Report of the Round Table Session
Lucke, K.1*, Popper, A.N.2, Hawkins, A.D. 3, Akamatsu, T.4, André, M.5, Branstetter, B.K.6, Lammers, M.7, Radford, C.A.8, Stansbury, A.L.9 and Mooney, T.A.10*
1 Centre for Marine Science & Technology, Curtin University, Australia
2 Department of Biology, University of Maryland, College Park, USA
3 Loughine Marine Research, UK
4 National Research Institute of Fisheries Science, Fisheries Research Agency, Japan
5 Laboratory of Applied Bioacoustics, Technical University of Catalonia, Spain
6 National Marine Mammal Foundation, USA
7 Hawaii Institute of Marine Biology & Oceanwide Science Institute, USA
8 Leigh Marine Laboratory University of Auckland, New Zealand
9 University of St. Andrews, UK
10 Biology Department, Woods Hole Oceanographic Institution, USA
This report can be referenced as:
Lucke, K., Popper, A.N., Hawkins, A.D., Akamatsu, T., André, M., Branstetter, B.K., Lammers, M., Radford, C.A., Stansbury, A.L. and Mooney, T.A. (2015). Report of the Sensitivity Session, Oceanoise2015, Vilanova i la Geltrú, Barcelona, Spain, 10-15 May. (Editors Michel André & Peter Sigray). Retrieved from http://oceanoise2015.com
Sensitivity for the purposes of this summary is defined as the capacity of response of an individual, or group of individuals, to sound stimuli or noise exposure, with those responses being behavioural, perceptual, physiological and/or anatomical. This is intentionally broad, and in the context of underwater sound and marine fauna, the term sensitivity covers a wide range of topics. First there is the hearing capacity of the animal, in terms of its ability to detect sounds. Second, the term sensitivity may also encompass the effects of underwater noise upon animals in terms of mortality or physical injury, impairment to hearing, or (when referring to behavioural sensitivity) any behavioural disturbance it might cause to animals in the aquatic environment. Here, threshold values or sound exposure criteria may specify those sound levels above which particular effects may potentially take place. The assessment end points are typically aimed at determining whether there is a significant impact on populations and on the wider ecosystem.
Over a century of auditory research in marine animals has produced audiograms for more than 30 of 129 (Perrin et al. 2009) species of marine mammals and just over 100 of more than 32,100 fish species. Only a very few species of invertebrates, perhaps the most diverse of these three marine taxa, have been tested for their sensitivity to sound.
In these three taxa, the respective challenges of conducting (auditory) research has resulted in species-defining audiograms being based on a few (or even one) representative individuals of a species, and generalizations to the sensitivities of all marine animal species (within the same taxon) being based on results from just a few species. This has resulted in a very limited understanding of species auditory diversity or the variation within species.
The vast majority of marine species sensitivities have yet to be defined, leaving great uncertainty regarding how well these species detect and respond to sound. The uncertainty regarding hearing and behavioural sensitivity resulting from such insufficient data is an important aspect in underwater sound-related research and management. While testing all species is unrealistic and unnecessary, the existing information deficit leaves open questions such as: How representative are results obtained from a small number of specimens representative of the whole species and what is the influence of size, age, season, motivation, etc. in these results; to what extent can results from one species be transferred extrapolated to other species within the same taxonomic group; and are there consistent trends/guidelines useable across taxonomic groups?
Masking, especially those of biologically relevant sound signals such as vocalisations and ambient soundscape, plays an important role in the context of sensitivity but is often overlooked in regulation of underwater noise. Masking studies using tonal sound may not provide a complete description of masking in the marine environment (Fay, 2010) as real-life signals are usually not sinusoidal and masking noise may not be Gaussian. Noise in the wild is much more complex, and effects such as co-modulation, spatial or temporal masking release can even lead to a reduction in hearing thresholds.
Some key objectives of future studies should include:
- How well do animals detect their overall acoustic environment in the presence of man-made sound?
- What is the potential of masking from repetitive man-made sounds (e.g. pile driving or seismic surveys)?
- What is the potential of masking from continuous man-made sounds (e.g. shipping, gas and oil platforms)?
- What are the relative masking effects of the different characteristics of man-made sound compared to that from white noise?
- Which cues are available and used by a species in an environment and which cues are masked if the noise level is increased?
In considering behavioural responses, and in addition to hearing sensitivity, contextual factors, including animal location, time of day, time of year, age of the animal, (and more) and their effect on sensitivity and reactions to sound also need to be taken into account, as well as the prior experience of the animal to the type of sound. Behavioural responses of individual animals depend on the internal state, motivation, and learned associations between sounds and external information. All of these affect whether the sound will have a deterrent, attractive or neutral effect on exposure and thus sensitivity. Such considerations should be taken into account for all taxonomic groups. However, this tends to provide an exceedingly high number of variables, many of which are often difficult to quantify.
Are we asking the right questions?
