A 3D stereo camera system for precisely positioning animals in space and time

PLT was supported by the Scottish Funding Council (grant HR09011) through the Marine Alliance for Science and Technology for Scotland.Here, we describe a portable stereo camera system that integrates a GPS receiver, an attitude sensor and 3D stereo photogrammetry to rapidly estimate the position of multiple animals in space and time. We demonstrate the performance of the system during a field test by simultaneously tracking the individual positions of six long-finned pilot whales, Globicephala melas. In shore-based accuracy trials, a system with a 50-cm stereo baseline had an average range estimation error of 0.09 m at a 5-m distance increasing up to 3.2 at 50 m. The system is especially useful in field situations where it is necessary to follow groups of animals travelling over relatively long distances and time periods whilst obtaining individual positions with high spatial and temporal resolution (up to 8 Hz). These positions provide quantitative estimates of a variety of key parameters and indicators for behavioural studies such as inter-animal distances, group dispersion, speed and heading. This system can additionally be integrated with other techniques such as archival tags, photo-identification methods or acoustic playback experiments to facilitate fieldwork investigating topics ranging from natural social behaviour to how animals respond to anthropogenic disturbance. By grounding observations in quantitative metrics, the system can characterize fine-scale behaviour or detect changes as a result of disturbance that might otherwise be difficult to observe.PostprintPeer reviewe

Dose response severity functions for acoustic disturbance in cetaceans using recurrent event survival analysis

This work was financially supported by the U. S. Office of Naval Research grant N00014‐12‐1‐0204, under the project “Multi‐study Ocean acoustics Human effects Analysis” (MOCHA). . L. Tyack received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. The case study data were provided by the 3S project, which was funded by the U.S. Office of Naval Research, the Norwegian Ministry of Defense, the Netherlands Ministry of Defense, and WWF Norway.Behavioral response studies (BRSs) aim to enhance our understanding of the behavior changes made by animals in response to specific exposure levels of different stimuli, often presented in an increasing dosage. Here, we focus on BRSs that aim to understand behavioral responses of free-ranging whales and dolphins to manmade acoustic signals (although the methods are applicable more generally). One desired outcome of these studies is dose-response functions relevant to different species, signals and contexts. We adapted and applied recurrent event survival analysis (Cox proportional hazard models) to data from the 3S BRS project, where multiple behavioral responses of different severities had been observed per experimental exposure and per individual based upon expert scoring. We included species, signal type, exposure number and behavioral state prior to exposure as potential covariates. The best model included all main effect terms, with the exception of exposure number, as well as two interaction terms. The interactions between signal and behavioral state, and between species and behavioral state highlighted that the sensitivity of animals to different signal types (a 6–7 kHz upsweep sonar signal [MFAS] or a 1–2 kHz upsweep sonar signal [LFAS]) depended on their behavioral state (feeding or nonfeeding), and this differed across species. Of the three species included in this analysis (sperm whale [Physeter macrocephalus], killer whale [Orcinus orca] and long-finned pilot whale [Globicephala melas]), killer whales were consistently the most likely to exhibit behavioral responses to naval sonar exposure. We conclude that recurrent event survival analysis provides an effective framework for fitting dose-response severity functions to data from behavioral response studies. It can provide outputs that can help government and industry to evaluate the potential impacts of anthropogenic sound production in the ocean.Publisher PDFPeer reviewe

Flash and grab : deep-diving southern elephant seals trigger anti-predator flashes in bioluminescent prey

Funding: Fondation BNP Paribas; Centre National d'Etudes Spatiales; Institut Polaire Français Paul Emile Victor; Natural Environment Research Council; H2020 Marie Skłodowska-Curie Actions.Bioluminescence, which occurs in approximately 80% of the world's mesopelagic fauna, can take the form of a low-intensity continuous glow (e.g. for counter-illumination or signalling) or fast repetitions of brighter anti-predatory flashes. The southern elephant seal (SES) is a major consumer of mesopelagic organisms, in particular the abundant myctophid fish, yet the fine-scale relationship between this predator's foraging behaviour and bioluminescent prey remains poorly understood. We hypothesised that brief, intense light emissions should be closely connected with prey strikes when the seal is targeting bioluminescent prey that reacts by emitting anti-predator flashes. To test this, we developed a biologging device containing a fast-sampling light sensor together with location and movement sensors to measure simultaneously anti-predator bioluminescent emissions and the predator's attack motions with a 20 ms resolution. Tags were deployed on female SES breeding at Kerguelen Islands and Península Valdés, Argentina. In situ light levels in combination with duration of prey capture attempts indicated that seals were targeting a variety of prey types. For some individuals, bioluminescent flashes occurred in a large proportion of prey strikes, with the timing of flashes closely connected with the predator's attack motion, suggestive of anti-predator emissions. Marked differences across individuals and location indicate that SES do exploit bioluminescent organisms but the proportion of these in the diet varies widely with location. The combination of wideband light and acceleration data provides new insight into where and when different prey types are encountered and how effectively they might be captured.Publisher PDFPeer reviewe

