Urging cautious policy applications of captive research data is not the same as rejecting those data

Marine Pollution Bulletin 58 (2009) 314–316

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Correspondence

Urging cautious policy applications of captive research data is not the same as rejecting those data We welcome the opportunity to debate the controversial issues surrounding the impacts of anthropogenic noise on marine mammals. Ridgway and Houser (2008) chose to focus on and criticize what was really a minor component of our paper’s overall argument, which was that the weight of scientific evidence from all sources merits a reconsideration of mitigation measures for, and more limitations on, naval exercises in order to adequately protect marine mammals (Parsons et al., 2008). We believe that, regardless of their criticisms, this overall point remains unassailable, as we offered support for the position from a variety of sources. We also believe that they over-interpreted at best, and misunderstood at worst, our points regarding data gained from captive animal studies. We disagree that our arguments expressed an ‘‘‘anti-captivity’ bias” – indeed, the tone of Ridgway and Houser (2008) suggests the reverse; that the authors have a ‘‘pro-captivity” bias. Our goal with the discussion on captive animal studies in Parsons et al. (2008) was not to ‘‘protest the use of temporary threshold shift (TTS) studies to understand ‘safe’ limits of sound exposure” (Ridgway and Houser, 2008). We did not advocate throwing the baby out with the bathwater because of an alleged ‘‘anti-captivity bias.” Our goal was to express the need for a precautionary approach in using this research to establish safe noise exposure standards in policy frameworks; a very different objective than opposing the research itself. We do not dispute that much of what is known about hearing and echolocation in dolphins and other small whales has been obtained through work with captive animals. However, our paper contended that, while these studies represent some of the best available science at this time, they have inherent limitations that raise concerns with directly (and at times exclusively) applying the results to management action. A case in point – Ridgway and Houser (2008) offered our statement that ‘‘[i]t is possible that the high level of background noise in captive facilities led to hearing impairment (Finneran et al., 2005a; Popov et al., 2007) and even deafness (Ridgway and Carder, 1997)” as an example of the ‘‘overreaching zeal of the authors to denigrate ‘captive animal’ research.” The key phrase in our text was that ‘‘it is possible.” Again, a desire for precaution is not rejection or opposition. We do not dispute that the one case of deafness discovered was from a mute dolphin, although we maintain that the argument by Ridgway and Carder (1997) that the deaf-mute condition was probably a result of an infection, while reasonable, is hardly the only possibility. We also accept that presbycusis (hearing loss with age) is a primary factor in hearing loss across a variety of facilities with different noise profiles (Ridgway and Houser, 2008) – Parsons et al. (2008) indeed acknowledged the role of presbycusis in hearing loss. However, we cited Popov et al. (2007) because they noted 0025-326X/$ - see front matter Ó 2008 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2008.12.004

that, ‘‘in regards to hearing loss, there was a significant difference between the long-kept captive animals. . .and the briefly kept animals” (p. 31). They went on to suggest that one reason may be that ‘‘significant hearing loss in captive populations was associated with some condition of being kept in captivity (e.g., the diet, medical treatment, etc.)” (p. 31, Popov et al., 2007). Thus, we were simply exercising our ‘‘right to speculate about how noise in captive facilities might impact marine mammals” (Ridgway and Houser, 2008) and expressing concern over the direct and at times exclusive application of captive study results to management actions and standards. Ridgway and Houser (2008) made similar arguments about antibiotic-related hearing loss, noting that only one case has been identified with certainty (Finneran et al., 2005a) and that this ‘‘animal was not employed in TTS studies to set ‘safe’ sound limits.” We concede their point that the ‘‘process of screening marine mammals for hearing sensitivity prior to psychophysical testing is now routine at established laboratories and there is little chance that marine mammals participating in auditory studies at these facilities have unknown or unquantified hearing deficits.” However, we can be sure that not all results in the literature used to date to establish safe exposure standards arose after such screening. Likewise, the definition of ‘‘normal” hearing is wide enough in most if not all marine mammals that limited impairment could pass unnoticed through this screening process. Again, we are not criticizing the work itself, as it clearly represents the best efforts possible at this time or when it was undertaken. We are simply noting possible (and at times probable) limitations and suggesting that the application of the research’s results to management actions and standards should be done conservatively and with precaution, which we contend is not presently the case. At this time, we would like to note that Ridgway and Houser (2008) made little attempt to refute our additional points on work to determine impacts of noise exposure on marine mammals through behavioral observations of captive animals. We feel that this demonstrates a bias toward their own research methodology involving auditory evoked potentials (AEP). Their single mention of behavioral responses was used to argue against our position that such studies on captive animals are subject to additional inherent limitations, thus raising further concern with their direct application to management of wild animals. They suggested that we expressed these concerns ‘‘seemingly unaware of the differences between the manifestation of auditory fatigue and the psychophysics of signal detection. Even with respect to signal detection, laboratory work is uncovering reasons as to why detection capabilities are greater than might be expected based on threshold measurements alone (Branstetter and Finneran,

