Author Posting. © The Author(s), 2016.  This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution.  The definitive version was published in "The Effects of Noise on Aquatic Life II," edited by Arthur N. Popper, Anthony Hawkins, 729-735. New York, NY: Springer, 2016. doi: 10.1007/978-1-4939-2981-8_88.We measured the hearing abilities of seven wild beluga whales (Delphinapterus leucas)
during a collection-and-release experiment in Bristol Bay, AK, USA. Here we summarize the
methods and initial data from one animal, discussing the implications of this experiment.
Audiograms were collected from 4-150 kHz. The animal with the lowest threshold heard best
at 80 kHz and demonstrated overall good hearing from 22-110 kHz. The robustness of the
methodology and data suggest AEP audiograms can be incorporated into future collection-and-release health assessments. Such methods may provide high-quality results for multiple
animals facilitating population-level audiograms and hearing measures in new species.Project funding and field support provided by Georgia Aquarium and the National Marine
Mammal Laboratory of the Alaska Fisheries Science Center (NMML/AFSC). Field work also
supported by National Marine Fisheries Service Alaska Regional Office (NMFS AKR),
WHOI Arctic Research Initiative, WHOI Ocean Life Institute, U.S. Fish and Wildlife
Service, Bristol Bay Native Association, Alaska SeaLife Center, Shedd Aquarium and Mystic
Aquarium. Audiogram analyses were funded by the Office of Naval Research award number
N000141210203 (from Michael Weise)

AF Pacini

C Gervaise

D Titley

JJ Finneran

M Castellote

M Wang

MLH Cook

National Academy of Sciences

NMFS

PE Nachtigall

RC Ferrero

SE Moore

TA Mooney

Mooney, T. Aran

Castellote, Manuel

Quakenbush, Lori T.

