Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching

Disturbance from whale-watching can cause significant behavioural changes with fitness consequences for targeted whale populations. However, the sensory stimuli triggering these responses are unknown, preventing effective mitigation. Here, we test the hypothesis that vessel noise level is a driver of disturbance, using humpback whales (Megaptera novaeangliae) as a model species. We conducted controlled exposure experiments (n = 42) on resting mother-calf pairs on a resting ground off Australia, by simulating whale-watch scenarios with a research vessel (range 100 m, speed 1.5 knts) playing back vessel noise at control/low (124/148 dB), medium (160 dB) or high (172 dB) low frequency-weighted source levels (re 1 μPa RMS@1 m). Compared to control/low treatments, during high noise playbacks the mother’s proportion of time resting decreased by 30%, respiration rate doubled and swim speed increased by 37%. We therefore conclude that vessel noise is an adequate driver of behavioural disturbance in whales and that regulations to mitigate the impact of whale-watching should include noise emission standards

Cetacean noise criteria revisited in the light of proposed exposure limits for harbour porpoises

The impact of underwater noise on marine life calls for identification of exposure criteria to inform mitigation. Here we review recent experimental evidence with focus on the high-frequency cetaceans and discuss scientifically-based initial exposure criteria. A range of new TTS experiments suggest that harbour and finless porpoises are more sensitive to sound than expected from extrapolations based on results from bottlenose dolphins. Furthermore, the results from TTS experiments and field studies of behavioural reactions to noise, suggest that response thresholds and TTS critically depend on stimulus frequency. Sound exposure levels for pure tones that induce TTS are reasonably consistent at about 100 dB above the hearing threshold for pure tones and sound pressure thresholds for avoidance reactions are in the range of 40-50 dB above the hearing threshold. We propose that frequency weighting with a filter function approximating the inversed audiogram might be appropriate when assessing impact

Time-varying auditory gain control in response to double-pulse stimuli in harbour porpoises is not mediated by a stapedial reflex

Echolocating animals reduce their output level and hearing sensitivity with decreasing echo delays, presumably to stabilize the perceived echo intensity during target approaches. In bats, this variation in hearing sensitivity is formed by a call-induced stapedial reflex that tapers off over time after the call. Here, we test the hypothesis that a similar mechanism exists in toothed whales by subjecting a trained harbour porpoise to a series of double sound pulses varying in delay and frequency, while measuring the magnitudes of the evoked auditory brainstem responses (ABRs). We find that the recovery of the ABR to the second pulse is frequency dependent, and that a stapedial reflex therefore cannot account for the reduced hearing sensitivity at short pulse delays. We propose that toothed whale auditory time-varying gain control during echolocation is not enabled by the middle ear as in bats, but rather by frequency-dependent mechanisms such as forward masking and perhaps higher-order control of efferent feedback to the outer hair cells

Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-toparticle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods

Harbour porpoises react to low levels of high frequency vessel noise

Cetaceans rely critically on sound for navigation, foraging and communication and are therefore potentially affected by increasing noise levels from human activities at sea. Shipping is the main contributor of anthropogenic noise underwater, but studies of shipping noise effects have primarily considered baleen whales due to their good hearing at low frequencies, where ships produce most noise power. Conversely, the possible effects of vessel noise on small toothed whales have been largely ignored due to their poor low-frequency hearing. Prompted by recent findings of energy at medium- to high-frequencies in vessel noise, we conducted an exposure study where the behaviour of four porpoises (Phocoena phocoena) in a net-pen was logged while they were exposed to 133 vessel passages. Using a multivariate generalised linear mixed-effects model, we show that low levels of high frequency components in vessel noise elicit strong, stereotyped behavioural responses in porpoises. Such low levels will routinely be experienced by porpoises in the wild at ranges of more than 1000 meters from vessels, suggesting that vessel noise is a, so far, largely overlooked, but substantial source of disturbance in shallow water areas with high densities of both porpoises and vessels

Whale-watch vessel noise levels with applications to whale-watching guidelines and conservation

The number and size of whale-watching and swim-with-cetacean vessels are increasing worldwide, but the noise impact on targeted species depends on vessel source characteristics, which remain largely unquantified. Here, we report the acoustic characteristics from 13 whale-watching vessels from Australia and Canary Islands. Acoustic recorders were deployed to measure the frequency-weighted sound levels (for low [LF], mid [MF] and high frequency [HF] cetacean hearing types) of motor sailing, catamarans, and motor vessels operating at 4–8 kn representing the slow speed of whale-watch scenarios. The highest estimated source levels (SLs) were recorded from large catamarans with inboard engines (LF = 160 ± 3, MF = 148 ± 2, HF = 146 ± 2 dB re 1 µPa m). The lowest SLs were from smaller motor vessels and particularly by a hybrid vessel powered by electrical outboard engines (LF = 140 ± 3, MF = 136 ± 2, HF = 134 ± 2 dB re 1 µPa m). We demonstrate that at the same speed and distance, different vessels may produce very different received levels to the animals. To reduce disturbance to cetaceans we recommend tourism vessels meet a broadband (0.2–10 kHz) SL limit of <150 dB re 1 µPa (RMS) when within 500 m of cetaceans

Characteristics and propagation of airgun pulses in shallow water with implications for effects on small marine mammals