Correspondence / Marine Pollution Bulletin 58 (2009) 314–316

2008)” (Ridgway and Houser, 2008). While it is legitimate to note that new work is emerging that addresses one of our concerns, it is unreasonable to expect us to be aware of work that had not yet been published at the time we were drafting our original paper. However, we are aware of research in these areas in general and maintain that the reasons for the differences observed are not as important from a management perspective as the differences themselves. Our point was that behavioral responses in the wild are seen at exposure levels well below those inducing behavioral responses or TTS in captive animals. Consequently, as we do not yet know the extent of the impact to the animals responding at these greater distances, and are just beginning to understand that there may also be impacts for those not responding at all (see Beale and Monaghan, 2004; Beale, 2007), we maintain our position that applying results of captive studies involving behavioral responses directly to the management of wild populations is inadvisable at present – or at least must be done in a very conservative manner. It is simply common sense that the behavioral responses of a relatively small number of trained, conditioned, habituated and probably acclimated marine mammals in an artificial setting are unlikely to mirror the responses of diverse populations of naïve animals in nature. We are not the only ones to express such concerns; for example, Nowacek et al. (2007) commented on hearing sensitivity tests conducted on captive dolphins by Finneran et al. (2000): ‘‘These trained animals were tested in a context where they were being rewarded for tolerating high levels of noise. Given this training, it is likely that behavioural disruption would likely [sic] be observed at lower levels in other contexts” (p. 91). They also commented on Finneran et al. (2005b): ‘‘. . .an animal failing to return to the experimental station for additional exposures is usually ‘punished’ in some way, which can certainly affect the level(s) it is willing to withstand. A study designed to measure behavioural thresholds would follow a different paradigm than one intended to investigate the physiological limits of the auditory system” (p. 106–107). Ridgway is a co-author of both the Finneran et al. papers. The need for conservative interpretation of captive animal data by scientists should be evident. One would, after all, be conservative when extrapolating the behavioral responses of trained riding horses to the behavior of free-ranging mustangs when making policy decisions for the management of the latter animals. We would also like to point out that, after the discussion of this matter in our paper, we noted that ‘‘[m]any problems inherent with acoustic-related behavioral response studies have. . .been largely removed by recent use of auditory evoked potentials (AEP) to estimate marine mammal hearing abilities” (Parsons et al., 2008). The above discussion relates to the use of TTS to establish safe sound exposure limits. Ridgway and Houser (2008) argued that the use of TTS to establish safe sound exposure limits is appropriate, as it was called for by the National Research Council (NRC) in its 1994 report. However, we should bear in mind that this report was produced a decade and a half ago and that our understanding of the effects of sound on cetaceans has changed considerably. In particular, as stated in Parsons et al. (2008), it is likely that stranding events that lead to beaked whale mortality occur at exposure levels well below those at which TTS occurs, probably due to changes in whale diving behavior rather than acoustic damage (see Cox et al., 2006, of which Houser is a co-author, for a substantive discussion on behavioral changes that could lead to pathology and mortality in beaked whales as the result of exposure to anthropogenic sound; cf. Tyack et al., 2006). Ridgway and Houser (2008) also noted that TTS has been valuable for setting noise standards in the human workplace. However, we argued that some quite major impacts can result from repeated or prolonged exposure at levels that are too low to induce TTS and that this should be considered. Returning to the human analogy,

