Report of the Round Table Session
Siebert, U.1*, Houser, D.2*, André, M.3, Debusschere, E.4, Morell, M.5,3, Ruser, A.6, and Solé, M.3
1 University of Veterinary Medicine, Hannover, Germany
2 Department of Conservation and Biological Research, National Marine Mammal Foundation, USA
3 Laboratory of Applied Bioacoustics, Technical University of Catalonia, BarcelonaTech (UPC), Spain
4 Institute for Agricultural and Fisheries Research & Ghent University Belgium
5 Zoology Department, University of British Columbia, Canada
6 Institute of Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine, Hannover, Germany
Session Chairs: Ursula Siebert & Michel André
This report can be referenced as:
Siebert, U., Houser, D., André, M., Debusschere, E., Morell, M., Ruser, A., and Solé, M. (2015). Report of the Pathology Session, Oceanoise2015, Vilanova i la Geltrú, Barcelona, Spain, 10-15 May. (Editors Michel André & Peter Sigray). Retrieved from http://oceanoise2015.com
Pathology associated with anthropogenic sound exposure is fundamentally related to impacts on hearing. Panellists presented and discussed recent efforts to determine hearing functionality through the use of auditory evoked potentials (AEP), which has rapidly become a popular approach to hearing assessments in odontocete cetaceans. This approach has the greatest potential for determining population-level hearing sensitivity and demographic variability within odontocete cetaceans, as demonstrated by two of the speakers. However, the impact of AEP methods on the results of AEP hearing assessments in odontocetes was discussed as a critical issue; reports of hearing thresholds obtained within the same species by different laboratories and using different methodologies have been shown to have threshold differences on the order of tens of decibels. This is compounded by large variations in thresholds across individuals in the populations measured to date. Nevertheless, this has occasionally led to comparison statements about the hearing abilities of populations of animals that are more likely due to experimental methods and calibration procedures than to actual differences in hearing. It was proposed that future efforts to standardize methods of AEP hearing assessments in odontocetes be pursued in order to reduce variability in threshold estimates obtained by different investigators. In this manner, consistency in the offset between AEP thresholds and those obtained behaviourally, the gold standard, can be obtained. Such efforts would be particularly beneficial to regulators responsible with the enforcement of marine mammal protections and scientists and governmental agencies concerned with accurately assessing and mitigating the impact of anthropogenic sound on marine mammals. Standardization does not imply that the thresholds would be “correct” relative to behavioural thresholds, but that the estimates would be consistent across measurements. Additional exploration of AEP methods must also be performed to address the issue of problems with low frequency (e.g. <5 kHz) hearing studies in odontocetes. This is particularly important because of concerns for the potential of low-frequency sources (e.g. seismic air guns) to affect odontocetes, especially the harbour porpoise (Phocoena phocoena).
Utilizing AEPs for the testing of low frequency hearing in odontocetes remains a challenge. AEP approaches are usable for sub-kilohertz measurements in pinnipeds, but the anatomical specialization of the delphinid and phocoenid brain for echolocation likely contributes to a lower limit in its utility in species belonging to these families. It is possible that low frequency AEP approaches will be suitable for mysticete hearing tests because of the relatively less-derived brain anatomy of mysticete whales (i.e. the auditory system is apparently not evolved for echolocation, as in the odontocetes). However, this remains to be observed as few efforts have been undertaken to test mysticete hearing with AEP methods and the large size of the animals presents a different set of challenges (e.g. poor brain-to-body mass ratio, large blubber layer which attenuates neural signals).
Efforts continue to utilize the onset of temporary threshold shift (TTS), a temporary reduction in hearing sensitivity due to a sound exposure, as a means of estimating the onset of impacts to the auditory system. The onset of TTS is used by multiple countries to regulate sound producing activities in the oceans. Traditionally, TTS was assumed to be non-injurious because thresholds, obtained either behaviourally or through evoked potential methods, eventually returned to normal under experimental investigations. However, work by Kujawa and Liberman (2009), as well as other researchers, demonstrated that a robust TTS (~40 dB TTS 24 hours following the cessation of a sound exposure), resulted in a progressive degeneration of the auditory nerve and disappearance of synaptic junctions at the inner hair cell. The outer hair cells remained unaffected. These pathological consequences manifest over a period of months to years following the sound exposure and were missed in earlier studies with a shorter observation period following TTS induction. Thus, TTS has the potential to be injurious because of the destruction or loss of tissue. This finding has implications for the use of TTS as a criterion of impact in the regulation of acoustic impacts to marine mammals. However, the relevance to the marine mammal world remains open to debate. Studies of TTS and TTS-based regulations are based on the onset of TTS measured within minutes of the sound exposure, not the production of robust TTS measured 24 hours following the fatiguing stimulus. As a result, excepting an acoustic exposure that resulted in an unexpected PTS in a harbour seal, no exposures equivalent to those that induced the robust TTS observed in terrestrial mammals exists within the body of marine mammal TTS research. Because of a lack of information on differences in the long-term consequences of experiencing a minor or severe TTS, it is uncertain as to whether or not a minor TTS truly represents fully recoverable auditory fatigue, or whether it is associated with some degree of tissue damage. The progression of damage to the auditory system from the onset of TTS to the persistence of a robust TTS (e.g. 40 dB, Kujawa and Liberman (2009)) hours or days after exposure is unknown. This area of study is open to investigation, and the results of studies characterizing the relationship between acoustic exposure and tissue loss can potentially alter the regulatory landscape. However, because of ethical concerns related to the types of measurements that need to be made to determine this relationship, studies of this type will need to be creative in their approach to assessing auditory system trauma in marine mammals.
