Auditory Evoked Potentials and Behavioral Considerations with Hearing Loss in Small Cetaceans: Application as a Standard Diagnostic Test in Health Assessment
Abstract
Odontocete cetaceans are auditory-based predators, with a large portion of their brain devoted to the auditory processing of echolocation signals.1 Hearing deficits in odontocetes potentially present a challenge to survival and reproduction in the wild due to compromises in the ability to find food, navigate, socialize, and evade predators. In 2010, Mann et al. demonstrated that as many as 57% of stranded common bottlenose dolphins (Tursiops truncatus) and 36% of stranded rough-toothed dolphins (Steno bredanensis) studied had hearing impairments.2 They described diagnosing hearing deficits as an essential component of stranded animal evaluations. In some cases of deafness in stranded cetaceans, it was observed that animals take longer to adapt to new environments and cohorts, swim less, and may be less or unresponsive to interaction with caretakers. Nevertheless, there is little published information regarding how odontocete behavior is affected following hearing loss, though it is expected that hearing deficits would influence an animal's response to its cohorts and environment.
The objectives of this study were to document age-related hearing deficits in odontocetes through auditory evoked potential (AEP) testing, and to evaluate whether individual behavior correlates with a diagnosis of hearing impairment. As with other species of mammals, the occurrence of presbycusis was hypothesized to increase in animals as they aged. All cetaceans (n = 26) evaluated received an AEP hearing test within the last 15 years; most (n = 15) were tested as part of this study. The study consisted of 17 Tursiops truncatus, 1 Atlantic spotted dolphin (Stenella frontalis), and 8 rough-toothed dolphins with ages between 2.5 and 54 years. Thirteen had originally stranded and 13 originated from the wild or within the collection. Behavioral questionnaires for participating animals (n = 21) were completed by individuals with extensive knowledge of the animal's history and behavior. Hearing loss was evaluated in comparison to normals for each species.3,4
Results indicated that 63% of stranded individuals with hearing loss (8 out of 13 individuals) exhibited behavior differences compared with other animals. These differences included taking longer times to learn new behaviors (6/8), to acclimate to new types of enrichment (3/8), and to acclimate to new environments (2/8). In individuals with profound hearing losses (n=6), they may display an increase in vocalizations in various situations (4/6).
Thirteen non-stranded individuals between 5.5 and 54 years of age were assessed for age-related hearing loss. All individuals tested over 35 years of age had some degree of hearing loss; however, the magnitude of the loss was not correlated with age. A decrease in responsiveness to whistle signals was observed in 66.6% of the participating individuals with hearing losses (n = 8).
As a result of these findings, the authors reinforce the recommendation for conducting AEP studies in all stranded individuals entering a rehabilitation environment. It is further recommended that all animals under human management be tested via AEP as part of their normal health assessment, with particular emphasis on aging individuals and animals that seem to learn slowly, appear to not respond to trainers, or show changes in vocalization.
Acknowledgments
The authors wish to thank Ms. Jane Hoppe of the International Fund for Animal Welfare, Ms. Adrienne Cardwell of Clearwater Marine Aquarium, Dr. Abraham Robinson of Mote Marine Laboratory, Drs. Andy Stamper and Wendi Fellner of Disney's The Living Seas, Dr. Eric Montie of the University of South Carolina, Dr. Craig Pelton of the University of Florida Aquatic Animal Health Program, and Ms. Sarah Orfanedes and Dr. Daniel Vanderhart for their support throughout this project. We also wish to thank the incredible staff at the Dolphin Research Center, SeaWorld Orlando, Gulf World Marine Park, Dolphins Plus, and Clearwater Marine Aquarium for their relentless efforts throughout testing and in submitting surveys. The authors thank the Aquatic Animal Health Program at the University of Florida, College of Veterinary Medicine (CVM) and the IAAAM Medway Award for financial support, and Dr. Jorge Hernandez at the University of Florida CVM for statistical advice and support.
* Presenting author
+ Student presenter
Literature Cited
1. Ketten DR. Marine mammal auditory systems: a summary of audiometric and anatomical data and implications for underwater acoustic impacts. Polarforshung. 2002;72(2–3):79–92.
2. Mann DA, Cook MLH, Manire CA, Greenhow D, Montie E, Powell J, Wells R, Bauer R, Cunningham-Smith P, Lingenfelser R, DiGiovanni Jr. R, Stone A, Brodsky M, Stevens R, Kieffer G, Hoetjes P. Hearing loss in stranded odontocete dolphins and whales. PLoS One. 2010;5(11):e13824.
3. Houser DS, Finneran JJ. Variation in the hearing sensitivity of a dolphin population obtained through the use of evoked potential audiometry. Journal of the Acoustical Society of America. 2006;120:4090–4099.
4. Cook MLH, Manire CA, Mann DA. Auditory evoked potential (AEP) measurements in stranded rough-toothed dolphins (Steno bredanensis). Journal of the Acoustical Society of America. 2005;117:2441.