FY 2006 PI Report - National Oceanographic Partnership Program

Measuring the behavior and response to sound of beaked whales using recording
Mark Johnson
Woods Hole Oceanographic Institution, Woods Hole, MA 02543
Phone: (508) 289-2605 FAX: (508) 457-2195 E-mail: [email protected]
Peter Tyack
Woods Hole Oceanographic Institution, Woods Hole, MA 02543
Phone: (508) 289-2818 FAX: (508) 457-2138 E-mail: [email protected]
Award Number: OCE-0427577
The goals of this project are to understand the reasons for, and to help to reduce, the strandings of two
little-known species of beaked whales related to mid-frequency navy sonars. Although widely
distributed, these cryptic species are extremely difficult to study and, until recently, almost nothing
was known about their sub-surface behavior or vocalizations. The current project combines an
advanced acoustic and orientation recording tag with visual survey, photo-identification and habitat
characterization in productive field sites. Using these tools, we aim to provide a thorough
characterization of the movement patterns, vocalizations, foraging styles, and preferred habitat of the
two species. Understanding of these factors is critical to designing, and evaluating the success of, any
mitigation measure. Results from the study are directed at two strategies to reduce beaked whale
mortality: first, with a specification of how and when these animals vocalize, it may be possible to
develop systems for passive acoustic detection of beaked whales. Since beaked whales are so difficult
to sight, acoustic detection is a critical method to monitor for the presence of these sensitive species.
The second, longer-term strategy is to determine what factors heighten the risk of stranding and to
identify opportunities to minimize these. While such risk factors may become evident upon examining
the behavior of undisturbed animals, we will also evaluate the practicality of studying the responses of
beaked whales to low levels of sonar-like sounds as a means to define safe exposure limits.
We have been performing a multi-year integrated study of the two beaked whale species most
represented in the atypical strandings, Cuvier's beaked whale (Ziphius cavirostris) and Blainville's
beaked whale (Mesoplodon densirostris). The study is focused on providing crucial information for the
mitigation of sonar-related strandings and is dedicated to the rapid dissemination of this information.
The study takes advantage of two productive field sites for the species of concern, developed under a
prior program (SERDP), in Italy and the Canary Islands. Cornerstones of the study are:
• Year-round visual observation and photo-identification of beaked whales to establish site fidelity,
population size, group composition, patterns of individual associations and habitat preferences.
• Tagging campaigns using high-sampling rate acoustic recording tags to characterize vocalizations,
use of sound, movement patterns, and sub-surface behavior.
• Characterization of the habitats in terms of biological and physical parameters. What are the
environmental factors that attract beaked whales?
The combination of a long-term visual study with a concentrated tagging effort greatly amplifies the
power of each component to describe normal behavior. The study will produce a multi-scale
description of beaked whales that can be used to evaluate hypotheses, and mitigation strategies, for the
strandings. Comparison of data from this study with that from studies of other deep-diving toothedwhales may pinpoint factors that heighten the sensitivity of beaked whales to sonar sounds.
The project brought together new technology in the form of miniature tag devices, and well-established
biological survey methods. We developed a high-frequency acoustic recording tag specifically for
studying beaked whales. The multi-sensor tag is attached to whales using suction cups and provides
unprecedented detail of the acoustic environment and movements of tagged whales. Although the
beaked whale species of concern are notoriously difficult to approach, our success at tagging these
animals is improving with each field season. The integration of tagging work within on-going
population studies provides a context for the detailed short-term data produced by the tag. Monthly
transects of the study areas are carried out by partner groups in Italy and the Canary Islands. Each
group of beaked whales encountered is photographed and observed to determine group structure.
The third and final year of the project was a no-cost extension to provide an opportunity to complete
visual surveys postponed from the previous year due to poor weather. We have also used the extension
year to complete two additional publications (Tyack et al., 2006; Johnson et al., 2006) which describe
the deep diving behavior and vocalizations of the study species with implications to acoustic sensitivity
and to passive acoustic detection.
