Echolocation-based foraging by harbor porpoises and sperm whales, including effects of noise and acoustic propagation

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2008.In this thesis, I provide quantitative descriptions of toothed whale echolocation and foraging behavior, including assessment of the effects of noise on foraging behavior and the potential influence of ocean acoustic propagation conditions on biosonar detection ranges and whale noise exposure. In addition to presenting some novel basic science findings, the case studies presented in this thesis have implications for future work and for management. In Chapter 2, I describe the application of a modified version of the Dtag to studies of harbor porpoise echolocation behavior. The study results indicate how porpoises vary the rate and level of their echolocation clicks during prey capture events; detail the differences in echolocation behavior between different animals and in response to differences in prey fish; and show that, unlike bats, porpoises continue their echolocation buzz after the moment of prey capture. Chapters 3-4 provide case studies that emphasize the importance of applying realistic models of ocean acoustic propagation in marine mammal studies. These chapters illustrate that, although using geometric spreading approximations to predict communication/target detection ranges or noise exposure levels is appropriate in some cases, it can result in large errors in other cases, particularly in situations where refraction in the water column or multi-path acoustic propagation are significant. Finally, in Chapter 5, I describe two methods for statistical analysis of whale behavior data, the rotation test and a semi-Markov chain model. I apply those methods to test for changes in sperm whale foraging behavior in response to airgun noise exposure. Test results indicate that, despite the low-level exposures experienced by the whales in the study, some (but not all) of them reduced their buzz production rates and altered other foraging behavior parameters in response to the airgun exposure.Work presented in this thesis was supported by a National Science Foundation Graduate Research Fellowship, the WHOI Ocean Life Institute (Grant Numbers 32031300 and 25051351), the Office of Naval Research, the U.S. Department of the Interior Minerals Management Service (Cooperative Agreement Numbers 1435-01-02-CA-85186 and NA87RJ0445; WHOI Grant Number 15205601), the Industry Research Funding Coalition, and the WHOI/MIT Joint Program in Oceanography/Applied Ocean Science & Engineering (including a Fye Teaching Fellowship)

Beluga whale (Delphinapterus leucas) acoustic foraging behavior and applications for long term monitoring

This paper is not subject to U.S. copyright. The definitive version was published in Castellote, M., Mooney, A., Andrews, R., Deruiter, S., Lee, W.-J., Ferguson, M., & Wade, P. Beluga whale (Delphinapterus leucas) acoustic foraging behavior and applications for long term monitoring. Plos One, 16(11), (2021): e0260485, https://doi.org/10.1371/journal.pone.0260485.Cook Inlet, Alaska, is home to an endangered and declining population of 279 belugas (Delphinapterus leucas). Recovery efforts highlight a paucity of basic ecological knowledge, impeding the correct assessment of threats and the development of recovery actions. In particular, information on diet and foraging habitat is very limited for this population. Passive acoustic monitoring has proven to be an efficient approach to monitor beluga distribution and seasonal occurrence. Identifying acoustic foraging behavior could help address the current gap in information on diet and foraging habitat. To address this conservation challenge, eight belugas from a comparative, healthy population in Bristol Bay, Alaska, were instrumented with a multi-sensor tag (DTAG), a satellite tag, and a stomach temperature transmitter in August 2014 and May 2016. DTAG deployments provided 129.6 hours of data including foraging and social behavioral states. A total of 68 echolocation click trains ending in terminal buzzes were identified during successful prey chasing and capture, as well as during social interactions. Of these, 37 click trains were successfully processed to measure inter-click intervals (ICI) and ICI trend in their buzzing section. Terminal buzzes with short ICI (minimum ICI <8.98 ms) and consistently decreasing ICI trend (ICI increment range <1.49 ms) were exclusively associated with feeding behavior. This dual metric was applied to acoustic data from one acoustic mooring within the Cook Inlet beluga critical habitat as an example of the application of detecting feeding in long-term passive acoustic monitoring data. This approach allowed description of the relationship between beluga presence, feeding occurrence, and the timing of spawning runs by different species of anadromous fish. Results reflected a clear preference for the Susitna River delta during eulachon (Thaleichthys pacificus), Chinook (Oncorhynchus tshawytscha), pink (Oncorhynchus gorbuscha), and coho (Oncorhynchus kisutch) salmon spawning run periods, with increased feeding occurrence at the peak of the Chinook and pink salmon runs.Project funding was provided by Georgia Aquarium, the Marine Mammal Laboratory of the Alaska Fisheries Science Center (MML/AFSC). Tagging was funded by the NOAA Fisheries Office of Science and Technology’s Ocean Acoustics Program. DTAG data analysis was funded by the U.S. Marine Mammal Commission grant #16-239. Funding for collecting and analyzing Cook Inlet beluga acoustic data in Susitna Delta was provided by the National Marine Fisheries Service Section 6 Office to the Alaska Department of Fish and Game. This publication is partially funded by the Cooperative Institute for Climate, Ocean, and Ecosystem Studies (CICOES), University of Washington, under NOAA Cooperative Agreement NA15OAR4320063, Contribution No. 2021-1145