Airguns used in seismic surveys are among the most prevalent and powerful anthropogenic noise sources in marine habitats. They are designed to produce most energy below 100 Hz, but the pulses have also been reported to contain medium-to-high frequency components with the potential to affect small marine mammals, which have their best hearing sensitivity at higher frequencies. In shallow water environments, inhabited by many of such species, the impact of airgun noise may be particularly challenging to assess due to complex propagation conditions. To alleviate the current lack of knowledge on the characteristics and propagation of airgun pulses in shallow water with implications for effects on small marine mammals, we recorded pulses from a single airgun with three operating volumes (10 in3, 25 in3 and 40 in3) at six ranges (6, 120, 200, 400, 800 and 1300 m) in a uniform shallow water habitat using two calibrated Reson 4014 hydrophones and four DSG-Ocean acoustic data recorders. We show that airgun pulses in this shallow habitat propagated out to 1300 meters in a way that can be approximated by a 18log(r) geometric transmission loss model, but with a high pass filter effect from the shallow water depth. Source levels were back-calculated to 192 dB re µPa2s (sound exposure level) and 200 dB re 1 µPa dB Leq-fast (rms over 125 ms duration), and the pulses contained substantial energy up to 10 kHz, even at the furthest recording station at 1300 meters. We conclude that the risk of causing hearing damage when using single airguns in shallow waters is small for both pinnipeds and porpoises. However, there is substantial potential for significant behavioral responses out to several km from the airgun, well beyond the commonly used shut-down zone of 500 meters

Energy compensation and received echo level dynamics in constant-frequency bats during active target approaches

This work was supported by the Semper Arden Carlsberg grant to P.T.M., by a National Science Foundation grant [1658620] to R.M. and by a National Natural Science Foundation of China [11574183] to R.M.Bats have been reported to adjust the energy of their outgoing vocalizations to target range (R) in a logarithmic fashion close to 20log10R which has been interpreted as providing one-way compensation for increasing echo levels during target approaches. However, it remains unknown how species using high-frequency calls, which are strongly affected by absorption, adjust their vocal outputs during approaches to point targets. We hypothesized that such species should compensate less than the 20log10R model predicts at longer distances and more at shorter distances as a consequence of the significant influence of absorption at longer ranges. Using a microphone array and an acoustic recording tag, we show that the output adjustments of two Hipposideros pratti and one Hipposideros armiger do not decrease logarithmically during approaches to different-sized targets. Consequently, received echo levels increase dramatically early in the approach phase with near-constant output levels, but level off late in the approach phase as a result of substantial output reductions. To improve echo-to-noise ratio, we suggest that bats using higher frequency vocalizations compensate less at longer ranges, where they are strongly affected by absorption. Close to the target, they decrease their output levels dramatically to mitigate reception of very high echo levels. This strategy maintains received echo levels between 6 and 40 dB re. 20 µPa2 s across different target sizes. The bats partially compensated for target size, but not in a one-to-one dB fashion, showing that these bats do not seek to stabilize perceived echo levels, but may instead use them to gauge target size.Publisher PDFPeer reviewe

Sperm whale echolocation behaviour reveals a directed, prior-based search strategy informed by prey distribution

The fieldwork was funded by a grant from the Carlsberg Foundation to B. Møhl and ONR, SERDP and FNU grants to MJ, PJOM and PTM. PJOM was supported by a Royal Society Fellowship, NAS by the International Campus of Excellence of the Canary Islands, MJ by the Marine Alliance for Science and Technology for Scotland and AF partly by project CETOBAPH (grant number CGL2009-1311218).Predators make foraging decisions based upon sensory information about resource availability, but little is known about how large, air-breathing predators collect and use such information to maximize energy returns when foraging in the deep sea. Here, we used archival tags to study how echolocating sperm whales (Physeter macrocephalus) use their long-range sensory capabilities to guide foraging in a deep-water habitat consisting of multiple, depth-segregated prey layers. Sperm whales employ a directed search behaviour by modulating their overall sonar sampling with the intention to exploit a particular prey layer. They forage opportunistically during some descents while actively adjusting their acoustic gaze to sequentially track different prey layers. While foraging within patches, sperm whales adjust their clicking rate both to search new water volumes as they turn and to match the prey distribution. This strategy increases information flow and suggests that sperm whales can perform auditory stream segregation of multiple targets when echolocating. Such flexibility in sampling tactics in concert with long-range sensing capabilities apparently allow sperm whales to efficiently locate and access prey resources in vast, heterogeneous, deep water habitats.PostprintPeer reviewe

Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales

Author Posting. © Elsevier B.V., 2007. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Deep Sea Research Part I: Oceanographic Research Papers 54 (2007): 1421-1444, doi:10.1016/j.dsr.2007.04.020.Toothed whales produce short, ultrasonic clicks of high directionality and source level to probe their environment acoustically. This process, termed echolocation, is to a large part governed by the properties of the emitted clicks. Therefore derivation of click source parameters from free-ranging animals is of increasing importance to understand both how toothed whales use echolocation in the wild and how they may be monitored acoustically. This paper addresses how source parameters can be derived from free-ranging toothed whales in the wild using calibrated multi-hydrophone arrays and digital recorders. We outline the properties required of hydrophones, amplifiers and analog to digital converters, and discuss the problems of recording echolocation clicks on the axis of a directional sound beam. For accurate localization the hydrophone array apertures must be adapted and scaled to the behavior of, and the range to, the clicking animal, and precise information on hydrophone locations is critical. We provide examples of localization routines and outline sources of error that lead to uncertainties in localizing clicking animals in time and space. Furthermore we explore approaches to time series analysis of discrete versions of toothed whale clicks that are meaningful in a biosonar context.This work was supported by a Steno Fellowship from the Danish National Science Foundation to PTM, a grant from the Carlsberg Foundation to MW with additional support to the authors from Reson, the Novo Nordisk Science Foundation, Aarhus University Research Fund, and the Oticon Foundation