Since the start of the NOPP project in May 2004, we have performed 5 field experiments in Italy and
the Canary Islands. We have now placed tags on 11 Cuvier's and 8 Blainville's beaked whales yielding
a data set of more than 180 hours of on-animal recording. A majority of the whales were tagged with
high sampling-rate (192kHz) stereo DTAGs, specially developed for this study, providing fullbandwidth recordings of the two species. On two occasions, we tagged pairs of whales swimming in
the same group providing an opportunity to study the behavioral coordination of these whales and to
estimate the source level of vocalizations. Because of the high recording rate of the DTAGs used on
beaked whales, a special suite of analysis and quality assurance tools has been developed.
Colleagues at the University of La Laguna (ULL) and BluWest have performed monthly photoidentification surveys since April 2004 amassing photo-identification data bases of over 70 individual
beaked whales at each study site. Of these, some 10-15 animals at each site have been re-sighted in
different months indicating that at least a part of the population has a pattern of residency and that
overall the populations may be quite small. Calves of Blainville's beaked whale have been recorded in
the Canary Islands site during most surveys while calves of Cuvier's beaked whale were observed for
the first time in September 2005. Calves of Cuvier's beaked whales are often observed in the Italian
site where Blainville's beaked whales are not present. About 16 samples of partially eaten deep sea
squid and fish have been collected in the vicinity of beaked whales providing a possible indication of
Results from the tagging and survey efforts have been reported in 6 journal papers and 19 presentations
at international conferences including two invited talks. We organized a public workshop on beaked
whales and sonar at the European Cetacean Society meeting in La Rochelle in April 2005 to share
information and identify research priorities.
The unique data set collected during this project has yielded a range of new insights into beaked whale
behavior as testified by our growing list of publications. The following is a digest of results obtained to
The click sounds made by the study species during foraging dives are unlike any other sounds reported
from marine mammals (Fig. 1). This result is important not only in understanding the acoustic
behavior of beaked whales but also in developing remote detection methods. We have described the
spectral, temporal, and directionality characteristics of the distinctive clicks in three papers (Johnson et
al., 2004; Zimmer et al., 2005; Johnson et al., 2006). The results have allowed us to explore the
feasibility of detecting beaked whale clicks remotely. Combining the movement data and the
vocalization rates and characteristics collected by the tags in a Monte Carlo simulation we have
modeled the density of listening stations that would be required to detect beaked whales in a given area
with a given level of statistical power. Results have been reported in a conference paper (Tyack et al.,
IEEE-MTS 2006) and a full paper is in preparation.
The foraging dives made by tagged Blainville's and Cuvier's beaked whales are extreme both in terms
of depth (maximum of 2000 m) and duration (maximum of 85 mins). In fact, Cuvier's dive, on average,
deeper and longer than reported for any other marine mammal. Using figures extrapolated from deep
diving seals, both beaked whale species routinely appear to dive well beyond their aerobic dive limit.
Given this, the stereotypical slow ascents from deep dives and the silent shallow dives following deep
dives are puzzling (Fig. 2). Necropsies of some sonar-stranded beaked whales revealed symptoms
consistent with decompression sickness (Jepson, 2004), and it has been suggested that extreme diving
may heighten the risk of this condition. We have described beaked whale diving behavior with an
evaluation of the risk of acquiring decompression sickness in a recent paper (Tyack et al., 2006) and
are continuing with efforts to model the levels of nitrogen saturation in deep-diving marine mammals.
Fast sequences of special clicks, called buzzes, are made periodically during deep foraging dives.
Based on our findings with sperm whales (Miller 2004), we associate buzzes with capture attempts.
Recordings of buzzes together with echoes from prey, made by the tag, provide an unprecedented
opportunity to investigate prey selection and capture, and to estimate foraging efficiency (Madsen et
al., 2005). We have found that Blainville's beaked whales perform stereotypical maneuvers while
approaching certain prey and from this have determined that prey selection can occur at least 10-15
seconds prior to the buzz (paper in preparation) while buzzes are initiated when the prey is about 3 m
from the whale (Johnson et al., 2006). We have also described an occasion in which a tagged Cuvier's
beaked whale appeared to interrupt a foraging dive when sound from a passing ship significantly
increased the ambient noise (Aguilar et al., 2006). This may represent the first direct observation of a
response of a beaked whale to anthropogenic sound and highlights the need to consider the impact of
noise sources other than sonars.