The impact of neural degeneration potentially associated with TTS is uncertain, as the inner hair cells affected in terrestrial mammals appear to be those with higher thresholds of activation. Kujawa and Liberman (2009) proposed that this may result in poor encoding of acoustic signals in poor signal to noise conditions. There are no psychophysical studies that have been conducted to provide evidence for or against this hypothesis, which further confounds the ability to determine the magnitude of the long-term consequences potentially associated with TTS. However, as pointed at in the discussion, this type of hearing loss, in addition to other forms of hearing impacts (e.g. masking, age-related hearing loss), lacks a comprehensive integration into both understanding the cumulative impacts to marine mammals and the ability to regulate these impacts. As more information becomes available on the magnitude of various hearing related impacts to marine mammals, it is reasonable to assume that there will be a lag time between discovery and synthesizing disparate studies into a comprehensive framework of cumulative hearing impacts. This, unfortunately, will suffer further lag as it undergoes regulatory integration, particularly since regulations are often driven by the word of the law and not the emerging science.
At the other extreme of the uncertainty in the relationship between TTS and its potential for injury is the potential for marine mammals to protect themselves from acoustic trauma. Although evidence exists for a protective mechanism in odontocetes, the mechanism itself is elusive. Potential mechanisms briefly discussed include stapedial reflexes and neural protective mechanisms (Nachtigall and Supin, 2015). Beyond being poorly understood, the degree to which these mechanisms can protect animal hearing, and whether or not they are under conscious control, requires much further study.
One approach to potentially improve understanding of the impact of sound on marine mammals is the post-mortem histology and microscopy of marine mammal inner ear tissues. Promising advances have been made in this area of study and frequency placement maps have been developed for a number of marine mammal species based on inner ear morphology (Houser et al. 2001; Parks et al. 2007). An integrated approach to inner ear structure could be potentially powerful when access to animals while they are alive, prior to natural death or euthanasia, permits a better clinical evaluation of the animal. Conversely, validation of frequency-position maps is required as these provide a predictive tool of the hearing range. This is likely to be best achieved by conducting electrophysiological studies in animals prior to death and comparing to post-mortem morphological predictions of hearing loss (or range of hearing). However, as with TTS studies previously discussed, this approach may need to be creative in order to address potential ethical concerns associated with animal use.
In addition to cetaceans, it is necessary and urgent to increase the studies about the pathological effects in other taxa of marine animals, especially fishes and invertebrates, because of their fundamental role in the ecological net of the oceans, like being the prey of cetaceans and the predators of other species. Recent findings on cephalopods showed that exposure to artificial noise had a direct consequence on the functionality and physiology of the statocysts, which are sensory organs analogue to the vertebrate inner ear, and responsible for the animal’s equilibrium, also playing a part in their movement through the water column, and vital for the detection of low-frequency sounds (Octopus vulgaris , Kaifu et al . 2008; Sepioteuthis lessoniana, Octopus vulgaris , Hu et al . 2009; Loligo pealei , Mooney et al . 2010). These experiments proved for the first time the sensitivity of marine invertebrates to sound exposure through pathological effects. Due to a lack of data on other species of invertebrates, the ultrascopically visible pathological effects of sound exposure on two species of Mediterranean Scyphozoan medusa were presented in the session. The lesions described are new to Cnidarian’s pathology and are compatible with massive acoustic trauma observed in other species that have been exposed to similar stimuli (André, et al. 2011, Solé et al. 2012; 2013). Given that low-frequency noise levels in the ocean are increasing and that reliable data on the bioacoustics of invertebrates are scarce, this urges a necessary development of efforts and resources dedicated to research on the effects of sound on invertebrates in order to contribute to a sustainable use of the global marine environment.
