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Marine mammal auditory research: Mischaracterization of published results
Marine Pollution Bulletin 58 (2009) 312–313
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Correspondence
Marine mammal auditory research: Mischaracterization of published results
Parsons et al. (2008) have mischaracterized results of controlled experiments and findings on small whales. What is known about hearing and echolocation of dolphins and other small whales has been primarily determined from studies in pools or bays where the background noise field was carefully assessed and hearing thresholds were measured in healthy animals (cf. Johnson, 1966; Au, 1993). The ‘anti-captivity’ bias expressed by Parsons et al. (2008) is not helpful in determining the facts about ocean sound pollution. Parsons et al. (2008) protest the use of temporary threshold shift (TTS) studies to understand ‘safe’ limits of sound exposure. However, TTS studies were called for by the first National Research Council report (1994) on ocean noise and marine mammals based on the fact that TTS has been a valuable criterion for setting noise standards in the human workplace. TTS measurements of marine mammals have been made with careful attention to the measurement and/ or control of background noise (Finneran et al., 2002, 2003, 2005a, 2007). Parsons et al. state that such physiological measurements are debatable as to their relevance to wild animals. To this end, they cite behavioral responses of animals in the wild 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, 2008). An example of the overreaching zeal of the authors to denigrate ‘captive animal’ research is found on page 1251 of the article when they say ‘‘It is possible that the high level of background noise in captive facilities led to hearing impairment (Finneran et al., 2005; Popov et al., 2007) and even deafness (Ridgway and Carder, 1997).” The one case of deafness discovered was from an animal that was mute – the first mute dolphin ever found. Given that this animal never produced whistles or echolocation pulses while in captivity, it probably suffered from an infection such as meningitis as a newborn in the wild (Ridgway and Carder, 1997). Although prolonged exposure to noise is linked to hearing loss, evidence from a large number of dolphins has demonstrated that hearing loss in dolphins is predominantly a function of age (presbycusis). Indeed, this pattern holds across facilities for which background noise is variable (Houser and Finneran, 2006; Houser et al., 2008; Finneran et al., 2008). As noted by Parsons et al., male dolphins tend to lose high-frequency hearing earlier than females living with them in the same facility, although in both instances the age at which high-frequency hearing loss typically begins is between 20 and 30 years of age. It is worth noting that the reference to Popov et al. (2007) fails to note that all of the animals tested in 0025-326X/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2008.09.011
that study of ‘normal’ dolphins were estimated to be less than 15 years of age, below which age-related hearing loss would not be expected. A high percentage of the human population (males more than females) shows hearing loss with age (Ries, 1982) and it should not be surprising that other mammals share this deficit. Although Parsons et al. have every right to speculate about how noise in captive facilities might impact marine mammals, the data to date do not support that conjecture that noise induced hearing loss in captive facilities is problematic. We have long been aware of the potential for certain antibiotics, especially with long term treatment with aminoglycosides, to cause hearing loss. However, we have been able to identify only one case with certainty (Finneran et al., 2005b). This animal was not employed in TTS studies to set ‘safe’ sound limits and neither were either of the animals found with profound hearing deficits by Houser and Finneran (2006). 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. Certainly, loud, human made sound in the ocean is a pollutant but small whales evolved in the oceans where natural sound sources such as volcanic activity, lightening strikes on the ocean, ice movements, and pounding surf, may be very loud as well. Effort needs to be focused on when and where human generated sound impacts marine mammals. Careful studies with trained mammals are an essential component of this focus along with observations of marine mammals in their varied ocean habitats. References Au, W.W.L., 1993. The Sonar of Dolphins. Springer-Verlag, New York. Branstetter, B.K., Finneran, J.J., 2008. Comodulation masking release in bottlenose dolphins (Tursiops truncatus). J. Acoust. Soc. Am. 124, 625–633. Finneran, J.J., Dear, R., Carder, D.A., Ridgway, S.H., 2003. Auditory and behavioral responses of California sea lions (Zalophus californianus) to single underwater impulses from an arc-gap transducer. J. Acoust. Soc. Am. 114, 1667–1677. Finneran, J.J., Carder, D.A., Schlundt, C.E., Ridgway, S.H., 2005a. Temporary threshold shift (TTS) in bottlenose dolphins (Tursiops truncatus) exposed to mid-frequency tones. J. Acoust. Soc. Am. 118, 2696–2705. Finneran, J.J., Carder, D.A., Dear, R., Belting, T., McBain, J., Dalton, L., Ridgway, S.H., 2005b. Pure tone audiograms and possible aminoglycoside-induced hearing loss in the belugas (Delphinapterus leucas). J. Acoust. Soc. Am. 117, 3936–3943. Finneran, J.J., Schlundt, C.E., Branstetter, B., Dear, R.L., 2007. Assessing temporary threshold shift in a bottlenose dolphin (Tursiops truncatus) using multiple simultaneous auditory evoked potentials. J. Acoust. Soc. Am. 122, 1249–1264. Finneran, J.J., Houser, D.S., Blasko, D., Hicks, C., Hudson, J., Osborn, M., 2008. Estimating bottlenose dolphin (Tursiops truncatus) hearing thresholds from single and multiple simultaneous auditory evoked potentials. J. Acoust. Soc. Am. 123, 542–551.
