Disturbance-specific social responses in long-finned pilot whales, Globicephala melas

The study was funded by the US Office of Naval Research, The Netherlands Ministry of Defence, Norwegian Ministry of Defence and French Ministry of Defence. F.V., C.C., P.K., F.P.L. and P.M. were supported by one or two of these funders. P.T. received 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.Social interactions among animals can influence their response to disturbance. We investigated responses of long-finned pilot whales to killer whale sound playbacks and two anthropogenic sources of disturbance: Tagging effort and naval sonar exposure. The acoustic scene and diving behaviour of tagged individuals were recorded along with the social behaviour of their groups. All three disturbance types resulted in larger group sizes, increasing social cohesion during disturbance. However, the nature and magnitude of other responses differed between disturbance types. Tagging effort resulted in a clear increase in synchrony and a tendency to reduce surface logging and to become silent (21% of cases), whereas pilot whales increased surface resting during sonar exposure. Killer whale sounds elicited increased calling rates and the aggregation of multiple groups, which approached the sound source together. This behaviour appears to represent a mobbing response, a likely adaptive social defence against predators or competitors. All observed response-Tactics would reduce risk of loss of group coordination, suggesting that, in social pilot whales, this could drive behavioural responses to disturbance. However, the behavioural means used to achieve social coordination depends upon other considerations, which are disturbance-specific.Publisher PDFPeer reviewe

Behavioral responses to predatory sounds predict sensitivity of cetaceans to anthropogenic noise within a soundscape of fear

Funding was provided by the US Navy Living Marine Resources and Office of Naval Research programs, Netherlands Ministry of Defence, Norwegian Ministry of Defence, UK Defence Science and Technology Laboratory, and DGA French Ministry of Defence.Acoustic signals travel efficiently in the marine environment, allowing soniferous predators and prey to eavesdrop on each other. Our results with four cetacean species indicate that they use acoustic information to assess predation risk and have evolved mechanisms to reduce predation risk by ceasing foraging. Species that more readily gave up foraging in response to predatory sounds of killer whales also decreased foraging more during 1- to 4-kHz sonar exposures, indicating that species exhibiting costly antipredator responses also have stronger behavioral reactions to anthropogenic noise. This advance in our understanding of the drivers of disturbance helps us to predict what species and habitats are likely to be most severely impacted by underwater noise pollution in oceans undergoing increasing anthropogenic activities. As human activities impact virtually every animal habitat on the planet, identifying species at-risk from disturbance is a priority. Cetaceans are an example taxon where responsiveness to anthropogenic noise can be severe but highly species and context specific, with source–receiver characteristics such as hearing sensitivity only partially explaining this variability. Here, we predicted that ecoevolutionary factors that increase species responsiveness to predation risk also increase responsiveness to anthropogenic noise. We found that reductions in intense-foraging time during exposure to 1- to 4-kHz naval sonar and predatory killer whale sounds were highly correlated (r = 0.92) across four cetacean species. Northern bottlenose whales ceased foraging completely during killer whale and sonar exposures, followed by humpback, long-finned pilot, and sperm whales, which reduced intense foraging by 48 to 97level responses to killer whale playbacks, implying a similar level of perceived risk. The correlation cannot be solely explained by hearing sensitivity, indicating that species- and context-specific antipredator adaptations also shape cetacean responses to human-made noise. Species that are more responsive to predator presence are predicted to be more disturbance sensitive, implying a looming double whammy for Arctic cetaceans facing increased anthropogenic and predator activity with reduced ice cover.Publisher PDFPeer reviewe

How effectively do horizontal and vertical response strategies of long-finned pilot whales reduce sound exposure from naval sonar?

PJW was supported with studentships of The Netherlands Ministry of Defence (grant number 032.30370/01.02) and the VSB Foundation (grant number VSB.08/228-E) and Ren e Dekeling is acknowledged for making funding possible. The 3S project was supported by the US Office of Naval Research, The Netherlands Ministry of Defence, Royal Norwegian Navy and Norwegian Ministry of Defence, and by World Wildlife Fund Norway. PLT received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged.The behaviour of a marine mammal near a noise source can modulate the sound exposure it receives. We demonstrate that two long-finned pilot whales both surfaced in synchrony with consecutive arrivals of multiple sonar pulses. We then assess the effect of surfacing and other behavioural response strategies on the received cumulative sound exposure levels and maximum sound pressure levels (SPLs) by modelling realistic spatiotemporal interactions of a pilot whale with an approaching source. Under the propagation conditions of our model, some response strategies observed in the wild were effective in reducing received levels (e.g. movement perpendicular to the source's line of approach), but others were not (e.g. switching from deep to shallow diving; synchronous surfacing after maximum SPLs). Our study exemplifies how simulations of source-whale interactions guided by detailed observational data can improve our understanding about motivations behind behaviour responses observed in the wild (e.g., reducing sound exposure, prey movement).PostprintPeer reviewe

Biological significance of sperm whale responses to sonar: comparison with anti-predator responses