Hobbs, Roderick

Goertz, Caroline

Gaglione, Eric

Woods Hole Open Access Server

1		 Measuring hearing in wild beluga whales  1	 2	T. Aran Mooney1*, Manuel Castellote2,3*, Lori Quakenbush4, Roderick Hobbs2, Caroline 3	Goertz5, Eric Gaglione6  4	 5	1Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, 6	USA 7	2National Marine Mammal Laboratory, Alaska Fisheries Science Center, National Marine 8	Fisheries Service, Seattle, WA 98115 9	3North Gulf Oceanic Society, Homer, AK 99603, USA. 10	4Alaska Department of Fish and Game, 1300 College Road, Fairbanks, AK. 99701, USA 11	5Alaska SeaLife Center, Seward, AK 99664, USA 12	6Georgia Aquarium, 225 Baker St NW, Atlanta, GA 30313, USA 13	 14	*These authors contributed equally to this work 15	 16	Emails: amooney@whoi.edu, manuel.castellote@noaa.gov, lori.quakenbush@alaska.gov, 17	rod.hobbs@noaa.gov, egaglione@georgiaaquarium.org 18	 19	Corresponding author: T. Aran Mooney, WHOI, 266 Woods Hole Rd, MRF MS# 50, Woods 20	Hole, MA 02543, USA; amooney@whoi.edu 21	 22	Key words: anthropogenic noise, sensory, marine mammal, cetacean, odontocete, arctic 23	 24	 25	2		Abstract 1	We measured the hearing abilities of seven wild beluga whales (Delphinapterus leucas) 2	during a collection-and-release experiment in Bristol Bay, AK, USA. Here we summarize the 3	methods and initial data from one animal, discussing the implications of this experiment. 4	Audiograms were collected from 4-150 kHz. The animal with the lowest threshold heard best 5	at 80 kHz and demonstrated overall good hearing from 22-110 kHz.  The robustness of the 6	methodology and data suggest AEP audiograms can be incorporated into future collection-7	and-release health assessments.  Such methods may provide high-quality results for multiple 8	animals facilitating population-level audiograms and hearing measures in new species.  9	1. Introduction 10	Hearing is the primary sensory modality for odontocete marine mammals.  They are 11	generally considered to have sensitive hearing and may detect a broad range of frequencies.  12	Relying on hearing can be particularly adaptive in the marine environment where light and 13	other cues are often limited and natural sounds are frequently abundant.  Yet, these sensitive 14	auditory abilities may also be easily impacted by anthropogenic noise.  15	Human use of the Earth’s oceans has steadily increased over the last century resulting in 16	an increase in anthropogenically produced noise (e.g., National Academy of Sciences 2003).  17	The Arctic is no exception to this increase (Blackwell & Greene 2003). Reductions of polar sea 18	ice and the opening of the Northwest Passage presumably will open up habitat for many top 19	predators. Yet, this decrease in sea ice provides greater human access to high latitude 20	environment and such a change poised to transform a relatively pristine environment into to 21	one saturated with human activities and associated noise.  Sources are varied and include: naval 22	exercises, boundary definitions, shipping/movement along Alaska's North Slope, seismic 23	resources exploration, and the construction of infrastructure needed to support it (Wang & 24	Overland 2009;  Titley & St. John 2010). These changes encompass habitats of Delphinapterus 25	3		leucas (beluga whales) and other top predators. Despite this obvious overlap of human-natural 1	interests, there is a poor understanding of influences of these sound-associated changes.   In 2	order to estimate the impacts of this noise it is crucial to evaluate the natural hearing abilities 3	and the variation with marine mammal populations.  4	Yet a primary challenge is that audiograms of odontocetes marine mammals have most 5	often been estimated from stranded animals or non-wild individuals (for a review see Mooney 6	et al. 2012).  In many instances, these records have produced valuable data that is otherwise 7	unavailable.  For example, hearing in several stranded beaked whale species have helped define 8	what these sound-sensitive animals hear (Finneran et al. 2009;  Pacini et al. 2011).  The 9	audiogram of a stranded infant Risso’s dolphin helped redefine what the species actually 10	detects (Nachtigall et al. 2005).  Work with trained odontocetes provides scientific data that is 11	likely unique to those settings and can address how animals hear or how they may be protected 12	from anthropogenic noise (Nachtigall & Supin 2008).  Yet, in many instances health 13	compromised, stranded animals may not have normal auditory abilities, thus not necessarily 14	representative of wild populations. Further, without baselines to wild individuals it is difficult 15	to put differences and results of non-wild individuals in a relative context.   Clearly, there is 16	value in increasing the number of animals within a species measured for hearing capabilities 17	whenever possible.  18	Here we describe methods and initial results for the measuring the hearing of wild D. 19	leucas (Castellote et al. 2013).  The goal of this study was to determine hearing sensitivity in 20	wild Bristol Bay D. leucas, during a planned collection-and-release operation.  Monitoring of 21	D. leucas has been recommended in recent years because this species is likely to be 22	negatively impacted by climate change, but also because such a broadly dispersed, high 23	trophic feeder can serve as an effective sentinel of the ecosystem(s) in which they live 24	4		(Moore 2008;  Moore & Huntington 2008;  Simpkins et al. 2009). Because noise may impact 1	D. leucas in a variety of ways, it is essential to determine what these animals hear.  2	In view of the expected changes in the Arctic acoustic environment, expanding our 3	knowledge on D. leucas hearing is of central importance for an appropriate conservation 4	management framework. One of the five distinct stocks of D. leucas whales that are currently 5	recognized in U.S. waters, the Cook Inlet D. leucas population, is endangered and efforts for 6	its recovery to date have not been successful. The impact of anthropogenic noise has been 7	identified as a serious threat potentially impeding its recovery (NMFS 2008). On the 8	contrary, the Bristol Bay D. leucas  population is increasing and is considered to be a healthy 9	population (NMFS 2008). The acoustic environment in Bristol Bay is different; many of the 10	chronic anthropogenic sources typically found in Cook Inlet D. leucas habitat are essentially 11	absent or seasonally present at lower intensities in Bristol Bay habitat. This suggests that 12	Bristol Bay D. leucas are a valuable asset to evaluate baseline hearing and health measures 13	for comparison to effected populations, such as Cook Inlet D. leucas. 14	 15	2. Temporary collection of beluga whales and hearing tests methods 16	 This study was conducted in September, 2012 in Bristol Bay AK, USA. The 17	audiograms were measured during an overall health assessment study that required the 18	collection-and-release of D. leucas.  