Correspondence / Marine Pollution Bulletin 58 (2009) 312–313 Houser, D.S., Gomez-Rubio, A., Finneran, J.J., 2008. Evoked potential audiometry of 13 Pacific bottlenose dolphins (Tursiops truncatus gilli). Mar. Mammal Sci. 24, 28–41. Houser, D.S., Finneran, J.J., 2006. Variation in the hearing sensitivity of a dolphin population obtained through the use of evoked potential audiometry. J. Acoust. Soc. Am. 120, 4090–4099. Johnson, C.S., 1966. US Naval Ordinance Test Station Reports. NOTS TP 4178. National Research Council, 1994. Low-Frequency Sound and Marine Mammals: Current Knowledge and Research Needs. National Academy Press, Washington, DC (75pp). Parsons, E.C.M., Dolman, S.J., 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? Mar. Pollut. Bull. 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). Aquat. Mam. 33, 24–33. Ridgway, S.H., Carder, D.A., 1997. Hearing deficits measured in some Tursiops truncatus, and discovery of a deaf/mute dolphin. J. Acoust. Soc. Am. 101, 590– 594. Ries, P.W., 1982. Hearing ability of persons by sociodemographic and health characteristics in the United States (Series 10, No. 140). National Center for Health Statistics, US Government Printing Office, Washington, DC.
313
Sam H. Ridgway Department of Pathology, School of Medicine, La Jolla, CA 92093, United States Dorian S. Houser Biomimetica, Santee, CA 92071, United States. Tel.: +1 619 7498657 E-mail address: [email protected]
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Correspondence
Marine mammal auditory research: Mischaracterization of published results
Parsons et al. (2008) have mischaracterized results of controlled experiments and findings on small whales. What is known about hearing and echolocation of dolphins and other small whales has been primarily determined from studies in pools or bays where the background noise field was carefully assessed and hearing thresholds were measured in healthy animals (cf. Johnson, 1966; Au, 1993). The ‘anti-captivity’ bias expressed by Parsons et al. (2008) is not helpful in determining the facts about ocean sound pollution. Parsons et al. (2008) protest the use of temporary threshold shift (TTS) studies to understand ‘safe’ limits of sound exposure. However, TTS studies were called for by the first National Research Council report (1994) on ocean noise and marine mammals based on the fact that TTS has been a valuable criterion for setting noise standards in the human workplace. TTS measurements of marine mammals have been made with careful attention to the measurement and/ or control of background noise (Finneran et al., 2002, 2003, 2005a, 2007). Parsons et al. state that such physiological measurements are debatable as to their relevance to wild animals. To this end, they cite behavioral responses of animals in the wild 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, 2008). An example of the overreaching zeal of the authors to denigrate ‘captive animal’ research is found on page 1251 of the article when they say ‘‘It is possible that the high level of background noise in captive facilities led to hearing impairment (Finneran et al., 2005; Popov et al., 2007) and even deafness (Ridgway and Carder, 1997).” The one case of deafness discovered was from an animal that was mute – the first mute dolphin ever found. Given that this animal never produced whistles or echolocation pulses while in captivity, it probably suffered from an infection such as meningitis as a newborn in the wild (Ridgway and Carder, 1997). Although prolonged exposure to noise is linked to hearing loss, evidence from a large number of dolphins has demonstrated that hearing loss in dolphins is predominantly a function of age (presbycusis). Indeed, this pattern holds across facilities for which background noise is variable (Houser and Finneran, 2006; Houser et al., 2008; Finneran et al., 2008). As noted by Parsons et al., male dolphins tend to lose high-frequency hearing earlier than females living with them in the same facility, although in both instances the age at which high-frequency hearing loss typically begins is between 20 and 30 years of age. It is worth noting that the reference to Popov et al. (2007) fails to note that all of the animals tested in 0025-326X/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2008.09.011
