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.

Comparison of auditory evoked potential thresholds in three shark species.

Auditory sensitivity measurements have been published for only 12 of the more than 1150 extant species of elasmobranchs (sharks, skates and rays). Thus, there is a need to further understand sound perception in more species from different ecological niches. In this study, the auditory evoked potential (AEP) technique was used to compare hearing abilities of the bottom-dwelling New Zealand carpet shark (Cephaloscyllium isabellum) and two benthopelagic houndsharks (Triakidae), the rig (Mustelus lenticulatus) and the school shark (Galeorhinus galeus). AEPs were measured in response to tone bursts (frequencies: 80, 100, 150, 200, 300, 450, 600, 800 and 1200 Hz) from an underwater speaker positioned 55 cm in front of the shark in an experimental tank. AEP detection thresholds were derived visually and statistically, with statistical measures slightly more sensitive (∼4 dB) than visual methodology. Hearing abilities differed between species, mainly with respect to bandwidth rather than sensitivity. Hearing was least developed in the benthic C. isabellum [upper limit: 300 Hz, highest sensitivity: 100 Hz (82.3±1.5 dB re. 1 µm s-2)] and had a wider range in the benthopelagic rig and school sharks [upper limit: 800 Hz; highest sensitivity: 100 Hz (79.2±1.6 dB re. 1 µm s-2) for G. galeus and 150 Hz (74.8±1.8 dB re. 1 µm s-2) for M. lenticulatus]. The data are consistent with those known for 'hearing non-specialist' teleost fishes that detect only particle motion, not pressure. Furthermore, our results provide evidence that benthopelagic sharks exploit higher frequencies (max. 800 Hz) than some of the bottom-dwelling sharks (max. 300 Hz). Further behavioural and morphological studies are needed to identify what ecological factors drive differences in upper frequency limits of hearing in elasmobranchs.

Comparison of acoustic particle acceleration detection capabilities in three shark species.

Behavioural studies have shown that sharks are capable of directional orientation to sound. However, only one previous experiment addresses the physiological mechanisms of directional hearing in sharks. Here, we used a directional shaker table in combination with the auditory evoked potential (AEP) technique to understand the broadscale directional hearing capabilities in the New Zealand carpet shark (Cephaloscyllium isabellum), rig shark (Mustelus lenticulatus) and school shark (Galeorhinus galeus). The aim of this experiment was to test if sharks are more sensitive to vertical (z-axis) or head-to-tail (x-axis) accelerations, and whether there are any differences between species. Our results support previous findings, suggesting that shark ears can receive sounds from all directions. Acceleration detection bandwidth was narrowest for the carpet shark (40-200 Hz), and broader for rig and school sharks (40-800 Hz). Greatest sensitivity bands were 40-80 Hz for the carpet shark, 100-200 Hz for the rig and 80-100 Hz for the school shark. Our results indicate that there may be differences in directional hearing abilities among sharks. The bottom-dwelling carpet shark was equally sensitive to vertical and head-to-tail particle accelerations. In contrast, both benthopelagic rig and school sharks appeared to be more sensitive to vertical accelerations at frequencies up to 200 Hz. This is the first study to provide physiological evidence that sharks may differ in their directional hearing and sound localisation abilities. Further comparative physiological and behavioural studies in more species with different lifestyles, habitats and feeding strategies are needed to further explore the drivers for increased sensitivity to vertical accelerations among elasmobranchs.

Comparative sound detection abilities of four decapod crustaceans.

Sound perception and detection in decapod crustaceans is surprisingly poorly understood, even though there is mounting evidence for sound playing a critical role in many life history strategies. The suspected primary organ of sound perception is the paired statocysts at the base of the first antennal segment. To better understand the comparative sound detection of decapods, auditory evoked potentials were recorded from the statocyst nerve region of four species (Leptograpsus variegate, Plagusia chabrus, Ovalipes catharus, Austrohelice crassa) in response to two different auditory stimuli presentation methods, shaker table (particle acceleration) and underwater speaker (particle acceleration and pressure). The results showed that there was significant variation in the sound detection abilities between all four species. However, exposure to the speaker stimuli increased all four species sound detection abilities, in terms of both frequency bandwidth and sensitivity, compared with shaker table-derived sound detection abilities. This indicates that there is another sensory mechanism in play as well as the statocyst system. Overall, the present research provides comparative evidence of sound detection in decapods and indicates underwater sound detection in this animal group was even more complex than previously thought.

