Prey encounters and spatial memory influence use of foraging patches in a marine central place forager.

Given the patchiness and long-term predictability of marine resources, memory of high-quality foraging grounds is expected to provide fitness advantages for central place foragers. However, it remains challenging to characterize how marine predators integrate memory with recent prey encounters to adjust fine-scale movement and use of foraging patches. Here, we used two months of movement data from harbour seals (Phoca vitulina) to quantify the repeatability in foraging patches as a proxy for memory. We then integrated these data into analyses of fine-scale movement and underwater behaviour to test how both spatial memory and prey encounter rates influenced the seals' area-restricted search (ARS) behaviour. Specifically, we used one month's GPS data from 29 individuals to build spatial memory maps of searched areas and archived accelerometery data from a subset of five individuals to detect prey catch attempts, a proxy for prey encounters. Individuals were highly consistent in the areas they visited over two consecutive months. Hidden Markov models showed that both spatial memory and prey encounters increased the probability of seals initiating ARS. These results provide evidence that predators use memory to adjust their fine-scale movement, and this ability should be accounted for in movement models.

When the human brain goes diving: using near-infrared spectroscopy to measure cerebral and systemic cardiovascular responses to deep, breath-hold diving in elite freedivers.

Continuous measurements of haemodynamic and oxygenation changes in free living animals remain elusive. However, developments in biomedical technologies may help to fill this knowledge gap. One such technology is continuous-wave near-infrared spectroscopy (CW-NIRS)-a wearable and non-invasive optical technology. Here, we develop a marinized CW-NIRS system and deploy it on elite competition freedivers to test its capacity to function during deep freediving to 107 m depth. We use the oxyhaemoglobin and deoxyhaemoglobin concentration changes measured with CW-NIRS to monitor cerebral haemodynamic changes and oxygenation, arterial saturation and heart rate. Furthermore, using concentration changes in oxyhaemoglobin engendered by cardiac pulsation, we demonstrate the ability to conduct additional feature exploration of cardiac-dependent haemodynamic changes. Freedivers showed cerebral haemodynamic changes characteristic of apnoeic diving, while some divers also showed considerable elevations in venous blood volumes close to the end of diving. Some freedivers also showed pronounced arterial deoxygenation, the most extreme of which resulted in an arterial saturation of 25%. Freedivers also displayed heart rate changes that were comparable to diving mammals both in magnitude and patterns of change. Finally, changes in cardiac waveform associated with heart rates less than 40 bpm were associated with changes indicative of a reduction in vascular compliance. The success here of CW-NIRS to non-invasively measure a suite of physiological phenomenon in a deep-diving mammal highlights its efficacy as a future physiological monitoring tool for human freedivers as well as free living animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

Shining new light on sensory brain activation and physiological measurement in seals using wearable optical technology.

Sensory ecology and physiology of free-ranging animals is challenging to study but underpins our understanding of decision-making in the wild. Existing non-invasive human biomedical technology offers tools that could be harnessed to address these challenges. Functional near-infrared spectroscopy (fNIRS), a wearable, non-invasive biomedical imaging technique measures oxy- and deoxyhaemoglobin concentration changes that can be used to detect localized neural activation in the brain. We tested the efficacy of fNIRS to detect cortical activation in grey seals (Halichoerus grypus) and identify regions of the cortex associated with different senses (vision, hearing and touch). The activation of specific cerebral areas in seals was detected by fNIRS in responses to light (vision), sound (hearing) and whisker stimulation (touch). Physiological parameters, including heart and breathing rate, were also extracted from the fNIRS signal, which allowed neural and physiological responses to be monitored simultaneously. This is, to our knowledge, the first time fNIRS has been used to detect cortical activation in a non-domesticated or laboratory animal. Because fNIRS is non-invasive and wearable, this study demonstrates its potential as a tool to quantitatively investigate sensory perception and brain function while simultaneously recording heart rate, tissue and arterial oxygen saturation of haemoglobin, perfusion changes and breathing rate in free-ranging animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Estimating the effects of pile driving sounds on seals: Pitfalls and possibilities.