Although not directly relevant to the pathology discussion, a good point arose about utilizing bottlenose dolphins (or any species) as surrogates for other species of marine mammals. Several other species have shown lower thresholds of sensitivity, both behaviourally and physiologically, than bottlenose dolphins. For example, harbour porpoises have lower thresholds for behavioural reactions to sound and to the onset of TTS than do bottlenose dolphins for relatively similar levels of sound exposure (Finneran 2015). Conversely, there are species that, at least behaviourally, show a similar degree of robustness to bottlenose (e.g. pilot whales). Additionally, there is evidence that sound pathways may vary somewhat between species. This presents a challenge for selecting and testing surrogate species, as well as extrapolating from laboratory settings to wild animals. Given the limited number of species available for any form of testing, what then is the appropriate approach by which to group species and select appropriate surrogates? Although prior groupings of species based on hearing specialty has advanced efforts to mitigate and regulate anthropogenic acoustic impacts to marine mammals, it seems probable that other grouping approaches (e.g. an ecological grouping of species) may also be beneficial, particularly if such groupings can be integrated with hearing specializations. Complicating this approach, however, may be the difficulty of capturing the nuances of animal behaviour in which noise sources will be tolerated for other purposes, such as feeding or mating. Several instances were noted in which marine mammals have been observed to presumably tolerate noise exposures in order to capitalize on easily captured prey species more seriously affected by the anthropogenic sound exposures (e.g. Cox et al. 2003; Jacobs and Terhune 2002). However, it cannot be discounted that marine mammals have a better knowledge of the noise field than is accomplished through modelling and utilize areas of reduced sound exposure when exploiting prey near acoustic sources.
– André, M., Solé, M., Lenoir, M., Durfort, M., Quero, C., Mas, A., Lombarte, A., van der Schaar, M., López-Bejar, M., Morell, M., Zaugg, S., Houégnigan, L. Low-frequency sounds induce acoustic trauma in cephalopods. Frontiers in Ecology and the Environment (e-View) , p.doi:10.1890/100124, 2011.
– Cox, T. M., A. J. Read, D. Swanner, K. Urian, and D. Waples. 2003. Behavioral responses of bottlenose dolphins, Tursiops truncatus, to gillnets and acoustic alarms. Biol Conserv 115:203-212.
– Finneran, J. J. 2015. Noise-induced hearing loss in marine mammals: A review of temporary threshold shift studies from 1996 to 2015. J Acoust Soc Ame 138(3):1702-1726.
– Houser, D. S., D. A. Helweg, and P. W. B. Moore. 2001. A bandpass filter-bank model of auditory sensitivity in the humpback whale. Aq Mammals 27:82-91.
– Hu MY, Yan HY, Chung W, et al. 2009. Acoustically evoked potentials in two cephalopods inferred using the auditory brainstem response (ABR) approach. Comp Biochem Phys A 153: 278–84.
– Jacobs, S.R.and Terhune, J.M. (2002) The effectiveness of acoustic harassment devices in the Bay of Fundy, Canada: seal reactions and a noise exposure model. Aq Mammals, 28, 147–158.
– Kaifu K, Akamatsu T, and Segawa S. 2008. Underwater sound detection by cephalopod statocyst. Fisheries Sci 74: 781–86.
– Kujawa, S. G., & Liberman, M. C. (2009). Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. Journal of Neuroscience, 29(45), 14077-14085.
– Mooney AT, Hanlon RT, Christensen-Dalsgaard, J, et al. 2010. Sound detection by the longfin squid (Loligo pealei) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure. J Exp Biol: 213, 3748–59.
– Nachtigall, P. E., and A. Y. Supin. 2015. Conditioned frequency-dependent hearing sensitivity reduction in the bottlenose dolphin (Tursiops truncatus). J Exp Biol 218:999-1005.
– Parks, S. E., D. R. Ketten, J. T. O’Malley, and J. Arruda. 2007. Anatomical predictions of hearing in the North Atlantic right whale. Anatomical Record 290:734–744.
– Solé, M., Lenoir, M., Durfort, M., López-Bejar, Lombarte, A., van der Schaar, M., André, M. 2012. Does exposure to noise from human activities compromise sensory information from cephalopod statocysts? Deep-Sea Res. II (2012), http://dx.doi.org/10.1016/j.dsr2.2012.10.006
– Solé, M., Lenoir, M., Durfort, M., López-Bejar, Lombarte, A., van der Schaar, M., André, M. 2013. Ultrastructural Damage of Loligo vulgaris and Illex coindetii statocysts after Low Frequency Sound Exposure. PLoS ONE 8(10): e78825. doi:10.1371/journal.pone.0078825