Energy conservation characterizes sleep in sharks.

Sharks represent the earliest group of jawed vertebrates and as such, they may provide original insight for understanding the evolution of sleep in more derived animals. Unfortunately, beyond a single behavioural investigation, very little is known about sleep in these ancient predators. As such, recordings of physiological indicators of sleep in sharks have never been reported. Reduced energy expenditure arising from sustained restfulness and lowered metabolic rate during sleep have given rise to the hypothesis that sleep plays an important role for energy conservation. To determine whether this idea applies also to sharks, we compared metabolic rates of draughtsboard sharks (Cephaloscyllium isabellum) during periods ostensibly thought to be sleep, along with restful and actively swimming sharks across a 24 h period. We also investigated behaviours that often characterize sleep in other animals, including eye closure and postural recumbency, to establish relationships between physiology and behaviour. Overall, lower metabolic rate and a flat body posture reflect sleep in draughtsboard sharks, whereas eye closure is a poorer indication of sleep. Our results support the idea for the conservation of energy as a function of sleep in these basal vertebrates.

A Gulf in lockdown: How an enforced ban on recreational vessels increased dolphin and fish communication ranges.

From midnight of 26 March 2020, New Zealand became one of the first countries to enter a strict lockdown to combat the spread of COVID-19. The lockdown banned all non-essential services and travel both on land and sea. Overnight, the country's busiest coastal waterway, the Hauraki Gulf Marine Park, became devoid of almost all recreational and non-essential commercial vessels. An almost instant change in the marine soundscape ensued, with ambient sound levels in busy channels dropping nearly threefold the first 12 h. This sudden drop led fish and dolphins to experience an immediate increase in their communication ranges by up to an estimated 65%. Very low vessel activity during the lockdown (indicated by the presence of vessel noise over the day) revealed new insights into cumulative noise effects from vessels on auditory masking. For example, at sites nearer Auckland City, communication ranges increased approximately 18 m (22%) or 50 m (11%) for every 10% decrease in vessel activity for fish and dolphins, respectively. However, further from the city and in deeper water, these communication ranges were increased by approximately 13 m (31%) or 510 m (20%). These new data demonstrate how noise from small vessels can impact underwater soundscapes and how marine animals will have to adapt to ever-growing noise pollution.

Behavioural sleep in two species of buccal pumping sharks (Heterodontus portusjacksoni and Cephaloscyllium isabellum).

Sleep is known to occur in most, if not all, animals studied thus far. Recent studies demonstrate the presence of sleep in flatworms and jellyfish, suggesting that this behaviour evolved early in the evolution of animals. Sharks are the earliest known extant, jawed vertebrates and may play an important role in understanding the evolutionary history of sleep in vertebrates, and yet, it is unknown whether they sleep. The Port Jackson (Heterodontus portusjacksoni) and draughtsboard (Cephaloscyllium isabellum) sharks are both benthic, buccal pumping species and remain motionless for extended periods of time. Whether these periods of prolonged inactivity represent sleep or quiet wakefulness is unknown. A key criterion for separating sleep from other quiescent states is an increased arousal threshold. We show here that inactive sharks of both species require significantly higher levels of electric stimulation before they show a visible response. Sharks deprived of rest, however, show no significant compensatory increase in restfulness during their normal active period following enforced swimming. Nonetheless, increased arousal thresholds in inactive animals suggest that these two species of shark sleep - the first such demonstration for members of this group of vertebrates. Further research, including electrophysiological studies, on these and other sharks, is required for a comprehensive understanding of sleep in cartilaginous fishes.

The use of evoked potentials to determine sensory sub-modality contributions to acoustic and hydrodynamic sensing.