Parameterizing animal sounds and motion with animal-attached tags to study acoustic communication

Funding: Dolphin Quest, Inc.; School of Biology, University of St Andrews; Scottish Universities Life Sciences Alliance; Office of Naval Research; Marine Alliance for Science and Technology for Scotland; Horizon H2020.Stemming from the traditional use of field observers to score states and events, the study of animal behaviour often relies on analyses of discrete behavioural categories. Many studies of acoustic communication record sequences of animal sounds, classify vocalizations, and then examine how call categories are used relative to behavioural states and events. However, acoustic parameters can also convey information independent of call type, offering complementary study approaches to call classifications. Animal-attached tags can continuously sample high-resolution behavioural data on sounds and movements, which enables testing how acoustic parameters of signals relate to parameters of animal motion. Here, we present this approach through case studies on wild common bottlenose dolphins (Tursiops truncatus). Using data from sound-and-movement recording tags deployed in Sarasota (FL), we parameterized dolphin vocalizations and motion to investigate how senders and receivers modified movement parameters (including vectorial dynamic body acceleration, “VeDBA”, a proxy for activity intensity) as a function of signal parameters. We show that (1) VeDBA of one female during consortships had a negative relationship with centroid frequency of male calls, matching predictions about agonistic interactions based on motivation-structural rules; (2) VeDBA of four males had a positive relationship with modulation rate of their pulsed vocalizations, confirming predictions that click-repetition rate of these calls increases with agonism intensity. Tags offer opportunities to study animal behaviour through analyses of continuously sampled quantitative parameters, which can complement traditional methods and facilitate research replication. Our case studies illustrate the value of this approach to investigate communicative roles of acoustic parameter changes.Publisher PDFPeer reviewe

Sperm whales reduce foraging effort during exposure to 1-2 kH z sonar and killer whale sounds

We would like to thank 3S partners and funders especially for enabling this research (NL Ministry of Defence, NOR Ministry of Defence, US Office of Naval Research, and World Wildlife Fund, Norway). PLT was supported by the Scottish Funding Council (grant HR09011) through the Marine Alliance for Science and Technology for Scotland.The time and energetic costs of behavioral responses to incidental and experimental sonar exposures, as well as control stimuli, were quantified using hidden state analysis of time series of acoustic and movement data recorded by tags (DTAG) attached to 12 sperm whales (Physeter macrocephalus) using suction cups. Behavioral state transition modeling showed that tagged whales switched to a non-foraging, non-resting state during both experimental transmissions of low-frequency active sonar from an approaching vessel (LFAS; 1-2 kH z, source level 214 dB re 1 μPa m, four tag records) and playbacks of potential predator (killer whale, Orcinus orca) sounds broadcast at naturally occurring sound levels as a positive control from a drifting boat (five tag records). Time spent in foraging states and the probability of prey capture attempts were reduced during these two types of exposures with little change in overall locomotion activity, suggesting an effect on energy intake with no immediate compensation. Whales switched to the active non-foraging state over received sound pressure levels of 131-165 dB re 1 μPa during LFAS exposure. In contrast, no changes in foraging behavior were detected in response to experimental negative controls (no-sonar ship approach or noise control playback) or to experimental medium-frequency active sonar exposures (MFAS; 6-7 kH z, source level 199 re 1 μPa m, received sound pressure level [SPL] = 73-158 dB re 1 μPa). Similarly, there was no reduction in foraging effort for three whales exposed to incidental, unidentified 4.7-5.1 kH z sonar signals received at lower levels (SPL = 89-133 dB re 1 μPa). These results demonstrate that similar to predation risk, exposure to sonar can affect functional behaviors, and indicate that increased perception of risk with higher source level or lower frequency may modulate how sperm whales respond to anthropogenic sound.Publisher PDFPeer reviewe

