Estimating the risks of exposure to harmful algal toxins among Scottish harbour seals.

Harmful algal bloom (HAB) toxins consumed by marine predators through fish prey can be lethal but studies on the resulting population consequences are lacking. Over the past approximately 20 years there have been large regional declines in some harbour seal populations around Scotland. Analyses of excreta (faeces and urine from live and dead seals and faecal samples from seal haulout sites) suggest widespread exposure to toxins through the ingestion of contaminated prey. A risk assessment model, incorporating concentrations of the two major HAB toxins found in seal prey around Scotland (domoic acid (DA), and saxitoxins (STX)), the seasonal persistence of the toxins in the fish and the foraging patterns of harbour seals were used to estimate the proportion of adults and juveniles likely to have ingested doses above various estimated toxicity thresholds. The results were highly dependent on toxin type, persistence, and foraging regime as well as age class, all of which affected the proportion of exposed animals exceeding toxicity thresholds. In this preliminary model STX exposure was unlikely to result in mortalities. Modelled DA exposure resulted in doses above an estimated lethal threshold of 1900 µg/kg body mass affecting up to 3.8 % of exposed juveniles and 5.3 % of exposed adults. Given the uncertainty in the model parameters and the limitations of the data these conclusions should be treated with caution, but they indicate that DA remains a potential factor involved in the regional declines of harbour seals. Similar risks may be experienced by other top predators, including small cetaceans and seabirds that feed on similar prey in Scottish waters.

Toxins from harmful algae in fish from Scottish coastal waters.

Harmful algal bloom events are increasing in a number of water bodies around the world with significant economic impacts on the aquaculture, fishing and tourism industries. As well as their potential impacts on human health, toxin exposure from harmful algal blooms (HABs) has resulted in widespread morbidity and mortality in marine life, including top marine predators. There is therefore a need for an improved understanding of the trophic transfer, and persistence of toxins in marine food webs. For the first time, the concentrations of two toxin groups of commercial and environmental importance, domoic acid (DA) and saxitoxin (including Paralytic Shellfish Toxin (PST) analogues), were measured in the viscera of 40 different fish species caught in Scotland between February and November, 2012 to 2019. Overall, fish had higher concentrations of DA compared to PSTs, with a peak in the summer / autumn months. Whole fish concentrations were highest in pelagic species including Atlantic mackerel and herring, key forage fish for marine predators including seals, cetaceans and seabirds. The highest DA concentrations were measured along the east coast of Scotland and in Orkney. PSTs showed highest concentrations in early summer, consistent with phytoplankton bloom timings. The detection of multiple toxins in such a range of demersal, pelagic and benthic fish prey species suggests that both the fish, and by extension, piscivorous marine predators, experience multiple routes of toxin exposure. Risk assessment models to understand the impacts of exposure to HAB toxins on marine predators therefore need to consider how chronic, low-dose exposure to multiple toxins, as well as acute exposure during a bloom, could lead to potential long-term health effects ultimately contributing to mortalities. The potential synergistic, neurotoxic and physiological effects of long-term exposure to multiple toxins require investigation in order to appropriately assess the risks of HAB toxins to fish as well as their predators.

Classifying grey seal behaviour in relation to environmental variability and commercial fishing activity - a multivariate hidden Markov model.

Classifying movement behaviour of marine predators in relation to anthropogenic activity and environmental conditions is important to guide marine conservation. We studied the relationship between grey seal (Halichoerus grypus) behaviour and environmental variability in the southwestern Baltic Sea where seal-fishery conflicts are increasing. We used multiple environmental covariates and proximity to active fishing nets within a multivariate hidden Markov model (HMM) to quantify changes in movement behaviour of grey seals while at sea. Dive depth, dive duration, surface duration, horizontal displacement, and turning angle were used to identify travelling, resting and foraging states. The likelihood of seals foraging increased in deeper, colder, more saline waters, which are sites with increased primary productivity and possibly prey densities. Proximity to active fishing net also had a pronounced effect on state occupancy. The probability of seals foraging was highest <5 km from active fishing nets (51%) and decreased as distance to nets increased. However, seals used sites <5 km from active fishing nets only 3% of their time at sea highlighting an important temporal dimension in seal-fishery interactions. By coupling high-resolution oceanographic, fisheries, and grey seal movement data, our study provides a scientific basis for designing management strategies that satisfy ecological and socioeconomic demands on marine ecosystems.