Both the lateral line and the inner ear contribute to near-field dipole source detection in fish. The precise roles these two sensory modalities provide in extracting information about the flow field remain of interest. In this study, evoked potentials (EP, 30-200 Hz) for blind Mexican cavefish were measured in response to a dipole source. Greatest sensitivity was observed at the lower and upper ends of the tested frequency range. To evaluate the relative contributions of the lateral line and inner ear, we measured the effects of neomycin on EP response characteristics at 40 Hz, and used the vital dye DASPEI to verify neuromast ablation. Neomycin increased the latency of the EP response up until 60 min post-treatment. DASPEI results confirmed that neuromast hair cell death was significant in treated fish over this timeframe. These results indicate that the inner ear, whether it is sound pressure or particle motion detection, makes a significant contribution to the dipole-induced EP in blind cavefish at near-field low frequencies where the lateral line contribution would be expected to be strongest. The results from this study imply that under some circumstances, lateral line function could be complemented by the inner ear.

Ecology of fish hearing.

Underwater sound is directional and can convey important information about the surrounding environment or the animal emitting the sound. Therefore, sound is a major sensory channel for fishes and plays a key role in many life-history strategies. The effect of anthropogenic noise on aquatic life, which may be causing homogenisation or fragmentation of biologically important signals underwater is of growing concern. In this review we discuss the role sound plays in the ecology of fishes, basic anatomical and physiological adaptations for sound reception and production, the effects of anthropogenic noise and how fishes may be coping to changes in their environment, to put the ecology of fish hearing into the context of the modern underwater soundscape.

Vessel noise cuts down communication space for vocalizing fish and marine mammals.

Anthropogenic noise across the world's oceans threatens the ability of vocalizing marine species to communicate. Some species vocalize at key life stages or whilst foraging, and disruption to the acoustic habitat at these times could lead to adverse consequences at the population level. To investigate the risk of these impacts, we investigated the effect of vessel noise on the communication space of the Bryde's whale Balaenoptera edeni, an endangered species which vocalizes at low frequencies, and bigeye Pempheris adspersa, a nocturnal fish species which uses contact calls to maintain group cohesion while foraging. By combining long-term acoustic monitoring data with AIS vessel-tracking data and acoustic propagation modelling, the impact of vessel noise on their communication space was determined. Routine vessel passages cut down communication space by up to 61.5% for bigeyes and 87.4% for Bryde's whales. This influence of vessel noise on communication space exceeded natural variability for between 3.9 and 18.9% of the monitoring period. Additionally, during the closest point of approach of a large commercial vessel, <10 km from the listening station, the communication space of both species was reduced by a maximum of 99% compared to the ambient soundscape. These results suggest that vessel noise reduces communication space beyond the evolutionary context of these species and may have chronic effects on these populations. To combat this risk, we propose the application or extension of ship speed restrictions in ecologically significant areas, since our results indicate a reduction in sound source levels for vessels transiting at lower speeds.

Potential role of the anterior lateral line in sound localization in toadfish (Opsanus tau).

Male oyster toadfish (Opsanus tau) acoustically attract females to nesting sites using a boatwhistle call. The rapid speed of sound underwater combined with the close proximity of the otolithic organs makes inner ear interaural time differences an unlikely mechanism to localize sound. To determine the role that the mechanosensory lateral line may play in sound localization, microwire electrodes were bilaterally implanted into the anterior lateral line nerve to record neural responses to vibrational stimuli. Highest spike rates and strongest phase-locking occurred at distances close to the fish and decreased as the stimulus was moved further from the fish. Bilateral anterior lateral line neuromasts displayed differential directional sensitivity to incoming vibrational stimuli, which suggests the potential for the lateral line to be used for sound localization in the near field. The present study also demonstrates that the spatially separated neuromasts of the toadfish may provide sufficient time delays between sensory organs for determining sound localization cues. Multimodal sensory input processing through both the inner ear (far field) and lateral line (near field) may allow for effective sound localization in fish.

The Potential Overlapping Roles of the Ear and Lateral Line in Driving "Acoustic" Responses.

Examination of fish responses to sound stimuli has a rich and varied history but it is not always clear when responses are true measures of hearing or the lateral-line. The central innervation of auditory and lateral-line sensory afferents lie in close proximity in the brainstem and both sets of receptors are, at heart, hair cell-based particle motion detectors. While it is possible to separately measure physiological activity of these two receptor subtypes, many studies of fish "hearing" use whole brain potentials or behavioural assays in complex sound fields where it is not possible to distinguish inputs. We argue here that, as often measured, what is thought of as fish "hearing" is often a multisensory response of both auditory and lateral line receptors. We also argue that in many situations where fish use sound stimuli, the behaviour is also an integrative response of both systems, due to the often close proximity of fish during sound communication. We end with a set of recommendations for better understanding the separate and combined roles of ear and lateral-line hair cells as well as an acknowledgment of the seminal and continuing contributions of Arthur N. Popper and Richard R. Fay to this field.