First direct measurements of behavioural responses by Cuvier's beaked whales to mid-frequency active sonar

Most marine mammal­ strandings coincident with naval sonar exercises have involved Cuvier's beaked whales (Ziphius cavirostris). We recorded animal movement and acoustic data on two tagged Ziphius and obtained the first direct measurements of behavioural responses of this species to mid-frequency active (MFA) sonar signals. Each recording included a 30-min playback (one 1.6-s simulated MFA sonar signal repeated every 25 s); one whale was also incidentally exposed to MFA sonar from distant naval exercises. Whales responded strongly to playbacks at low received levels (RLs; 89–127 dB re 1 µPa): after ceasing normal fluking and echolocation, they swam rapidly, silently away, extending both dive duration and subsequent non-foraging interval. Distant sonar exercises (78–106 dB re 1 µPa) did not elicit such responses, suggesting that context may moderate reactions. The observed responses to playback occurred at RLs well below current regulatory thresholds; equivalent responses to operational sonars could elevate stranding risk and reduce foraging efficiency.Publisher PDFPeer reviewe

Behavioral responses of fin whales to military mid-frequency active sonar

Funding. Primary funding for the SOCAL-BRS project was initially provided by the US Navy’s Chief of Naval Operations Environmental Readiness Division and subsequently by the US Navy’s Living Marine Resources (LMR) Program. Additional support for environmental sampling and logistics was also provided by the Office of Naval Research, Marine Mammal Program.The effect of active sonars on marine mammal behavior is a topic of considerable interest and scientific investigation. Some whales, including the largest species (blue whales, Balaenoptera musculus), can be impacted by mid-frequency (1-10 kHz) military sonars. Here we apply complementary experimental methods to provide the first experimentally controlled measurements of behavioral responses to military sonar and similar stimuli for a related endangered species, fin whales (Balaenoptera physalus). Analytical methods include: (1) Principal Component Analysis paired with Generalized Additive Mixed Models; (2) Hidden Markov Models; and (3) structured expert elicitation using response severity metrics. These approaches provide complementary perspectives on the nature of potential changes within and across individuals. Behavioral changes were detected in five of 15 whales during controlled exposure experiments (CEEs) using mid-frequency active sonar (MFAS) or pseudorandom noise (PRN) of similar frequency, duration, and source and received level. No changes were detected during six control (no noise) sequences. Overall responses were more limited in occurrence, severity, and duration than in blue whales and were less dependent upon contextual aspects of exposure and more contingent upon exposure received level. Quantifying the factors influencing marine mammal responses to sonar is critical in assessing and mitigating future impacts.Publisher PDFPeer reviewe