Audiograms were obtained on seven of seven belugas 19	tested. The procedures were similar to those followed by (Ferrero et al. 2000) and were 20	conducted under National Marine Fisheries Service marine mammal research permit #14245 21	and approved by the necessary Institutional Animal Care and Use Committees. The full 22	results are to be published elsewhere (Castellote et al. 2013); here we provide a summary of 23	the methods and preliminary results.  24	5		 Bristol Bay is a generally shallow, muddy-bottomed estuary system that supports a 1	population of D. leucas.  Using three 3.5 m aluminum skiffs and one soft-bodied inflatable 2	boat, we would search for an adult beluga. When a suitable animal was spotted (Fig. 1), one 3	of the skiffs would follow and gradually approach the whale to encourage it to swim into 4	shallow water (< 2 m).  From one of the boats, a 125 m long by 4 m deep net, of 0.3 m 5	braided square mesh, was deployed around the whale. Once the deployment boat and net 6	encircled the whale the inflatable boat approached the outside of the net and three handlers 7	placed a soft tail-rope around the whale’s peduncle. The rope’s other end was fixed to the 8	inflatable boat to secure the whale.   The large net was gradually recalled while a “belly-9	band” stretcher was placed under the D. leucas. Handholds in this stretcher facilitated 10	adjusting the whale’s position as the water depth changed with the tide.  The animal was then 11	positioned parallel to the small inflatable boat. The D. leucas’s head was typically rested on 12	or just above the soft mud bottom, keeping the lower jaw and primary hearing pathways 13	below the water surface. The animal’s blowhole was generally above the surface. This setup 14	was consistent for all animals, except one for which the water level was too low and this test 15	was conducted partly out of the water. Animals were maintained in this position for the 16	audiogram and health exam. The AEP test equipment was outfitted in a ruggedized case; both 17	it and the operator sat in the small inflatable boat beside the D. leucas during the hearing tests 18	(Fig. 1).   19	  20	3. Discussion of results 21	 Audiograms were successfully collected on all seven adult D. leucas whales 22	temporarily collected and tested.  Evoked response waveforms and envelope following 23	responses were generally easily identifiable and distinct from the background 24	electrophysiological noise. The inset in Figure 2 shows an EFR that was recorded using 25	6		stimuli ca. 20 dB about the hearing threshold at 32 kHz. Such a measurement would take ca. 1	30 sec to collect. Thus, overall thresholds at a particular frequency were obtained in 3-5 min. 2	This relatively rapid threshold measurement facilitated collecting multiple thresholds per 3	animal but also minimizing the “with-animal” time. For example, animal #7’s audiogram 4	consisted of 12 frequencies tested. Two of these (4 and 150 kHz) did not induce measureable 5	AEPs.  The entire data set was collected in 55 min which includes multiple breaks for other 6	measurements such as blood samples or repositioning the animal.  Records were collected in 7	concert with a suite of other measurements with no discernible impact on the physiological 8	noise.  This allowed for a relatively efficient of data collection when compared to behavioral 9	methods which require significant time to train animals and conduct experiments.  It is also 10	relatively quick for other AEP audiograms which make take multiple days (sessions). Here 11	we collected seven audiograms over six field days (including one day which was poor 12	weather conditions and no whales were sighted).    13	 Despite the potential challenges of the experiment (cold conditions, electrophysiology 14	close to the water, confined spaces, concurrent measurements potentially introducing noise, 15	safety and welfare of the people and animals) the audiograms were of very good quality.  16	They are of equal quality to  the field-based collection-release audiometric data of Cook and 17	Mann (2004) for bottlenosed dolphins (Tursiops truncates) and of Nachtigall et al., (2008;  18	see also Mooney et al. 2009) for white-beaked dolphins (Lagenorhynchus albirostris)  Our 19	success both in ease and safety of data acquisition and quality of the data suggest the methods 20	could easily be applied to other species in similar situations.  This is of particular importance 21	for populations where anthropogenic noise is chronic and has been identified as a potential 22	stressor. Examples are the endangered Cook Inlet D. leucas or the threatened St. Lawrence D. 23	leucas populations. The prevalence of anthropogenic noise in their habitat and its cumulative 24	effects might be compromising the survival of both D. leucas  populations (NMFS 2008;  25	7		DFO 2012).  This assertion is based on current knowledge of the level and acuity of 1	anthropogenic noise in these ecosystems (e.g., Gervaise et al. 2012) and our understanding on 2	D. leucas  hearing and acoustic communication. However, because of the inherent difficulties 3	in evaluating noise impact on cetaceans, there are no data supporting this hypothesis. 4	Audiograms using the method described here could be collected in Cook Inlet and in the St. 5	Lawrence Estuary to measure the hearing of D. leucas with greater exposed to anthropogenic 6	noise and be compared to the baseline audiogram described for Bristol Bay D. leucas. 7	     8	Acknowledgements 9	Project funding and field support provided by Georgia Aquarium and the National Marine 10	Mammal Laboratory of the Alaska Fisheries Science Center (NMML/AFSC). Field work also 11	supported by National Marine Fisheries Service Alaska Regional Office (NMFS AKR), 12	WHOI Arctic Research Initiative, WHOI Ocean Life Institute, U.S. Fish and Wildlife 13	Service, Bristol Bay Native Association, Alaska SeaLife Center, Shedd Aquarium and Mystic 14	Aquarium. Audiogram analyses were funded by the Office of Naval Research award number 15	N000141210203 (from Michael Weise).  We also acknowledge substantial assistance 16	R.Andrews, G. Biedenbach, B. Long, S. Norman, M. Keogh, A. Moors, L. Thompson, T. 17	Binder, L. Naples, L. Cornick, K. Royer, and K. Burek-Huntington, R. Hiratsuka, A. Roehl, 18	B. Tinker and D. Togiak. All work conducted under NMFS permit no. 14245 and in 19	accordance with approval from the NMML/AFSC IACUC protocols (ID number: AFSC-20	NWFSC2012-1) and WHOI IACUC protocols (ID number: BI166330). 21	 22	References 23	Castellote	M	et	al.	(2013)	Baseline	hearing	abilities	and	variability	in	wild	beluga	whales	24	(Delphinapterus	leucas).	J	Exp	Biol	Submitted	25	8		Cook	MLH,	Mann	DA	(2004)	Auditory	brainstem	response	hearing	measurements	in	1	free‐ranging	bottlenose	dolphins	(Tursiops	truncatus).	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Measuring hearing in wild beluga whales

T. Aran Mooney

Manuel Castellote

Lori Quakenbush

Roderick Hobbs

Caroline Goertz

Eric Gaglione

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Measuring Hearing in Wild Beluga Whales

https://darchive.mblwhoilibrary.org/bitstream/1912/8108/1/Aquatic%20Noise%20meeting%20summary%20chapter%20submitted.pdf

Measuring hearing in wild beluga whales

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