The dive profiles of contemporaneously tagged beaked whales show remarkable coordination of both
foraging and shallow dives. Using the click sounds made during foraging we can measure the distance
between each pair of whales and have found that whales separate horizontally by up to 400 m at the
base of the dive while joining again for the ascent (Fig. 3). With the stereo tag, it is possible to track
untagged whales diving with each tagged whale. We have been able to count the number of individuals
present during a foraging dive and compare it to surface observations of the same group. In each case,
all of the whales in the group seen at the surface are audible during foraging dives. Given the diving
coordination, it appears that dive duration may be determined by the physiological limits of the leastcapable (e.g., smallest) animal in the group. If, as is likely, vocalizations mediate social cohesion
during dives, then there is an added risk that anthropogenic sound may disrupt communication by
masking. We are preparing a paper describing these results.
Fig. 1: Distinctive echolocation clicks produced by Ziphius cavirostris (left) and Mesoplodon
densirostris (right). The long duration frequency modulated clicks are quite unlike the short transients
produced by most delphinids and the high frequency tonal clicks produced by porpoises. The clicks
can be detected from several kilometers opening the possibility of remote acoustic detection of both
National Security
The potential for beaked whale strandings during deep-water naval exercises is a significant issue
facing the navy. The few options to mitigate such strandings requires that a choice be made between
preparedness on the one hand and environmental stewardship on the other. The NOPP project
addresses this issue in two ways: first, characterization of the vocalizations and movements of beaked
whales may enable remote detection of these animals. Secondly, examination of the behavior of
beaked whales may reveal risk factors which give rise to the apparent high sensitivity of these animals.
Such findings may indicate ways to change the usage pattern or the sound of navy sonars in order to
reduce mortality.
Fig 2: Example dive profile of a Ziphius cavirostris, left, and statistical analysis of vertical ascent rates,
right (28 dives from 7 individuals). While the descents are made at a steady vertical rate of some 1.5
m/s, the ascent rate varies widely with depth. Most enigmatically, the ascent rate in the depth range
400-700 m is significantly slower than at other depths.
Economic Development
Evidence is emerging that air-guns used in oil exploration may also trigger beaked whale strandings.
The results from the current study will provide insight into the ways in which anthropogenic noise in
general may impact beaked whales and how these impacts may be reduced.
Quality of Life
The current study indicates that the populations of beaked whales resident in steep submarine canyons
may be quite small. As these habitats coincide with areas of interest for ASW exercises, the resident
populations may be repeatedly impacted at an unsustainable level. While the current study is focused
on the impact of sonars on individual animals, the resulting mitigation measures will operate at the
population level and so improve ecosystem health.
Science Education and Communication
The project has provided data for one PhD and 5 masters-level students in the USA and Europe.
Fig. 3: Three-dimensional reconstruction of the track of two Mesoplodon densirostris tagged
simultaneously. Although the dive depths are very similar, the whales separated at the base of the dive
to forage independently. The whales rejoined during the ascent and were seen surfacing together.
National Security
We are working with Moretti of the U.S. Naval Undersea Warfare Center and Zimmer of the NATO
Undersea Research Center to develop acoustic detection systems based on findings from the study.
Using vocalizations recorded by DTAGs, both partners have been able to verify the presence of beaked
whales in their own acoustic recordings. In a parallel effort funded by the Navy environmental
compliance office, we have performed verification studies with Moretti to match visual observations
with acoustic detections of beaked whales in the AUTEC submarine range in the Bahamas.
Economic Development
Acoustic detection of beaked whales prior to sonar use may turn out to be an essential means to
mitigate strandings. By defining the vocalizations made by the study species, we have enabled an
economic opportunity in designing such systems.
