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.

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.

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.

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.

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.

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.

Ontogeny of the inner ear maculae in school sharks (Galeorhinus galeus).

Studies on the auditory system of fishes can provide fundamental information about the early evolution of vertebrate hearing. While there are limited data available on the auditory system of bony fishes, comparatively far less is known about auditory structures in elasmobranchs, despite their critical basal position within vertebrate evolution. Specifically, while there is a high degree of plasticity in the nervous system, little is known about how the different sensory epithelia within the inner ear vary throughout life in elasmobranchs. Using a combination of immunohistochemistry and fluorescence microscopy, we quantified macular area, number of sensory hair cells, hair cell density, and hair cell orientations in the saccule, lagena, utricle, and macula neglecta of school sharks (Galeorhinus galeus) of varying body size. In all maculae, macular area and the number of hair cells increased significantly throughout ontogeny, while hair cell density displayed a concurrent ontogenetic decrease (excluding the utricle). There were also significant differences in macular area, hair cell number, and hair cell density between the four maculae. However, hair cell orientation patterns did not vary between individuals and did not change with body growth. These findings represent one of the first comprehensive characterisations of the inner ear sensory epithelia in an elasmobranch, and reveal changes in morphology that may have implications for auditory capabilities through ontogeny.

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.

Small recreational boats: a ubiquitous source of sound pollution in shallow coastal habitats.

Sound from small recreational boats spans a wide range of frequencies and source levels, but the degree to which this impacts the soundscapes of shallow coastal habitats is poorly understood. Here, long-term passive acoustic recordings at five shallow coastal sites, including two MPAs, were used to quantify spatio-temporal variation in small boat sound and its effect on the soundscape. Boats were detected almost every day at each site, irrespective of protection status, significantly elevating the low-frequency (100-800 Hz) component of the soundscape. This frequency band is used by many species for communication, orientation, and predator avoidance. Therefore, highlighting the potential for small boat sound to alter soundscapes and mask cues. Existing tools for monitoring sound pollution are targeted at sound from shipping. These data highlight that the broadband and highly variable sound emitted by small boats must be considered when evaluating anthropogenic impacts on coastal marine ecosystems worldwide.

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.

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.

Marine soundscape variation reveals insights into baleen whales and their environment: a case study in central New Zealand.

Baleen whales reliably produce stereotyped vocalizations, enabling their spatio-temporal distributions to be inferred from acoustic detections. Soundscape analysis provides an integrated approach whereby vocal species, such as baleen whales, are sampled holistically with other acoustic contributors to their environment. Acoustic elements that occur concurrently in space, time and/or frequency can indicate overlaps between free-ranging species and potential stressors. Such information can inform risk assessment framework models. Here, we demonstrate the utility of soundscape monitoring in central New Zealand, an area of high cetacean diversity where potential threats are poorly understood. Pygmy blue whale calls were abundant in the South Taranaki Bight (STB) throughout recording periods and were also detected near Kaikoura during autumn. Humpback, Antarctic blue and Antarctic minke whales were detected in winter and spring, during migration. Wind, rain, tidal and wave activity increased ambient sound levels in both deep- and shallow-water environments across a broad range of frequencies, including those used by baleen whales, and sound from shipping, seismic surveys and earthquakes overlapped in time, space and frequency with whale calls. The results highlight the feasibility of soundscape analysis to quantify and understand potential stressors to free-ranging species, which is essential for conservation and management decisions.

The soundscape of the Anthropocene ocean.

Oceans have become substantially noisier since the Industrial Revolution. Shipping, resource exploration, and infrastructure development have increased the anthrophony (sounds generated by human activities), whereas the biophony (sounds of biological origin) has been reduced by hunting, fishing, and habitat degradation. Climate change is affecting geophony (abiotic, natural sounds). Existing evidence shows that anthrophony affects marine animals at multiple levels, including their behavior, physiology, and, in extreme cases, survival. This should prompt management actions to deploy existing solutions to reduce noise levels in the ocean, thereby allowing marine animals to reestablish their use of ocean sound as a central ecological trait in a healthy ocean.

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.

Diverse Activity Rhythms in Sharks (Elasmobranchii).

Sharks are an interesting group of vertebrates, as many species swim continuously to "ram" oxygen-rich seawater over their gills (ram ventilators), whereas other species "pump" seawater over their gills by manipulating buccal cavity volume while remaining motionless (buccal pumpers). This difference in respiratory physiology raises the question: What are the implications of these differences in lifestyle for circadian rhythms? We investigated the diel activity patterns of 5 species of sharks, including 3 ram ventilating species: the school shark (Galeorhinus galeus), the spotted estuary smooth-hound (Mustelus lenticulatus), and the spiny dogfish (Squalus acanthias); and 2 buccal pumping species: the Port Jackson (Heterodontus portusjacksoni) and draughtsboard (Cephaloscyllium isabellum) sharks. We measured the amount, duration, and distance traveled while swimming over multiple days under a 12:12 light:dark light regime for all species and used modified light regimes for species with a clear diel rhythm in activity. We identified a surprising diversity of activity rhythms. The school shark and smooth-hound swam continuously; however, whereas the school shark swam at the same speed and covered the same distance during the day and night, the smooth-hound swam slower at night and traversed a shorter distance. A similar pattern was observed in the spiny dogfish, although this shark swam less overall. Both the Port Jackson and draughtsboard sharks showed a marked nocturnal preference for swimming. This pattern was muted and disrupted during constant light and constant dark regimes, although circadian organization of this pattern was maintained under certain conditions. The consequences of these patterns for other biological processes, such as sleep, remain unclear. Nonetheless, these 5 species demonstrate remarkable diversity within the activity rhythms of sharks.

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.

Barking mad: The vocalisation of the John Dory, Zeus faber.

Studies on the behavioural function of sounds are very rare within heterospecific interactions. John Dory (Zeus faber) is a solitary, predatory fish that produces sound when captured, but has not been documented to vocalize under natural conditions (i.e. in the wild). The present study provides the first in-situ recordings of John Dory vocalisations and correlates them to behavioural response of snapper (Pagrus auratus) a common species found through New Zealand. Vocalisations or 'barks', ranged between 200-600 Hz, with a peak frequency of 312 ± 10 Hz and averaged 139 ± 4 milliseconds in length. Baited underwater video (BUV) equipped with hydrophones determined that under natural conditions a John Dory vocalization induced an escape response in snapper present, causing them to exit the area opposite to the position of the John Dory. We speculate that the John Dory vocalisation may be used for territorial display towards both conspecifics and heterospecifics, asserting dominance in the area or heightening predatory status.

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 effect of motorboat sound on Australian snapper Pagrus auratus inside and outside a marine reserve.

Human-generated sound affects hearing, movement, and communication in both aquatic and terrestrial animals, but direct natural underwater behavioral observations are lacking. Baited underwater video (BUV) were deployed in near shore waters adjacent to Goat Island in the Cape Rodney-Okakari Point Marine Reserve (protected) or outside the reserve approximately four km south in Mathesons Bay (open), New Zealand to determine the natural behavior of Australian snapper Pagrus auratus exposed to motorboat sound. BUVs worked effectively at bringing fish into video range to assess the effects of sound. The snapper inhabiting the protected area showed no behavioral response to motorboat transits; however, fish in the open zones either scattered from the video frame or decreased feeding activity during boat presence. Our study suggests that motorboat sound, a common source of anthropogenic activity in the marine environment can affect fish behavior differently depending on the status of their habitat (protected versus open).