A rotation test for behavioural point-process data

Author Posting. © Elsevier B.V., 2008. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Animal Behaviour 76 (2008): 1429-1434, doi:10.1016/j.anbehav.2008.06.016.A common problem in animal behavior is determining whether the rate at which a certain behavioural event occurs is affected by an environmental or other factor. In the example considered later in this paper, the event is a vocalization by an individual sperm whale and the factor is the operation or non-operation of an underwater sound source. A typical experiment to test for such effects involves observing animals during control and treatment periods and recording the times of the events that occur in each. In statistical terminology, the data arising from such an experiment – the times at which events of a specified type occur – represent a point process (Cox & Lewis 1978). Events in a point process are treated as having no duration. Although this is not strictly correct for behavioural events, the approximation is reasonable when the duration of events is small in relation to the interval between them.Funding for the sperm whale experiments was provided by the Office of Naval Research, the U.S. Department of the Interior Minerals Management Service Cooperative Agreements Nos. 1435-01-02-CA-321 85186 and NA87RJ0445, and the Industry Research Funding Coalition

First indications that northern bottlenose whales are sensitive to behavioural disturbance from anthropogenic noise

-Although northern bottlenose whales were the most heavily hunted beaked whale, we have little information about this species in its remote habitat of the North Atlantic Ocean. Underwater anthropogenic noise and disruption of their natural habitat may be major threats, given the sensitivity of other beaked whales to such noise disturbance. We attached dataloggers to 13 northern bottlenose whales and compared their natural sounds and movements to those of one individual exposed to escalating levels of 1–2 kHz upsweep naval sonar signals. At a received sound pressure level (SPL) of 98 dB re 1 μPa, the whale turned to approach the sound source, but at a received SPL of 107 dB re 1 μPa, the whale began moving in an unusually straight course and then made a near 180° turn away from the source, and performed the longest and deepest dive (94 min, 2339 m) recorded for this species. Animal movement parameters differed significantly from baseline for more than 7 h until the tag fell off 33–36 km away. No clicks were emitted during the response period, indicating cessation of normal echolocation-based foraging. A sharp decline in both acoustic and visual detections of conspecifics after exposure suggests other whales in the area responded similarly. Though more data are needed, our results indicate high sensitivity of this species to acoustic disturbance, with consequent risk from marine industrialization and naval activity

Vocal foragers and silent crowds : context-dependent vocal variation in Northeast Atlantic long-finned pilot whales

This study was financially supported by the US Office of Naval Research, The Netherlands Ministry of Defence, the Norwegian Research Council and the Norwegian Ministry of Defence.Vocalisations form a key component of the social interactions and foraging behaviour of toothed whales. We investigated changes in calling and echolocation behaviour of long-finned pilot whales between foraging and non-foraging periods, by combining acoustic recordings and diving depth data from tagged individuals with concurrent surface observations on social behaviour of their group. The pilot whales showed marked vocal variation, specific to foraging and social context. During periods of foraging, pilot whales showed more vocal activity than during non-foraging periods (rest, travel). In addition to the expected increase in echolocation activity, call rates also increased, suggesting that pilot whales communicate more during foraging. Furthermore, calls with multiple inflections occurred more often immediately before and after foraging dives and during the early descent and late ascent phases of foraging dives. However, these calls were almost never detected at diving depths of the tagged whale beyond 350 m. Calls with no or few inflections were produced at all times, irrespective of diving depth of the tagged whale. We discuss possible explanations for the distinct vocal variation associated with foraging periods. In addition, during non-foraging periods, the pilot whales were found to be more silent (no calling or echolocation) in larger, more closely spaced groups. This indicates that increased levels of social cohesion may release the need to stay in touch acoustically. Significance statement: Social toothed whales rely on vocalisations to find prey and interact with conspecifics. Species are often highly vocal and can have elaborate call repertoires. However, it often remains unclear how their repertoire use correlates to specific social and behavioural contexts, which is vital to understand toothed whale foraging strategies and sociality. Combining on-animal tag recordings of diving and acoustic behaviour with observations of social behaviour, we found that pilot whales produce more calls during foraging than during non-foraging periods. Moreover, highly inflected calls were closely associated to the periods around and during foraging dives. This indicates enhanced communication during foraging, which may, for example, enable relocation of conspecifics or sharing of information. Whales reduced their vocal activity (calling and echolocation) at increased levels of social cohesion, indicating that in certain behavioural contexts, closer association (i.e. more closely spaced) may release the need to stay in touch acoustically.Publisher PDFPeer reviewe

