and affect their subsequent nutritional condition in the pueruli of the southern spiny lobster, Jasus edwardsii. Individuals moulted to first instar juveniles up to 38% faster when exposed to the underwater sound from two types of typical settlement habitat (coastal kelp- and urchin-dominated reefs) compared to those with no underwater sound. The settlement delay in the post-larvae without underwater sound also resulted in juveniles in poorer survival and nutritional condition as measured by their protein and lipid contents. In a separate experiment, post-larvae presented with seaweed and rock substrates were found to complete settlement and moult to juvenile by as much as 20% faster compared to those on the sand and control treatments. Overall, the results are the first to demonstrate that the pueruli of J. edwardsii have the ability to detect and respond to underwater sound, as well as determining that both acoustic and substrate cues play a role in modulating physiological development during settlement.

Fouling in your own nest: vessel noise increases biofouling.

Globally billions of dollars are spent each year on attempting to reduce marine biofouling on commercial vessels, largely because it results in higher fuel costs due to increased hydrodynamic drag. Biofouling has been long assumed to be primarily due to the availability of vacant space on the surface of the hull. Here, it is shown that the addition of the noise emitted through a vessel's hull in port increases the settlement and growth of biofouling organisms within four weeks of clean surfaces being placed in the sea. More than twice as many bryozoans, oysters, calcareous tube worms and barnacles settled and established on surfaces with vessel noise compared to those without. Likewise, individuals from three species grew significantly larger in size in the presence of vessel noise. The results demonstrate that vessel noise in port is promoting biofouling on hulls and that underwater sound plays a much wider ecological role in the marine environment than was previously considered possible.

Location, location, location: finding a suitable home among the noise.

While sound is a useful cue for guiding the onshore orientation of larvae because it travels long distances underwater, it also has the potential to convey valuable information about the quality and type of the habitat at the source. Here, we provide, to our knowledge, the first evidence that settlement-stage coastal crab species can interpret and show a strong settlement and metamorphosis response to habitat-related differences in natural underwater sound. Laboratory- and field-based experiments demonstrated that time to metamorphosis in the settlement-stage larvae of common coastal crab species varied in response to different underwater sound signatures produced by different habitat types. The megalopae of five species of both temperate and tropical crabs showed a significant decrease in time to metamorphosis, when exposed to sound from their optimal settlement habitat type compared with other habitat types. These results indicate that sounds emanating from specific underwater habitats may play a major role in determining spatial patterns of recruitment in coastal crab species.

Behavioural response thresholds in New Zealand crab megalopae to ambient underwater sound.

A small number of studies have demonstrated that settlement stage decapod crustaceans are able to detect and exhibit swimming, settlement and metamorphosis responses to ambient underwater sound emanating from coastal reefs. However, the intensity of the acoustic cue required to initiate the settlement and metamorphosis response, and therefore the potential range over which this acoustic cue may operate, is not known. The current study determined the behavioural response thresholds of four species of New Zealand brachyuran crab megalopae by exposing them to different intensity levels of broadcast reef sound recorded from their preferred settlement habitat and from an unfavourable settlement habitat. Megalopae of the rocky-reef crab, Leptograpsus variegatus, exhibited the lowest behavioural response threshold (highest sensitivity), with a significant reduction in time to metamorphosis (TTM) when exposed to underwater reef sound with an intensity of 90 dB re 1 µPa and greater (100, 126 and 135 dB re 1 µPa). Megalopae of the mud crab, Austrohelice crassa, which settle in soft sediment habitats, exhibited no response to any of the underwater reef sound levels. All reef associated species exposed to sound levels from an unfavourable settlement habitat showed no significant change in TTM, even at intensities that were similar to their preferred reef sound for which reductions in TTM were observed. These results indicated that megalopae were able to discern and respond selectively to habitat-specific acoustic cues. The settlement and metamorphosis behavioural response thresholds to levels of underwater reef sound determined in the current study of four species of crabs, enables preliminary estimation of the spatial range at which an acoustic settlement cue may be operating, from 5 m to 40 km depending on the species. Overall, these results indicate that underwater sound is likely to play a major role in influencing the spatial patterns of settlement of coastal crab species.