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we offer that the World Health Organization (WHO) Centre for Environment and Health recently convened a workshop to examine the evidence for the effects of aircraft noise exposure on physical and mental health, which concluded that ‘‘there is good evidence for exposure–response associations between aircraft noise and annoyance, sleep disturbance, high blood pressure, and children’s cognitive impairment” (Berglund et al., 2008).1 One specific example clearly demonstrates that impaired reading comprehension and recognition memory in children is linked to aircraft noise at exposure levels considerably less than 75 dB2 (Stansfeld et al., 2005), which, according to the US National Institute on Deafness and Other Communication Disorders (NIDCD), are unlikely to cause hearing loss (temporary or otherwise) even after long exposure (NIDCD, 2007). We contend that similar impacts could place additional (cumulative or synergistic) burdens on animal populations that are already declining due to other threats and may even threaten stable populations. Furthermore, we note that our understanding of conditions relating to chronic stress in humans has advanced considerably over recent years (e.g., Segerstrom and Miller, 2004) and the implications of this new understanding for marine mammals are not encouraging (e.g., Wright et al., 2007a,b). Regarding the last point Ridgway and Houser (2008) made, that the ocean is naturally a noisy place, we believe (and have consistently maintained in other forums) that it is invalid to compare anthropogenic sound to natural sound sources. It is certainly true that marine mammals are likely to have adapted over evolutionary time scales to some commonly encountered loud natural sound sources; however, they are unlikely to be similarly adapted to the relatively recent addition of anthropogenic noise (Dolman et al., 2007). At best, exposure to additional anthropogenic noise would require the activation of these coping mechanisms much more frequently than is natural, which could have unknown consequences for those exposed. (Consider that the stress response is adaptive, but over-activation of the stress response – chronic stress – is maladaptive.) However, animals, especially long-lived species such as most marine mammals, are probably unable to adapt at a pace similar to that of habitat change (Rabin and Greene, 2002). While some natural and anthropogenic sound sources share some acoustic characteristics, there is no evidence that marine mammals cannot detect the difference, especially regarding factors such as the context in which they occur (Dolman et al., 2007). We agree that focus should be on ‘‘when and where human generated sound impacts marine mammals” (Ridgway and Houser, 2008), but the central point in Parsons et al. (2008) was that there is much uncertainty on this issue and that we believe, given this uncertainty, the current application of available data to management is neither sufficiently precautionary nor conservative. In summary, we believe that data about the impacts of noise on marine mammals gained through research using captive animals can and should be considered by managers, but in Parsons et al. (2008) we advised that this consideration should be precautionary, especially with captive research involving behavioral responses. With all due respect, we see Ridgway and Houser (2008) offering a rebuttal in search of an argument. We believe that conservative application of such results is not only scientifically appropriate, but also appropriate under law in many countries (such as the United States), given the uncertainty introduced by observations in the wild and the potential for impacts at lower levels of exposure than indicated as ‘‘safe” in captive

1 WHO was to include this and other findings on the consequences of noise exposure for human health in a report that was scheduled to be published at the end of 2007 as part of its ‘‘Burden of Disease” project. However, the report has yet to be released. 2 It should be noted that this is an in-air sound measurement, which is not directly comparable to underwater levels.