Modeling acoustic propagation of airgun array pulses recorded on tagged sperm whales (Physeter macrocephalus)

Author Posting. © Acoustical Society of America, 2006. This article is posted here by permission of Acoustical Society of America for personal use, not for redistribution. The definitive version was published in Journal of the Acoustical Society of America 120 (2006): 4100-4114, doi:10.1121/1.2359705.In 2002 and 2003, tagged sperm whales (Physeter macrocephalus) were experimentally exposed to airgun pulses in the Gulf of Mexico, with the tags providing acoustic recordings at measured ranges and depths. Ray trace and parabolic equation (PE) models provided information about sound propagation paths and accurately predicted time of arrival differences between multipath arrivals. With adequate environmental information, a broadband acoustic PE model predicted the relative levels of multipath arrivals recorded on the tagged whales. However, lack of array source signature data limited modeling of absolute received levels. Airguns produce energy primarily below 250 Hz, with spectrum levels about 20–40 dB lower at 1 kHz. Some arrivals recorded near the surface in 2002 had energy predominantly above 500 Hz; a surface duct in the 2002 sound speed profile helps explain this effect, and the beampattern of the source array also indicates an increased proportion of high-frequency sound at near-horizontal launch angles. These findings indicate that airguns sometimes expose animals to measurable sound energy above 250 Hz, and demonstrate the influences of source and environmental parameters on characteristics of received airgun pulses. The study also illustrates that on-axis source levels and simple geometric spreading inadequately describe airgun pulse propagation and the extent of exposure zones.Funding for this work was provided by the Office of Naval Research, the U.S. Department of the Interior Minerals Management Service Cooperative Agreements Nos. 1435-01-02- CA-85186 and NA87RJ0445, and the Industry Research Funding Coalition. S.L.D.R. was supported by a National Science Foundation Graduate Research Fellowship

Diving Behavior and Fine-Scale Kinematics of Free-Ranging Risso's Dolphins Foraging in Shallow and Deep-Water Habitats

Air-breathing marine predators must balance the conflicting demands of oxygen conservation during breath-hold and the cost of diving and locomotion to capture prey. However, it remains poorly understood how predators modulate foraging performance when feeding at different depths and in response to changes in prey distribution and type. Here, we used high-resolution multi-sensor tags attached to Risso's dolphins (Grampus griseus) and concurrent prey surveys to quantify their foraging performance over a range of depths and prey types. Dolphins (N = 33) foraged in shallow and deep habitats [seabed depths less or more than 560 m, respectively] and within the deep habitat, in vertically stratified prey features occurring at several aggregation levels. Generalized linear mixed-effects models indicated that dive kinematics were driven by foraging depth rather than habitat. Bottom-phase duration and number of buzzes (attempts to capture prey) per dive increased with depth. In deep dives, dolphins were gliding for &gt;50% of descent and adopted higher pitch angles both during descent and ascents, which was likely to reduce energetic cost of longer transits. This lower cost of transit was counteracted by the record of highest vertical swim speeds, rolling maneuvers and stroke rates at depth, together with a 4-fold increase in the inter-buzz interval (IBI), suggesting higher costs of pursuing, and handling prey compared to shallow-water feeding. In spite of the increased capture effort at depth, dolphins managed to keep their estimated overall metabolic rate comparable across dive types. This indicates that adjustments in swimming modes may enable energy balance in deeper dives. If we think of the surface as a central place where divers return to breathe, our data match predictions that central place foragers should increase the number and likely quality of prey items at greater distances. These dolphins forage efficiently from near-shore benthic communities to depth-stratified scattering layers, enabling them to maximize their fitness