Empirical measures of harbor seal behavior and avoidance of an operational tidal turbine.

There is global interest in marine renewable energy from underwater tidal turbines. Due to overlap in animal habitat with locations for tidal turbines, the potential for collisions has led to concern around strike risk. Using data from tagged harbor seals collected before construction and after operation of the SeaGen tidal turbine in Northern Ireland, this study quantifies risks of an operational turbine to harbor seals by taking into account turbine characteristics, tidal state, and seal behavior. We found 68% spatial avoidance (95% C.I., 37%, 83%) by harbor seals within 200 m of the turbine. When additionally accounting for variation in seal occupancy over depth and tidal flows, there is an overall reduction in collision risk from 1.29 to 0.125 seals per tidal cycle (90.3% reduction; (95% C.I., 83%, 98%)) compared to risk calculated under assumptions of uniform habitat use. This demonstrates the need to incorporate environmental conditions to properly assess strike risk.

Predicting global killer whale population collapse from PCB pollution.

Killer whales (Orcinus orca) are among the most highly polychlorinated biphenyl (PCB)-contaminated mammals in the world, raising concern about the health consequences of current PCB exposures. Using an individual-based model framework and globally available data on PCB concentrations in killer whale tissues, we show that PCB-mediated effects on reproduction and immune function threaten the long-term viability of >50% of the world's killer whale populations. PCB-mediated effects over the coming 100 years predicted that killer whale populations near industrialized regions, and those feeding at high trophic levels regardless of location, are at high risk of population collapse. Despite a near-global ban of PCBs more than 30 years ago, the world's killer whales illustrate the troubling persistence of this chemical class.

Predicting the effects of polychlorinated biphenyls on cetacean populations through impacts on immunity and calf survival.

The potential impact of exposure to polychlorinated biphenyls (PCBs) on the health and survival of cetaceans continues to be an issue for conservation and management, yet few quantitative approaches for estimating population level effects have been developed. An individual based model (IBM) for assessing effects on both calf survival and immunity was developed and tested. Three case study species (bottlenose dolphin, humpback whale and killer whale) in four populations were taken as examples and the impact of varying levels of PCB uptake on achievable population growth was assessed. The unique aspect of the model is its ability to evaluate likely effects of immunosuppression in addition to calf survival, enabling consequences of PCB exposure on immune function on all age-classes to be explored. By incorporating quantitative tissue concentration-response functions from laboratory animal model species into an IBM framework, population trajectories were generated. Model outputs included estimated concentrations of PCBs in the blubber of females by age, which were then compared to published empirical data. Achievable population growth rates were more affected by the inclusion of effects of PCBs on immunity than on calf survival, but the magnitude depended on the virulence of any subsequent encounter with a pathogen and the proportion of the population exposed. Since the starting population parameters were from historic studies, which may already be impacted by PCBs, the results should be interpreted on a relative rather than an absolute basis. The framework will assist in providing quantitative risk assessments for populations of concern.

Fine-scale harbour seal usage for informed marine spatial planning.

High-resolution distribution maps can help inform conservation measures for protected species; including where any impacts of proposed commercial developments overlap the range of focal species. Around Orkney, northern Scotland, UK, the harbour seal (Phoca vitulina) population has decreased by 78% over 20 years. Concern for the declining harbour seal population has led to constraints being placed on tidal energy generation developments. For this study area, telemetry data from 54 animals tagged between 2003 and 2015 were used to produce density estimation maps. Predictive habitat models using GAM-GEEs provided robust predictions in areas where telemetry data were absent, and were combined with density estimation maps, and then scaled to population levels using August terrestrial counts between 2008 and 2015, to produce harbour seal usage maps with confidence intervals around Orkney and the North coast of Scotland. The selected habitat model showed that distance from haul out, proportion of sand in seabed sediment, and annual mean power were important predictors of space use. Fine-scale usage maps can be used in consenting and licensing of anthropogenic developments to determine local abundance. When quantifying commercial impacts through changes to species distributions, usage maps can be spatially explicitly linked to individual-based models to inform predicted movement and behaviour.

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.

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.

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.

The intensity of horizontal and vertical search in a diving forager: the harbour seal.