Effects of Underwater Turbine Noise on Crab Larval Metamorphosis.

The development of marine tidal turbines has advanced at a rapid rate over the last decade but with little detailed understanding of the potential noise impacts on invertebrates. Previous research has shown that underwater reef noise plays an important role in mediating metamorphosis in many larval crabs and fishes. New research suggests that underwater estuarine noise may also mediate metamorphosis in estuarine crab larvae and that the noise emitted from underwater tidal and sea-based wind turbines may significantly influence larval metamorphosis in estuarine crabs.

Auditory sensitivity in aquatic animals.

A critical concern with respect to marine animal acoustics is the issue of hearing "sensitivity," as it is widely used as a criterion for the onset of noise-induced effects. Important aspects of research on sensitivity to sound by marine animals include: uncertainties regarding how well these species detect and respond to different sounds; the masking effects of man-made sounds on the detection of biologically important sounds; the question how internal state, motivation, context, and previous experience affect their behavioral responses; and the long-term and cumulative effects of sound exposure. If we are to better understand the sensitivity of marine animals to sound we must concentrate research on these questions. In order to assess population level and ecological community impacts new approaches can possibly be adopted from other disciplines and applied to marine fauna.

Vocalisations of the bigeye Pempheris adspersa: characteristics, source level and active space.

Fish sounds are an important biological component of the underwater soundscape. Understanding species-specific sounds and their associated behaviour is critical for determining how animals use the biological component of the soundscape. Using both field and laboratory experiments, we describe the sound production of a nocturnal planktivore, Pempheris adspersa (New Zealand bigeye), and provide calculations for the potential effective distance of the sound for intraspecific communication. Bigeye vocalisations recorded in the field were confirmed as such by tank recordings. They can be described as popping sounds, with individual pops of short duration (7.9±0.3 ms) and a peak frequency of 405±12 Hz. Sound production varied during a 24 h period, with peak vocalisation activity occurring during the night, when the fish are most active. The source level of the bigeye vocalisation was 115.8±0.2 dB re. 1 µPa at 1 m, which is relatively quiet compared with other soniferous fish. Effective calling range, or active space, depended on both season and lunar phase, with a maximum calling distance of 31.6 m and a minimum of 0.6 m. The bigeyes' nocturnal behaviour, characteristics of their vocalisation, source level and the spatial scale of its active space reported in the current study demonstrate the potential for fish vocalisations to function effectively as contact calls for maintaining school cohesion in darkness.

Anterior lateral line nerve encoding to tones and play-back vocalisations in free-swimming oyster toadfish, Opsanus tau.

In the underwater environment, sound propagates both as a pressure wave and as particle motion, with particle motion dominating close to the source. At the receptor level, the fish ear and the neuromast hair cells act as displacement detectors, and both are potentially stimulated by the particle motion component of sound. The encoding of the anterior lateral line nerve to acoustic stimuli in freely behaving oyster toadfish, Opsanus tau, was examined. Nerve sensitivity and directional responses were determined using spike rate and vector strength analysis, a measure of phase-locking of spike times to the stimulus waveform. All units showed greatest sensitivity to 100 Hz stimulus. While sensitivity was independent of stimuli orientation, the neuron's ability to phase-lock was correlated with stimuli origin. Two different types of units were classified, type 1 (tonic), and type 2 (phasic). The type 1 fibres were further classified into two sub-types based on their frequency response (type 1-1 and type 1-2), which was hypothesised to be related to canal (type 1-1) and superficial (type 1-2) neuromast innervation. Lateral line units also exhibited sensitivity and phase locking to boatwhistle vocalisations, with greatest spike rates exhibited at the onset of the call. These results provide direct evidence that oyster toadfish can use their lateral line to detect behaviourally relevant acoustic stimuli, which could provide a sensory pathway to aid in sound source localisation.

An electrophysiological correlate of sleep in a shark.