Science Education and Communication
Results from the project have been presented at conferences and workshops, and have been the focus
of research by graduate students. The project has been described in numerous newspaper and television
pieces. Photographs from our field sites showing distinctive characteristics of the study species have
been shared with the Smithsonian Institution for a web-based beaked whale identification resource.
Skin samples from the study species are being shared with researchers in Australia who are performing
a global genetic analysis of beaked whales.
SERDP (www.serdp.org) has funded the PIs under project CS1188 since 2000 to develop methods and
field sites for studying beaked whales. The U.S. Navy office N45 has provided funding to the PIs to
accelerate beaked whale research. This has provided us with resources to develop DTAGs and to
extend the NOPP-funded field efforts. N45 and SERDP have also supported a verification effort with
Moretti of NUWC to match visual and acoustic detections of beaked whales in the AUTEC submarine
range. The University of La Laguna team who are partners on the NOPP project have received support
from the Canary Islands Government and the Spanish Ministry of Defense to support students within
the group and to contribute towards a longer tagging effort in El Hierro.
Jepson, P. D., Arbelo, M., Deaville, R., Patterson, I. A. P., Castro, P., Baker, J. R., Degollada, E., Ross,
H. M., Herráez, P., Pocknell, A. M., Rodriguez, F., Howie, F. E., Espinosa, A., Reid, R. J., Jaber, J. R.,
Martin, V., Cunningham, A. A. & Fernández, A., "Gas-bubble lesions in stranded cetaceans - Was
sonar responsible for a spate of whale deaths after an Atlantic military exercise?", Nature 425, 575576.
Miller P.J.O., Johnson M., Tyack P.L., "Sperm whale behaviour is consistent with use of rapid
echolocation click buzzes “creaks” in prey capture", Proc. R. Soc. Lond. B, Vol. 27, No. 1554, pp.
2239-2247, 2004.
Journal Papers
Johnson M., Madsen P.T., Aguilar Soto N., Tyack P., "Foraging Blainville's beaked whales
(Mesoplodon densirostris) produce distinct click types matched to different phases of echolocation", J.
Exp. Biol., 209, December, 2006.
Tyack P.L., Johnson M., Aguilar de Soto N., Sturlese A., Madsen P.T.M., "Extreme diving of beaked
whales", J. Exp. Biol., 209, October 2006.
Aguilar de Soto N., Johnson M., Madsen P.T.M., Tyack P.L., Bocconcelli A., Borsani F., "Does
intense ship noise disrupt foraging in deep-diving Cuvier's beaked whales (Ziphius cavirostris)?",
Marine Mammal Science, 2006.
Zimmer W. M. X., Johnson M., Madsen P.T.M., Tyack P.L., "Echolocation clicks of free-ranging
Cuvier's beaked whales (Ziphius cavirostris)", J. Ac. Soc. Am., 117, pp. 3919-3927, June 2005.
Madsen P.T., Johnson M., Aguilar de Soto N. , Zimmer W. M. X., Tyack P.L., "Biosonar performance
of foraging beaked whales (Mesoplodon densirostris)", J. Exp. Biology 208, 181-194, Jan. 2005.
Johnson M., Madsen P.T., Zimmer W. M. X., Aguilar de Soto N., Tyack P.L., "Beaked whales
echolocate on prey", Proc. R. Soc. Lond. B 271, pp. S383-386, 2004.
Conference Presentations
Tyack P.L., Johnson M., Zimmer W., Aguilar de Soto N., Madsen P.T., "Acoustic behavior of beaked
whales with implications for acoustic monitoring", IEEE-MTS, Boston, Sept. 2006.
Aguilar de Soto N., Johnson M., Madsen P., Dominguez I., Tyack P., Diaz F., "Buceamos? Cohesion
social durante las imersiones profundas del calderon de aleta corta (Globicephala macrorhynchus), y
los zifios de Blainville (Mesoplodon densirostris) y Cuvier (Ziphius cavirostris)", XI Nacional y VIII
Iber-American Conf. de Etologia, Tenerife, Spain, Sept. 2006.