BACKGROUND: Free ranging foraging animals can vary their searching intensity in response to the profitability of the environment by modifying their movements. Marine diving animals forage in a three dimensional space and searching intensity can be varied in both the horizontal and vertical planes. Therefore understanding the relationship between the allocation of searching effort in these two spaces can provide a better understanding of searching strategies and a more robust identification of foraging behaviour from the multitude of foraging indices (FIs) available. We investigated the movement of a widespread marine coastal predator, the harbour seal (Phoca vitulina), and compared two sets of foraging indices reflecting searching intensity respectively in the horizontal plane (displacement speed, extensive vs. intensive movement types, residence time) and in the vertical dimension (time at the bottom of a dive). We then tested how several factors (dive depth, direction of the trip with respect to haul-out site, different predatory tactics, the presence of factors confounding the detection of foraging, and temporal resolution of the data) affected their relationships. RESULTS: Overall the indices only showed a very weak positive correlation across the two spaces. However controlling for various factors strengthened the relationships. Resting at sea, a behaviour intrinsically static in the horizontal plane, was found to be strongly negatively related to the time spent at the bottom of the dives, indirectly weakening the relationship between horizontal and vertical foraging indices. Predatory tactic (benthic vs. pelagic) was found to directly affect the relationship. In benthic (as opposed to pelagic) foraging a stronger positive relationship was found between vertical and horizontal indices. CONCLUSIONS: Our results indicated that movement responses, leading to an intensification of search, are similar in the two spaces (positive relationship), but additional factors need to be taken into account for this relationship to emerge. Foraging indices measuring residence in the horizontal plane tend to be inflated by resting events at sea, while vertical indices tend to distinguish mainly between periods of activity and inactivity, or of benthic and pelagic foraging. The simultaneous consideration of horizontal and vertical movements, as well as topographic information, allows additional behavioural states to be inferred, providing greater insight into the interpretation of foraging activity.

Using GPS data to evaluate the accuracy of state-space methods for correction of Argos satellite telemetry error.

Recent studies have applied state-space models to satellite telemetry data in order to remove noise from raw location estimates and infer the true tracks of animals. However, while the resulting tracks may appear plausible, it is difficult to determine the accuracy of the estimated positions, especially for position estimates interpolated to times between satellite locations. In this study, we use data from two gray seals (Halichoerus grypus) carrying tags that transmitted Fastloc GPS positions via Argos satellites. This combination of Service Argos data and highly accurate GPS data allowed examination of the accuracy of state-space position estimates and their uncertainty derived from satellite telemetry data. After applying a speed filter to remove aberrant satellite telemetry locations, we fit a continuous-time Kalman filter to estimate the parameters of a random walk, used Kalman smoothing to infer positions at the times of the GPS measurements, and then compared the filtered telemetry estimates with the actual GPS measurements. We investigated the effect of varying maximum speed thresholds in the speed-filtering algorithm on the root mean-square error (RMSE) estimates and used minimum RMSE as a criterion to guide the final choice of speed threshold. The optimal speed thresholds differed between the two animals (1.1 m/s and 2.5 m/s) and retained 50% and 65% of the data for each seal. However, using a speed filter of 1.1 m/s resulted in very similar RMSE for both animals. For the two seals, the RMSE of the Kalman-filtered estimates of location were 5.9 and 12.76 km, respectively, and 75% of the modeled positions had errors less than 6.25 km and 11.7 km for each seal. Confidence interval coverage was close to correct at typical levels (80-95%), although it tended to be overly generous at smaller sizes. The reliability of uncertainty estimates was also affected by the chosen speed threshold. The combination of speed and Kalman filtering allows for effective calculation of location and also indicates the limits of accuracy when correcting service Argos locations and linking satellite telemetry data to spatial covariate and habitat data.

Exposure to persistent organic pollutants and first-year survival probability in gray seal pups.

Many studies have demonstrated that persistent organic pollutants are transferred from mother to pup during lactation in phocid seals, but none have been able to determine the significance of these findings for survivorship. The aim of this study was to investigate the relationship between blubber contaminant concentrations and first-year survival in gray seal pups. A mark-recapture framework was used to estimate survival probabilities and animals were "marked" using novel mobile phone tags. Individual and group covariates (sex, condition, and blubber contaminants) were embedded within a live-resighting model. The most significant covariates remained condition at weaning and sex (males in poor condition had the lowest survival probability), as was found previously, but there was also evidence indicating that higher blubber contaminants additionally decreased survivorship. The models' Akaike's Information Criteria (AICs) and their associated weights, point toward the tetrapolybrominated diphenyl ether congeners (dominated by BDE-47) as being the most important group of contaminants affecting survival probability, followed by the total dichlorodiphenyltrichloroethanes (DDTs) and pentapolychlorinated biphenyl congeners. These compounds were not the most abundant in the blubber, suggesting further studies into their toxicological effects in this species are necessary. The specific mechanisms driving the reduction in survivorship remain unknown.