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studies. We never ‘‘denigrated” captive research results, so the apparent basis for Ridgway and Houser (2008) does not exist. Finally, we would like to express our gratitude to Ridgway and Houser (2008) for acknowledging that (loud) anthropogenic sound in the ocean can be categorized as pollution – a long-standing semantic argument in this field. Debate should be welcome in science and an open, collegial discussion of how managers apply scientific results to policy decisions should be a standard feature of conservation biology (and a standard practice of conservation biologists). Unfortunately, in the debate over impacts of anthropogenic noise on marine mammals, this seems to have been forgotten by many members of the marine acoustics research community, whose reaction to criticism not of their work but of how it is applied to management has far too often missed this point and been automatically defensive. It is this defensive reaction that ‘‘is not helpful in determining the facts about ocean sound pollution” (Ridgway and Houser, 2008). References Beale, C.M., 2007. The behavioral ecology of disturbance responses. International Journal of Comparative Psychology 20, 111–120. Beale, C.M., Monaghan, P., 2004. Behavioral responses to human disturbance. A matter of choice. Animal Behavior 68, 1065–1069. Berglund, B., Stansfeld, S., & Kim, R. 2008. Overview of the World Health Organization workshop on aircraft noise and health. In: Proceedings of the 9th International Congress on Noise as a Public Health Problem (ICBEN) 21–25 July 2008. Connecticut, USA, ISBN: 978-3-9308342-4-7, 8pp. Branstetter, B.K., Finneran, J.J., 2008. Comodulation masking release in bottlenose dolphins (Tursiops truncatus). Journal of the Acoustical Society of America 124, 625–633. Cox, T.M., Ragen, T.J., Read, A.J., Vos, E., Baird, R.W., Balcomb, K., Barlow, J., Caldwell, J., Cranford, T., Crum, L., D’Amico, A., D’Spain, G., Fernandez, A., Finneran, J., Gentry, R., Gerth, W., Gulland, F., Hildebrand, J., Houser, D., Hullar, T., Jepson, P.D., Ketten, D., MacLeod, C.D., Miller, P., Moore, S., Mountain, D.C., Palka, D., Ponganis, P., Rommel, S., Rowles, T., Taylor, B., Tyack, P., Wartzok, D., Gisiner, R., Mead, J., Benner, L., 2006. Understanding the impacts of acoustic sound on beaked whales. Journal of Cetacean Research and Management 7, 177–187. Dolman, S., Green, M., Heskett, E., Reynolds, J., & Rose, N. 2007. Environmental Caucus Statement for the Report of the Advisory Committee on Acoustic Impacts on Marine Mammals to the Marine Mammal Commission, in Marine Mammals and Noise: A Sound Approach to Research and Management. A report to Congress from the Marine Mammal Commission, March 2007. Finneran, J.J., Schlundt, C.E., Carder, D.A., Clark, J.A., Young, J.A., Gaspin, J.B., Ridgway, S.H., 2000. Auditory and behavioral responses of bottlenose dolphins (Tursiops truncatus) and a beluga whale (Delphinapterus leucas) to impulsive sounds resembling distant signatures of underwater explosions. Journal of the Acoustical Society of America 108, 417–443. Finneran, J.J., Carder, D.A., Dear, R., Belting, T., McBain, J., Dalton, L., Ridgway, S.H., 2005a. Pure tone audiograms and possible aminoglycoside-induced hearing loss in belugas (Delphinapterus leucas). Journal of the Acoustical Society of America 117, 3936–3943. Finneran, J.J., Carder, D.A., Schlundt, C.E., Ridgway, S.H., 2005b. Temporary threshold shift in bottlenose dolphins (Tursiops truncatus) exposed to mid-frequency tones. Journal of the Acoustical Society of America 118, 2696–2705. NIDCD. 2007. NIDCD Fact Sheet: Noise-Induced Hearing Loss. NIH Publication No. 97–4233, Updated April 2007. NIDCD Information Clearinghouse, Bethesda, Maryland, 20892–3456. 4pp. Available from: . Nowacek, D.P., Thorne, L.H., Johnston, D.W., Tyack, P., 2007. Responses of cetaceans to anthropogenic noise. Mammal Review 37, 81–115. Parsons, E.C.M., Dolman, S., Wright, A.J., Rose, N.A., Burns, W.C.G., 2008. Navy sonar and cetaceans: just how much does the gun need to smoke before we act? Marine Pollution Bulletin 56, 1248–1257. Popov, V.V., Supin, A.Y., Pletenko, M.G., Tarakanov, M.B., Klishin, V.O., Bulgakova, T.N., Rosanova, E.I., 2007. Audiogram variability in normal bottlenose dolphins (Tursiops truncatus). Aquatic Mammals 33, 24–33. Rabin, L.A., Greene, C.M., 2002. Changes in acoustic communication systems in human-altered environments. Journal of Comparative Psychology 116, 137– 141.