Understanding the potential effects of pile driving sounds on marine wildlife is essential for regulating offshore wind developments. Here, tracking data from 24 harbour seals were used to quantify effects and investigate sensitivity to the methods used to predict these. The Aquarius pile driving model was used to model source characteristics and acoustic propagation loss (16 Hz-20 kHz). Predicted cumulative sound exposure levels (SELcums) experienced by each seal were compared to different auditory weighting functions and damage thresholds to estimate temporary (TTS) and permanent (PTS) threshold shift occurrence. Each approach produced markedly different results; however, the most recent criteria established by Southall et al. [(2019) Aquat. Mamm. 45, 125-232] suggests that TTS occurrence was low (17% of seals). Predictions of seal density during pile driving made by Russell et al. [(2016) J. Appl. Ecol. 53, 1642-1652] were compared to distance from the wind farm and predicted single-strike sound exposure levels (SELss) by multiple approaches. Predicted seal density significantly decreased within 25 km or above SELss (averaged across depths and pile installations) of 145 dB re 1 µPa2⋅s. However, there was substantial variation in SELss with depth and installation, and thus in the predicted relationship with seal density. These results highlight uncertainty in estimated effects, which should be considered in future assessments.

Physiological constraints and energetic costs of diving behaviour in marine mammals: a review of studies using trained Steller sea lions diving in the open ocean.

Marine mammals are characterized as having physiological specializations that maximize the use of oxygen stores to prolong time spent under water. However, it has been difficult to undertake the requisite controlled studies to determine the physiological limitations and trade-offs that marine mammals face while diving in the wild under varying environmental and nutritional conditions. For the past decade, Steller sea lions (Eumetopias jubatus) trained to swim and dive in the open ocean away from the physical confines of pools participated in studies that investigated the interactions between diving behaviour, energetic costs, physiological constraints, and prey availability. Many of these studies measured the cost of diving to understand how it varies with behaviour and environmental and physiological conditions. Collectively, these studies show that the type of diving (dive bouts or single dives), the level of underwater activity, the depth and duration of dives, and the nutritional status and physical condition of the animal affect the cost of diving and foraging. They show that dive depth, dive and surface duration, and the type of dive result in physiological adjustments (heart rate, gas exchange) that may be independent of energy expenditure. They also demonstrate that changes in prey abundance and nutritional status cause sea lions to alter the balance between time spent at the surface acquiring oxygen (and offloading CO2 and other metabolic by-products) and time spent at depth acquiring prey. These new insights into the physiological basis of diving behaviour further our understanding of the potential scope for behavioural responses of marine mammals to environmental changes, the energetic significance of these adjustments, and the consequences of approaching physiological limits.

Avoidance of wind farms by harbour seals is limited to pile driving activities.

As part of global efforts to reduce dependence on carbon-based energy sources there has been a rapid increase in the installation of renewable energy devices. The installation and operation of these devices can result in conflicts with wildlife. In the marine environment, mammals may avoid wind farms that are under construction or operating. Such avoidance may lead to more time spent travelling or displacement from key habitats. A paucity of data on at-sea movements of marine mammals around wind farms limits our understanding of the nature of their potential impacts.Here, we present the results of a telemetry study on harbour seals Phoca vitulina in The Wash, south-east England, an area where wind farms are being constructed using impact pile driving. We investigated whether seals avoid wind farms during operation, construction in its entirety, or during piling activity. The study was carried out using historical telemetry data collected prior to any wind farm development and telemetry data collected in 2012 during the construction of one wind farm and the operation of another.Within an operational wind farm, there was a close-to-significant increase in seal usage compared to prior to wind farm development. However, the wind farm was at the edge of a large area of increased usage, so the presence of the wind farm was unlikely to be the cause.There was no significant displacement during construction as a whole. However, during piling, seal usage (abundance) was significantly reduced up to 25 km from the piling activity; within 25 km of the centre of the wind farm, there was a 19 to 83% (95% confidence intervals) decrease in usage compared to during breaks in piling, equating to a mean estimated displacement of 440 individuals. This amounts to significant displacement starting from predicted received levels of between 166 and 178 dB re 1 µPa(p-p). Displacement was limited to piling activity; within 2 h of cessation of pile driving, seals were distributed as per the non-piling scenario. Synthesis and applications. Our spatial and temporal quantification of avoidance of wind farms by harbour seals is critical to reduce uncertainty and increase robustness in environmental impact assessments of future developments. Specifically, the results will allow policymakers to produce industry guidance on the likelihood of displacement of seals in response to pile driving; the relationship between sound levels and avoidance rates; and the duration of any avoidance, thus allowing far more accurate environmental assessments to be carried out during the consenting process. Further, our results can be used to inform mitigation strategies in terms of both the sound levels likely to cause displacement and what temporal patterns of piling would minimize the magnitude of the energetic impacts of displacement.