Sleep is a prominent physiological state observed across the animal kingdom. Yet, for some animals, our ability to identify sleep can be masked by behaviors otherwise associated with being awake, such as for some sharks that must swim continuously to push oxygenated seawater over their gills to breathe. We know that sleep in buccal pumping sharks with clear rest/activity cycles, such as draughtsboard sharks (Cephaloscyllium isabellum, Bonnaterre, 1788), manifests as a behavioral shutdown, postural relaxation, reduced responsiveness, and a lowered metabolic rate. However, these features of sleep do not lend themselves well to animals that swim nonstop. In addition to video and accelerometry recordings, we tried to explore the electrophysiological correlates of sleep in draughtsboard sharks using electroencephalography (EEG), electromyography, and electrooculography, while monitoring brain temperature. The seven channels of EEG activity had a surprising level of (apparent) instability when animals were swimming, but also when sleeping. The amount of stable EEG signals was too low for replication within- and across individuals. Eye movements were not measurable, owing to instability of the reference electrode. Based on an established behavioral characterization of sleep in draughtsboard sharks, we offer the original finding that muscle tone was strongest during active wakefulness, lower in quietly awake sharks, and lowest in sleeping sharks. We also offer several critical suggestions on how to improve techniques for characterizing sleep electrophysiology in future studies on elasmobranchs, particularly for those that swim continuously. Ultimately, these approaches will provide important insights into the evolutionary confluence of behaviors typically associated with wakefulness and sleep.

Interspecific Variation in the Inner Ear Maculae of Sharks.

There is well-documented diversity in the organization of inner ear hair cells in fishes; this variation is thought to reflect the differing functional requirements of species across a range of ecological niches. However, relatively little is known about interspecific variation (and its potential ecological implications) in the number and density of inner ear hair cells in elasmobranchs (sharks, skates, and rays). In this study, we quantified inner ear hair cells in the saccule, lagena, utricle, and macula neglecta of 9 taxonomically and ecologically distinct shark species. Using phylogenetically informed comparative approaches, sharks that feed in the water column had significantly greater hair cell density and total number of hair cells in the lagena and macula neglecta (i.e., vertically oriented maculae) compared to species that feed primarily on the seafloor. In addition, sharks within Carcharhinidae seemingly possess a specialized macula neglecta compared to other shark species. Overall, findings suggest that, similar to bony fishes, there is considerable variation in hair cell organization of shark inner ears, which may be tied to variation in ecology and/or specialized behaviors between different species.

Quantitative assessment of inner ear variation in elasmobranchs.

Considerable diversity has been documented in most sensory systems of elasmobranchs (sharks, rays, and skates); however, relatively little is known about morphological variation in the auditory system of these fishes. Using magnetic resonance imaging (MRI), the inner ear structures of 26 elasmobranchs were assessed in situ. The inner ear end organs (saccule, lagena, utricle, and macula neglecta), semi-circular canals (horizontal, anterior, and posterior), and endolymphatic duct were compared using phylogenetically-informed, multivariate analyses. Inner ear variation can be characterised by three primary axes that are influenced by diet and habitat, where piscivorous elasmobranchs have larger inner ears compared to non-piscivorous species, and reef-associated species have larger inner ears than oceanic species. Importantly, this variation may reflect differences in auditory specialisation that could be tied to the functional requirements and environmental soundscapes of different species.

Impact of small boat sound on the listening space of Pempheris adspersa, Forsterygion lapillum, Alpheus richardsoni and Ovalipes catharus.

Anthropogenic stressors, such as plastics and fishing, are putting coastal habitats under immense pressure. However, sound pollution from small boats has received little attention given the importance of sound in the various life history strategies of many marine animals. By combining passive acoustic monitoring, propagation modelling, and hearing threshold data, the impact of small-boat sound on the listening spaces of four coastal species was determined. Listening space reductions (LSR) were greater for fishes compared to crustaceans, for which LSR varied by day and night, due to their greater hearing abilities. Listening space also varied by sound modality for the two fish species, highlighting the importance of considering both sound pressure and particle motion. The theoretical results demonstrate that boat sound hinders the ability of fishes to perceive acoustic cues, advocating for future field-based research on acoustic cues, and highlighting the need for effective mitigation and management of small-boat sound within coastal areas worldwide.