Research funding was provided by the US Office of Naval Research and the Ministries of Defence of Norway, the Netherlands and France as well as the UK Natural Environmental Research Council.A key issue when investigating effects of anthropogenic noise on cetacean behavior is to identify the biological significance of the responses. Predator presence can be considered a natural high-level disturbance stimulus to which prey animals have evolved adaptive response strategies to reduce their risk of predation by altering behavior away from fitness-enhancing activities such as foraging. By contrasting the type and magnitude (duration, severity, consistency) of behavioral responses to anthropogenic noise and playback of killer whale (KW) sounds that simulated predator presence, this study aimed to provide a relative index of the disturbance level as an indication of the biological significance of responses to the anthropogenic stimulus. Using multi-sensor tags as well as visual observations of surface behavior of adult male sperm whales, we assessed a comprehensive range of behavioral metrics that could reduce individuals’ fitness if altered for a biologically relevant duration. Combining previously published results and new analyses, we showed that the responses to 1-2 kHz upsweep naval sonar and to KW playback were very similar, including horizontal avoidance, interruption of foraging or resting activities and an increase in social sound production. However, only KW playbacks elicited grouping behaviors, indicating that this social response component was specific to predator detection. Animals responded to a lesser extent to 6-7 kHz upsweep naval sonar, indicating weaker disturbance effects. Our study demonstrates the benefit of using anti-predator responses as a reference of disturbance when evaluating the relative impacts of anthropogenic stimuli, which can be of particular interest in studies of threatened species such as sperm whales.Publisher PDFPeer reviewe

Lack of behavioural responses of humpback whales (Megaptera novaeangliae) indicate limited effectiveness of sonar mitigation

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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

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

Avoidance responses of minke whales to 1–4 kHz naval sonar

The SOCAL project was funded by the US Navy Chief of Naval Operations Environmental Readiness Division and US Office of Naval Research. The 3S project was funded by the Norwegian Ministry of Defence, the US Office of Naval Research, the Netherlands Ministry of Defence and DGA French Ministry of Defence. The MOCHA project was funded by the US Office of Naval Research. 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.Minke whales are difficult to study and little information exists regarding their responses to anthropogenic sound. This study pools data from behavioural response studies off California and Norway. Data are derived from four tagged animals, of which one from each location was exposed to naval sonar signals. Statistical analyses were conducted using Mahalanobis distance to compare overall changes in parameters summarising dive behaviour, avoidance behaviour, and potential energetic costs of disturbance. Our quantitative analysis showed that both animals initiated avoidance behaviour, but responses were not associated with unusual dive behaviour. In one exposed animal the avoidance of the sonar source included a 5-fold increase in horizontal speed away from the source, implying a significant increase in metabolic rate. Despite the different environmental settings and exposure contexts, clear changes in behaviour were observed providing the first insights into the nature of responses to human noise for this wide-ranging species.PostprintPeer reviewe

Northern bottlenose whales in a pristine environment respond strongly to close and distant navy sonar signals

The research described in this paper was supported by US Office of Naval Research (ONR grants N00014-15-1-2533 and N00014-16-1-3059), US Strategic Environmental Research and Development Program (SERDP award RC-2337), the French Ministry of Defence (DGA) and the Netherlands Ministry of Defence. P.L.T. acknowledges support from the MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland; supported by the Scottish Funding Council, grant reference HR09011, and contributing institutions). All relevant data and scripts are within the paper and its electronic supplementary material, or available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.fc5c0s4Impact assessments for sonar operations typically use received sound levels to predict behavioural disturbance in marine mammals. However, there are indications that cetaceans may learn to associate exposures from distant sound sources with lower perceived risk. To investigate the roles of source distance and received level in an area without frequent sonar activity, we conducted multi-scale controlled exposure experiments (n = 3) with 12 northern bottlenose whales near Jan Mayen, Norway. Animals were tagged with high-resolution archival tags (n = 1 per experiment) or medium-resolution satellite tags (n = 9 in total) and subsequently exposed to sonar. We also deployed bottom-moored recorders to acoustically monitor for whales in the exposed area. Tagged whales initiated avoidance of the sound source over a wide range of distances (0.8–28 km), with responses characteristic of beaked whales. Both onset and intensity of response were better predicted by received sound pressure level (SPL) than by source distance. Avoidance threshold SPLs estimated for each whale ranged from 117–126 dB re 1 µPa, comparable to those of other tagged beaked whales. In this pristine underwater acoustic environment, we found no indication that the source distances tested in our experiments modulated the behavioural effects of sonar, as has been suggested for locations where whales are frequently exposed to sonar.Publisher PDFPeer reviewe

Network impact score is an independent predictor of post-stroke cognitive impairment: A multicenter cohort study in 2341 patients with acute ischemic stroke

BACKGROUND: Post-stroke cognitive impairment (PSCI) is a common consequence of stroke. Accurate prediction of PSCI risk is challenging. The recently developed network impact score, which integrates information on infarct location and size with brain network topology, may improve PSCI risk prediction. AIMS: To determine if the network impact score is an independent predictor of PSCI, and of cognitive recovery or decline. METHODS: We pooled data from patients with acute ischemic stroke from 12 cohorts through the Meta VCI Map consortium. PSCI was defined as impairment in ≥ 1 cognitive domain on neuropsychological examination, or abnormal Montreal Cognitive Assessment. Cognitive recovery was defined as conversion from PSCI 24 months) and cognitive recovery or decline using logistic regression. Models were adjusted for age, sex, education, prior stroke, infarct volume, and study site. RESULTS: We included 2341 patients with 4657 cognitive assessments. PSCI was present in 398/844 patients (47%) 24 months. Cognitive recovery occurred in 64/181 (35%) patients and cognitive decline in 26/287 (9%). The network impact score predicted PSCI in the univariable (OR 1.50, 95%CI 1.34-1.68) and multivariable (OR 1.27, 95%CI 1.10-1.46) GEE model, with similar ORs in the logistic regression models for specified post-stroke intervals. The network impact score was not associated with cognitive recovery or decline. CONCLUSIONS: The network impact score is an independent predictor of PSCI. As such, the network impact score may contribute to a more precise and individualized cognitive prognostication in patients with ischemic stroke. Future studies should address if multimodal prediction models, combining the network impact score with demographics, clinical characteristics and other advanced brain imaging biomarkers, will provide accurate individualized prediction of PSCI. A tool for calculating the network impact score is freely available at https://metavcimap.org/features/software-tools/lsm-viewer/