Dynamic habitat corridors for marine predators; intensive use of a coastal channel by harbour seals is modulated by tidal currents.

ABSTRACT: Previous studies have found that predators utilise habitat corridors to ambush prey moving through them. In the marine environment, coastal channels effectively act as habitat corridors for prey movements, and sightings of predators in such areas suggest that they may target these for foraging. Unlike terrestrial systems where the underlying habitat structure is generally static, corridors in marine systems are in episodic flux due to water movements created by tidal processes. Although these hydrographic features can be highly complex, there is generally a predictable underlying cyclic tidal pattern to their structure. For marine predators that must find prey that is often patchy and widely distributed, the underlying temporal predictability in potential foraging opportunities in marine corridors may be important drivers in their use. Here, we used data from land-based sightings and 19 harbour seals (Phoca vitulina) tagged with high-resolution GPS telemetry to investigate the spatial and temporal distribution patterns of seals in a narrow tidal channel. These seals showed a striking pattern in their distribution; all seals spent a high proportion of their time around the narrowest point of the channel. There was also a distinctive tidal pattern in the use of the channel; sightings of seals in the water peaked during the flood tide and were at a minimum during the ebb tide. This pattern is likely to be related to prey availability and/or foraging efficiency driven by the underlying tidal pattern in the water movements through the channel. SIGNIFICANCE STATEMENT: To maximise foraging efficiency, predators often make use of narrow constrictions in habitat to intercept prey using these corridors for movement. In the marine environment, narrow channels may act as corridors, and sightings of predators suggest that they may target these for foraging. Despite this, there is little information on how individual predators use such areas. Here, we investigate how individual harbour seals use a narrow coastal channel subject to strong tidal currents; results showed that seals spent the majority of their time at the narrowest point of the channel foraging during peak tidal currents. This highlights the importance of narrow channels for marine predators and suggests that this usually wide-ranging predator may restrict its geographic range to forage in the channel as a result of increased prey availability and/or foraging efficiency driven by water movements through the narrow corridor.

Aerial low-frequency hearing in captive and free-ranging harbour seals (Phoca vitulina) measured using auditory brainstem responses.

The hearing sensitivity of 18 free-ranging and 10 captive harbour seals (Phoca vitulina) to aerial sounds was measured in the presence of typical environmental noise through auditory brainstem response measurements. A focus was put on the comparative hearing sensitivity at low frequencies. Low- and mid-frequency thresholds appeared to be elevated in both captive and free-ranging seals, but this is likely due to masking effects and limitations of the methodology used. The data also showed individual variability in hearing sensitivity with probable age-related hearing loss found in two old harbour seals. These results suggest that the acoustic sensitivity of free-ranging animals was not negatively affected by the soundscape they experienced in the wild.

Multiple-Pulse Sounds and Seals: Results of a Harbor Seal (Phoca vitulina) Telemetry Study During Wind Farm Construction.

Offshore construction and survey techniques can produce pulsed sounds with a high sound pressure level. In coastal waters, the areas in which they are produced are often also used by seals, potentially resulting in auditory damage or behavioral avoidance. Here, we describe a study on harbor seals during a wind farm installation off southeast England. The study used GPS/global system for mobile communication tags on 23 harbor seals that provided distribution and activity data; the closest range of individual seals to piling varied from 6.65 to 46.1 km. Furthermore, the maximum predicted received levels (RLs) at individual seals varied between 146.9 and 169.4 dB re 1 µPa peak to peak.

Behavioral responses by grey seals (Halichoerus grypus) to high frequency sonar.

The use of high frequency sonar is now commonplace in the marine environment. Most marine mammals rely on sound to navigate, and for detecting prey, and there is the potential that the acoustic signals of sonar could cause behavioral responses. To investigate this, we carried out behavioral response tests with grey seals to two sonar systems (200 and 375 kHz systems). Results showed that both systems had significant effects on the seals behavior; when the 200 kHz sonar was active, seals spent significantly more time hauled out and, although seals remained swimming during operation of the 375 kHz sonar, they were distributed further from the sonar. The results show that although peak sonar frequencies may be above marine mammal hearing ranges, high levels of sound can be produced within their hearing ranges that elicit behavioral responses; this has clear implications for the widespread use of sonar in the marine environment.