Throughout the conference, one question was repeatedly raised: “Are we asking the right questions”? The answer clearly depends on the aspect/research question that needs to be addressed. For example, a noise impact experiment investigating the schooling behaviour of fishes in response to noise (e.g., Hawkins et al., 2014) may have implications on fisheries, but the results are equally important with regard to conservation management. An important aspect in such experiments is, once again, to carry them out under appropriate acoustic conditions. The appropriate acoustic field conditions are essential (e.g., pressure, particle motion, substrate contributions) in order to achieve useful results.
Therefore, experiments should be conducted under natural acoustic conditions where the acoustic field conditions are those normally experienced by the animals (e.g., Hawkins et al., 2014). This is of special importance with regards to experiments involving fishes and probably other taxonomic groups that are sensitive to the particle motion component of sound and not always to sound pressure. If we do not measure the correct components of sound, the results can be misleading. Moreover, behavioural response experiments carried out on marine animals held in a tank do not necessarily reflect the full range of natural, wild behaviour and conclusions should not be extrapolated to other behaviours (Popper et al., 2014; Hawkins et al., 2015).
How to deal with long-term consequences?
Marine animals live in an environment which can vary substantially with regards to acoustic conditions, and, like animals in air, have adapted to living in these soundscapes and evolved to deal with their respective levels of background noise. The exact effects of sound on the stress level in marine animals and associated secondary effects (e.g. behavioural response, fecundity) are not well known. The exposure to increasing underwater noise levels due to man-made activities is clearly an issue of concern, but at the moment it is unknown how an increase in chronic background sound may affect aquatic animals. The key questions are at what levels are effects induced and at what levels do effects begin to become biologically significant. However, it is also evident that underwater sound and its effect on the marine fauna should not be assessed in isolation, but together with other stressors in the marine environment.
Possible ways ahead
How do we avoid being at the same level of understanding two decades from now? There is still a paucity of data for all taxonomic groups with regard to hearing sensitivity, behavioural responses to sound and ecological effects of sound exposure. In order to address the significance of the behaviour it is necessary to assess the importance of any observed changes in behaviour, such as how do the observed behaviour affect vital functions and what does that mean in terms of changes to populations. The currently popular approaches to address population effects within a risk assessment framework (PCAD and PCoD) are data hungry and can seldom be applied successfully to marine mammal, fish or invertebrate species of concern. Alternatively, individual-based models are used to predict what an animal might do when it is exposed to sound, but again the results are not widely applicable.
A ‘rough & ready’ approach that looks at the ecological level of effects of sound exposure and other stressors have on the marine fauna is needed. Looking at fisheries science there is another approach available, the Productivity/Susceptibility Analysis (PSA) (e.g. Patrick et al. (2014)). Susceptibility refers to the degree to which sound exposure can have an impact upon a stock or species. Fish species may show extreme differences in their susceptibility to (acoustic) disturbance. Overall, PSA can be used to compare the vulnerability of different stocks and species to sound exposure and appropriate mitigation procedures can be considered.
A number of questions crystallised from this discussion which seem to be most relevant for research on sensitivity in marine animals:
- How do we deal with the uncertainty resulting from species for which there are few data, limitations in research setup, and different life stages?
- Do we need to know the lowest hearing sensitivity of all marine animals or can measurements conducted in ambient noise be used to determine sensitivity?
- What are the masking effects of man-made sounds on marine animals?
- How do internal state, motivation, context and previous experience affect behavioural responses and should these be taken into account?
- How should long-term and cumulative effects to be taken into account in assessing the effect of underwater sound on marine animals?
- Can we adopt techniques from other disciplines to assess population level impacts which are better applicable to marine fauna?
- Fay, R.R. (2010). Signal-to-noise ratio for source determination and for a co-modulated masker in goldfish, Carassius auratus. Journal of the Acoustical Society of America, 129:3367-3372
- Hawkins, A.D., Roberts, L., & Cheesman, S. (2014). Responses of free-living coastal pelagic fish to impulsive sounds. J. Acoust. Soc. Am., 135(5):3101–3116; http://dx.doi.org/10.1121/1.4870697.
- Patrick, W.S., Spencer, P., Link, J., Cope, J., Field, J., Kobayashi, D., … & Overholtz, W. (2010). Using productivity and susceptibility indices to assess the vulnerability of United States fish stocks to overfishing. Fishery Bulletin 108(3):305-322.
- Perrin, W.F., Würsig, B., & Thewissen, J.G.M. (2009). Encyclopedia of marine mammals. Academic Press, Amsterdam.
- Popper, A.N., Hawkins, A.D., Fay, R.R., Mann, D., Bartol, S., Carlson, T., Coombs, S., Ellison, W.T., Gentry, R., Halvorsen, M.B., Løkkeborg, S., Rogers, P., Southall, B.L., Zeddies, D., & Tavolga, W.N. (2014). Sound Exposure Guidelines for Fishes and Sea Turtles: A Technical Report prepared by ANSI-Accredited Standards Committee S3/SC1 and registered with ANSI. ASA S3/SC1.4 TR-2014. Springer and ASA Press, Cham, Switzerland.
 PCAD: Population Consequences of Acoustic Disturbance (National Research Council 2005)
PCoD: Population Consequences of Disturbance (see King et al. 2015)