that study of ‘normal’ dolphins were estimated to be less than 15 years of age, below which age-related hearing loss would not be expected. A high percentage of the human population (males more than females) shows hearing loss with age (Ries, 1982) and it should not be surprising that other mammals share this deficit. Although Parsons et al. have every right to speculate about how noise in captive facilities might impact marine mammals, the data to date do not support that conjecture that noise induced hearing loss in captive facilities is problematic. We have long been aware of the potential for certain antibiotics, especially with long term treatment with aminoglycosides, to cause hearing loss. However, we have been able to identify only one case with certainty (Finneran et al., 2005b). This animal was not employed in TTS studies to set ‘safe’ sound limits and neither were either of the animals found with profound hearing deficits by Houser and Finneran (2006). 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. Certainly, loud, human made sound in the ocean is a pollutant but small whales evolved in the oceans where natural sound sources such as volcanic activity, lightening strikes on the ocean, ice movements, and pounding surf, may be very loud as well. Effort needs to be focused on when and where human generated sound impacts marine mammals. Careful studies with trained mammals are an essential component of this focus along with observations of marine mammals in their varied ocean habitats. References Au, W.W.L., 1993. The Sonar of Dolphins. Springer-Verlag, New York. Branstetter, B.K., Finneran, J.J., 2008. Comodulation masking release in bottlenose dolphins (Tursiops truncatus). J. Acoust. Soc. Am. 124, 625–633. Finneran, J.J., Dear, R., Carder, D.A., Ridgway, S.H., 2003. Auditory and behavioral responses of California sea lions (Zalophus californianus) to single underwater impulses from an arc-gap transducer. J. Acoust. Soc. Am. 114, 1667–1677. Finneran, J.J., Carder, D.A., Schlundt, C.E., Ridgway, S.H., 2005a. Temporary threshold shift (TTS) in bottlenose dolphins (Tursiops truncatus) exposed to mid-frequency tones. J. Acoust. Soc. Am. 118, 2696–2705. Finneran, J.J., Carder, D.A., Dear, R., Belting, T., McBain, J., Dalton, L., Ridgway, S.H., 2005b. Pure tone audiograms and possible aminoglycoside-induced hearing loss in the belugas (Delphinapterus leucas). J. Acoust. Soc. Am. 117, 3936–3943. Finneran, J.J., Schlundt, C.E., Branstetter, B., Dear, R.L., 2007. Assessing temporary threshold shift in a bottlenose dolphin (Tursiops truncatus) using multiple simultaneous auditory evoked potentials. J. Acoust. Soc. Am. 122, 1249–1264. Finneran, J.J., Houser, D.S., Blasko, D., Hicks, C., Hudson, J., Osborn, M., 2008. Estimating bottlenose dolphin (Tursiops truncatus) hearing thresholds from single and multiple simultaneous auditory evoked potentials. J. Acoust. Soc. Am. 123, 542–551.
Correspondence / Marine Pollution Bulletin 58 (2009) 312–313 Houser, D.S., Gomez-Rubio, A., Finneran, J.J., 2008. Evoked potential audiometry of 13 Pacific bottlenose dolphins (Tursiops truncatus gilli). Mar. Mammal Sci. 24, 28–41. Houser, D.S., Finneran, J.J., 2006. Variation in the hearing sensitivity of a dolphin population obtained through the use of evoked potential audiometry. J. Acoust. Soc. Am. 120, 4090–4099. Johnson, C.S., 1966. US Naval Ordinance Test Station Reports. NOTS TP 4178. National Research Council, 1994. Low-Frequency Sound and Marine Mammals: Current Knowledge and Research Needs. National Academy Press, Washington, DC (75pp). Parsons, E.C.M., Dolman, S.J., 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? Mar. Pollut. Bull. 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). Aquat. Mam. 33, 24–33. Ridgway, S.H., Carder, D.A., 1997. Hearing deficits measured in some Tursiops truncatus, and discovery of a deaf/mute dolphin. J. Acoust. Soc. Am. 101, 590– 594. Ries, P.W., 1982. Hearing ability of persons by sociodemographic and health characteristics in the United States (Series 10, No. 140). National Center for Health Statistics, US Government Printing Office, Washington, DC.
313
Sam H. Ridgway Department of Pathology, School of Medicine, La Jolla, CA 92093, United States Dorian S. Houser Biomimetica, Santee, CA 92071, United States. Tel.: +1 619 7498657 E-mail address: [email protected]