Madsen P., Johnson M., Aguilar de Soto N., Zimmer W., Tyack P., "Biosonar use of foraging beaked
whales", Soc. of Marine Mammalogy, San Diego, Dec. 2005.
Johnson M., Tyack P., Madsen P., Aguilar de Soto N., Zimmer W., "Unraveling the behavior of
beaked whales (Ziphius cavirostris and Mesoplodon densirostris) using sound and orientation
recording DTAGs", Soc. of Marine Mammalogy, San Diego, Dec. 2005.
Aguilar de Soto N., Johnson M., Madsen P., Tyack P., Bocconcelli A., Borsani F., "Does intense ship
noise disrupt foraging in deep-diving Cuvier's beaked whales (Ziphius cavirostris)?", Society of
Marine Mammalogy, San Diego, Dec. 2005.
Arsenault R., Wiley D., Ware C., Barton K., Shorter K., Johnson M., Moller J., Plumlee M., Sardi K.,
"Geozui4d: a new method for viewing multisensor tag-derived data to investigate the underwater
behaviour of marine mammals", Society of Marine Mammalogy, San Diego, Dec. 2005.
Johnson M., "Make me one with everything: appropriate technology for holographic biologging",
plenary paper at Biologging II symposium, St. Andrews, Scotland, June 2005.
Johnson M., Aguilar de Soto N., Madsen P., Tyack P., "A binaural acoustic recording tag reveals
details of deep foraging in beaked whales", Invited paper at 149th meeting Ac. Soc. Am., Vancouver,
May 2005.
Tyack P.L., Johnson M., Madsen P.T., “Extreme diving behavior of beaked whale species known to
strand in conjunction with use of military sonars”, European Research on Cetaceans 19th, France,
April 2005.
Zimmer W.M.X., Johnson M., Madsen P.T., Tyack P.L., “Echolocation clicks of free-ranging Cuvier’s
beaked whales (Ziphius cavirostris)”, European Research on Cetaceans 19th, France, April 2005.
Johnson M., Madsen P.T.M., Aguilar de Soto N., Tyack P.L., “Echolocation and movement of a
foraging Blainville's beaked whale (Mesoplodon densirostris)”, European Research on Cetaceans 19th,
France, April 2005.
Aparicio C., Guerra M., Hernández A., Padrón A., Díaz F., Domínguez I., Brito A., Johnson M.,
Aguilar de Soto N., “Resident and reproductive populations of beaked whales in El Hierro, Canary
Islands”, European Research on Cetaceans 19th, France, April 2005.
Aguilar de Soto, N., Johnson, M., Madsen, P.T., “Deep foraging of pilot and beaked whales: DTag
results”, European Research on Cetaceans 19th, France, April 2005.
Ballardini, M., Pusser T., Nani B., “Photo-identification of Cuvier’s beaked whales (Ziphius
cavirostris) in the northern Ligurian sea”, submitted to the meeting of the European Cetacean Society,
April 2005.
Madsen P.T., Aguilar de Soto N., Johnson M., Tyack P.T., “Field metabolic rate estimates in large,
deep-diving toothed whales with implications for biomass turnover”, European Research on Cetaceans
19th, France, April 2005.
Madsen P.T., Johnson M., Tyack P.L., Aguilar de Soto N., Zimmer W. M. X., "Biosonar performance
of foraging Blainvilles beaked whales (Mesoplodon densirostris)", 147th meeting Ac. Soc. Am., NY,
May 2004.
Tyack P.L., Johnson M., Madsen P.T., "Echolocation in wild toothed whales", 147th meeting Ac. Soc.
Am., NY, May 2004.
Aguilar N., Johnson M., Aparicio C., Domínguez I., Díaz F., Hernández, A., Guerra, M., Bocconcelli,
A., Brito, A., Tyack, P., "High concentrations of beaked whales observed close to the shore of El
Hierro (Canary Islands)", European Research on Cetaceans 18th, Sweden, 2004.
Tregenza N.J.C., Johnson M., Aguilar de Soto N., "Automated detection of beaked whale sonar",
European Research on Cetaceans 18th, Sweden, 2004.