Ridgway, S.H., Carder, D.A., 1997. Hearing deficits measured in some Tursiops truncatus, and discovery of a deaf/mute dolphin. Journal of the Acoustical Society of America 101, 590–594. Ridgway, S.H., Houser, D.S., 2009. Marine mammal auditory research: mischaracterization of published results. Marine Pollution Bulletin 58 (2), 313–314. Segerstrom, S.C., Miller, G.E., 2004. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychological Bulletin 130, 601–630. Stansfeld, S.A., Berglund, B., Clark, C., Lopez-Barrio, I., Fischer, P., Öhrström, E., Haines, M.M., Head, J., Hygge, S., van Kamp, I., Berry, B.F., 2005. Aircraft and road traffic noise and children’s cognition and health: a cross-national study. The Lancet 365 (June 4), 1942–1949. Tyack, P.L., Johnson, M., Aguilar Soto, N., Sturlese, A., Madsen, P.T., 2006. Extreme diving of beaked whales. Journal of Experimental Biology 209, 4238–4253. Wright, A.J., Aguilar Soto, N., Baldwin, A.L., Bateson, M., Beale, C.M., Clark, C., Deak, T., Edwards, E.F., Fernández, A., Godinho, A., Hatch, L., Kakuschke, A., Lusseau, D., Martineau, D., Romero, L.M., Weilgart, L., Wintle, B., Notarbartolo di Sciara, G., Martin, V., 2007a. Anthropogenic noise as a stressor in animals: a multidisciplinary perspective. International Journal of Comparative Psychology 20, 250–273. Wright, A.J., Aguilar Soto, N., Baldwin, A.L., Bateson, M., Beale, C.M., Clark, C., Deak, T., Edwards, E.F., Fernández, A., Godinho, A., Hatch, L., Kakuschke, A., Lusseau, D., Martineau, D., Romero, L.M., Weilgart, L., Wintle, B., Notarbartolo di Sciara, G., Martin, V., 2007b. Do marine mammals experience stress related to anthropogenic noise? International Journal of Comparative Psychology 20, 274–316.

Andrew J. Wright Leviathan Sciences, 3414 17th St N,# 3, Arlington, Virginia, 22207, USA E-mail address: [email protected] Naomi A. Rose Humane Society International, 2100 L Street, NW, Washington DC, USA E.C.M. Parsons 3 Department of Environmental Science and Policy, George Mason University, 4400 University Drive, Fairfax, Virginia 22030, USA University Marine Biological Station Millport (University of London), Cumbrae, KA28 0EG, UK

Sarah J. Dolman Whale and Dolphin Conservation Society, Brookfield House, 38 St Paul St, Chippenham, Wiltshire, SN15 1LJ, UK School of Biological Sciences, Zoology Building, Tillydrone Avenue, University of Aberdeen, Aberdeen AB24 2TZ, Scotland

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E.C.M Parsons is Research Associate with the National Zoo’s Conservation Research Center, Front Royal, Virginia, USA.