The Sarasota Dolphin Whistle Database : a unique long-term resource for understanding dolphin communication

Funding for data collection and analysis over the years has been provided by the National Science Foundation, The Royal Society of London, Dolphin Quest, Adelaide M. and Charles B. Link Foundation, Marine Mammal Commission, National Oceanic and Atmospheric Administration, Earthwatch Institute, Protect Wild Dolphins Fund of the Harbor Branch Oceanographic Institute, Grossman Family Foundation, WHOI Ocean Life Institute, Vulcan Machine Learning Center for Impact, and the Allen Institute for Artificial Intelligence. Current support for PT’s involvement is provided by the Office of Naval Research Grants N00014-18-1-2062 and N00014-20-1-2709 through a subaward from Carnegie Mellon University. Current support for LS’s involvement is provided by the Adelaide M. & Charles B. Link Foundation and Dolphin Quest.Common bottlenose dolphins (Tursiops truncatus) produce individually distinctive signature whistles that are learned early in life and that help animals recognize and maintain contact with conspecifics. Signature whistles are the predominant whistle type produced when animals are isolated from conspecifics. Health assessments of dolphins in Sarasota, Florida (USA) provide a unique opportunity to record signature whistles, as dolphins are briefly separated from conspecifics. Recordings were first made in the mid 1970’s, and then nearly annually since 1984. The Sarasota Dolphin Whistle Database (SDWD) now contains 926 recording sessions of 293 individual dolphins, most of known age, sex, and matrilineal relatedness. The longest time span over which an individual has been recorded is 43 years, and 85 individuals have been recorded over a decade or more. Here we describe insights about signature whistle structure revealed by this unique and expansive dataset. Signature whistles of different dolphins show great variety in their fundamental frequency contours. Signature whistle types (with ‘whistle type’ defined as all whistles visually categorized as sharing a particular frequency modulation pattern) can consist of a single stereotyped element, or loop (single-loop whistles), or of multiple stereotyped loops with or without gaps (multi-loop whistles). Multi-loop signature whistle types can also show extensive variation in both number and contour of loops. In addition, fundamental frequency contours of all signature whistle types can be truncated (deletions) or embellished (additions), and other features are also occasionally incorporated. However, even with these variable features, signature whistle types tend to be highly stereotyped and easily distinguishable due to the extensive variability in contours among individuals. In an effort to quantify this individual distinctiveness, and to compare it to other species, we calculated Beecher’s Information Statistic and found it to be higher than for any other animal signal studied so far. Thus, signature whistles have an unusually high capacity to convey information on individual identity. We briefly review the large range of research projects that the SDWD has enabled thus far, and look ahead to its potential to answer a broad suite of questions about dolphin communication.Publisher PDFPeer reviewe

The multi-dimensional nature of vocal learning

Funding; S.C.V. was supported by a Max Planck Research Group (MPRG), a Human Frontiers Science Program (HFSP) Research grant (grant no. RGP0058/2016) and a UKRI Future Leaders Fellowship (grant no. MR/T021985/1). P.L.T. was supported by US Office of Naval Research (ONR) grant nos N00014-18-1-2062 and N00014-20-1-2709. B.P.K. was supported by the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 751356. V.C.B. was supported by the DK Cognition and Communication by the Austrian Science Fund (FWF) grant no. W1262-B29.How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav.60, 1–11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci.4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning.Publisher PDFPeer reviewe

Mitigation of harm during a novel behavioural response study involving active sonar and wild cetaceans