Individual-based model framework to assess population consequences of polychlorinated biphenyl exposure in bottlenose dolphins.

Marine mammals are susceptible to the effects of anthropogenic contaminants. Here we examine the effect of different polychlorinated biphenyl (PCB) accumulation scenarios on potential population growth rates using, as an example, data obtained for the population of bottlenose dolphins from Sarasota Bay, Florida. To achieve this goal, we developed an individual-based model framework that simulates the accumulation of PCBs in the population and modifies first-year calf survival based on maternal blubber PCB levels. In our example the current estimated annual PCB accumulation rate for the Sarasota Bay dolphin population might be depressing the potential population growth rate. However, our predictions are limited both by model naivety and parameter uncertainty. We emphasize the need for more data collection on the relationship between maternal blubber PCB levels and calf survivorship, the annual accumulation of PCBs in the blubber of females, and the transfer of PCBs to the calf through the placenta and during lactation. Such data require continued efforts directed toward long-term studies of known individuals in wild and semiwild populations.

Blubber and buoyancy: monitoring the body condition of free-ranging seals using simple dive characteristics.

Elephant seals regularly perform dives during which they spend a large proportion of time drifting passively through the water column. The rate of vertical change in depth during these "drift" dives is largely a result of the proportion of lipid tissue in the body, with fatter seals having higher (more positive or less negative) drift rates compared with leaner seals. We examined the temporal changes in drift rates of 24 newly weaned southern elephant seal (Mirounga leonina) pups during their first trip to sea to determine if this easily recorded dive characteristic can be used to continuously monitor changes in body composition of seals throughout their foraging trips. All seals demonstrated a similar trend over time: drift rates were initially positive but decreased steadily over the first 30-50 days after departure (Phase 1), corresponding to seals becoming gradually less buoyant. Over the following approximately 100 days (Phase 2), drift rates again increased gradually, while during the last approximately 20-45 days (Phase 3) drift rates either remained constant or decreased slightly. The daily rate of change in drift rate was negatively related to the daily rate of horizontal displacement (daily travel rate), and daily travel rates of more than approximately 80 km were almost exclusively associated with negative changes in drift rate. We developed a mechanistic model based on body compositions and morphometrics measured in the field, published values for the density of seawater and various body components, and values of drag coefficients for objects of different shapes. We used this model to examine the theoretical relationships between drift rate and body composition and carried out a sensitivity analysis to quantify errors and biases caused by varying model parameters. While variations in seawater density and uncertainties in estimated body surface area and volume are unlikely to result in errors in estimated lipid content of more than +/-2.5%, variations in drag coefficient can lead to errors of >or =10%. Finally, we compared the lipid contents predicted by our model with the lipid contents measured using isotopically labelled water and found a strong positive correlation. The best-fitting model suggests that the drag coefficient of seals while drifting passively is between approximately 0.49 (roughly corresponding to a sphere-shaped object) and 0.69 (a prolate spheroid), and we were able to estimate relative lipid content to within approximately +/-2% lipid. Our results suggest that this simple method can be used to estimate the changes in lipid content of free-ranging seals while at sea and may help improve our understanding of the foraging strategies of these important marine predators.

Overcoming the constraints of long range radio telemetry from animals: getting more useful data from smaller packages.

Many species carry out their most interesting activities where they cannot readily be observed or monitored. Marine mammals are extreme among this group, accomplishing their most astounding activities both distant from land and deep in the sea. Collection, storage and transmission of data about these activities are constrained by the energy requirements and size of the recording loggers and transmitters. The more bits of information collected, stored and transmitted, the more battery is required and the larger the tag must be. We therefore need to be selective about the information we collect, while maintaining detail and fidelity. To accomplish this in the study of marine mammals, we have designed "intelligent" data logger/transmitters that provide context-driven data compression, data relay, and automated data base storage. We later combine these data with remotely sensed environmental information and other oceanographic data sets to recreate the environmental context for the animal's activity, and we display the combined data using computer animation techniques. In this way, the system can provide near real time "observation" of animal behavior and physiology from the remotest parts of the globe.