Some studies of how human activities can affect wild free-ranging animals may be considered to have potential negative outcomes too severe to beethically studied. This creates a societal dilemma involving choices between continuing risky activities with high uncertainty about their potentialeffects on wildlife, often with considerable associated precaution or undertaking focused research to reduce uncertainty, but with some risk of harmfrom either strong response leading to potential stranding or direct physical injury from sound exposure. Recent and ongoing field experimentshave measured the conditions in which wild cetaceans respond to military sonar, and provided insight into the nature of responses. Here mitigationmeasures are reported for one of the first such experiments designed to measure fine-scale behavioural responses to controlled exposures of midfrequency(3–4 kHz) active sonar. The objective was to do so without causing the kinds of physical harm that have been previously observed (e.g.stranding events) and that motivated the study. A critical goal of this experimental study was to identify a response that was safe but that could beused as an indicator of the probability of risk from more extreme or sustained exposure from real military operations. A monitoring and mitigationprotocol was developed using a feedback control procedure for real-time mitigation of potential harm. Experimental protocols were modulatedrelative to indicators of potential risk with the explicit objective of detecting potentially harmful consequences of sound exposure and takingappropriate corrective action. Three categories of mitigation methods were developed and integrated within the experimental protocol incorporatingdesigned, engineered, and operational mitigation measures. Controlled exposure experiments involving free-ranging animals were conducted withoutany evident harm to the experimental subjects, while successfully eliciting behavioural responses that provided meaningful results to informmanagement decisions. This approach demonstrates the importance of careful design of protocols in exposure-response experiments, particularlyin pioneering studies assessing response where both the potential for harm and level of uncertainty may be high.Publisher PDFPeer reviewe

Marine mammals and sonar : dose-response studies, the risk-disturbance hypothesis and the role of exposure context

This manuscript was written following the Behavioral Response Research Evaluation Workshop (BRREW), jointly sponsored by the US Office of Naval Research, US Navy Living Marine Resources, and US National Oceanic and Atmospheric Administration - National Marine Fisheries Service. PLT acknowledges funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.1. Marine mammals may be negatively affected by anthropogenic noise. Behavioural response studies (BRSs) aim to establish a relationship between the exposure dose of a stressor and associated behavioural responses of animals. A recent series of BRSs have focused on the effects of naval sonar on cetaceans. Here we review the current state of understanding of the impact of sonar on marine mammals and highlight knowledge gaps and future research priorities. 2. Many marine mammal species exhibit responses to naval sonar. However, responses are highly variable between and within individuals, species and populations, highlighting the importance of context in modulating dose-response relationships. 3. There is increasing support for the risk-disturbance hypothesis as an underlying response mechanism. This hypothesis proposes that sonar sounds may be perceived by animals as a threat, evoking an evolved anti-predator response. An understanding of responses within both the dose-response and risk-disturbance frameworks may enhance our ability to predict responsiveness for unstudied species and populations. 4. Many observed behavioural responses are energetically costly, but the way in which these responses may lead to long-term individual and population level impacts is poorly understood. Synthesis and Applications Behavioural response studies have greatly enhanced our understanding of the potential effects of navy sonar on marine mammals. Despite data gaps, we believe a dose-response approach within a risk-disturbance framework will enhance our ability to predict responsiveness for unstudied species and populations. We advocate for (1) regulatory frameworks to utilise recent peer-reviewed research findings when making predictions of impact (where feasible within assessment cycles), (2) regulatory frameworks to account for the inherent uncertainty in predictions of impact, and (3) investment in monitoring programmes that are both directed by recent research and offer opportunities for validation of predictions at the individual and population level.Publisher PDFPeer reviewe

Estimating the effects of stressors on the health, survival and reproduction of a critically endangered, long-lived species

Funding: Office of Naval Research (Grant Number(s): N000142012697, N000142112096); Strategic Environmental Research and Development Program (Grant Number(s): RC20-1097, RC20-7188, RC21-3091).Quantifying the cumulative effects of stressors on individuals and populations can inform the development of effective management and conservation strategies. We developed a Bayesian state–space model to assess the effects of multiple stressors on individual survival and reproduction. In the model, stressor effects on vital rates are mediated by changes in underlying health, allowing for the comparison of effect sizes while accounting for intrinsic factors that might affect an individual's vulnerability and resilience. We applied the model to a 50-year dataset of sightings, calving events and stressor exposure of critically endangered North Atlantic right whales Eubalaena glacialis. The viability of this population is threatened by a complex set of stressors, including vessel strikes, entanglement in fishing gear and fluctuating prey availability. We estimated that blunt and deep vessel strike injuries and severe entanglement injuries had the largest effect on the health of exposed individuals, reinforcing the urgent need for mitigation measures. Prey abundance had a smaller but protracted effect on health across individuals, and estimated long-term trends in survival and reproduction followed the trend of the prey index, highlighting that long-term ecosystem-based management strategies are also required. Our approach can be applied to quantify the effects of multiple stressors on any long-lived species where suitable indicators of health and long-term monitoring data are available.Publisher PDFPeer reviewe