Multi-decadal trends in biomarkers in harp seal teeth from the North Atlantic reveal the influence of prey availability on seal trophic position.

Arctic food webs are being impacted by borealisation and environmental change. To quantify the impact of these multiple forcings, it is crucial to accurately determine the temporal change in key ecosystem metrics, such as trophic position of top predators. Here, we measured stable nitrogen isotopes (δ15 N) in amino acids in harp seal teeth from across the North Atlantic spanning a period of 60 years to robustly assess multi-decadal trends in harp seal trophic position, accounting for changes in δ15 N at the base of the food web. We reveal long-term variations in trophic position of harp seals which are likely to reflect fluctuations in prey availability, specifically fish- or invertebrate-dominated diets. We show that the temporal trends in harp seal trophic position differ between the Northwest Atlantic, Greenland Sea and Barents Sea, suggesting divergent changes in each local ecosystem. Our results provide invaluable data for population dynamic and ecotoxicology studies.

Understanding spatial effects in species distribution models.

Species Distribution Models often include spatial effects which may improve prediction at unsampled locations and reduce Type I errors when identifying environmental drivers. In some cases ecologists try to ecologically interpret the spatial patterns displayed by the spatial effect. However, spatial autocorrelation may be driven by many different unaccounted drivers, which complicates the ecological interpretation of fitted spatial effects. This study aims to provide a practical demonstration that spatial effects are able to smooth the effect of multiple unaccounted drivers. To do so we use a simulation study that fit model-based spatial models using both geostatistics and 2D smoothing splines. Results show that fitted spatial effects resemble the sum of the unaccounted covariate surface(s) in each model.

Estimating energetic intake for marine mammal bioenergetic models.

Bioenergetics is the study of how animals achieve energetic balance. Energetic balance results from the energetic expenditure of an individual and the energy they extract from their environment. Ingested energy depends on several extrinsic (e.g prey species, nutritional value and composition, prey density and availability) and intrinsic factors (e.g. foraging effort, success at catching prey, digestive processes and associated energy losses, and digestive capacity). While the focus in bioenergetic modelling is often on the energetic costs an animal incurs, the robust estimation of an individual's energy intake is equally critical for producing meaningful predictions. Here, we review the components and processes that affect energy intake from ingested gross energy to biologically useful net energy (NE). The current state of knowledge of each parameter is reviewed, shedding light on research gaps to advance this field. The review highlighted that the foraging behaviour of many marine mammals is relatively well studied via biologging tags, with estimates of success rate typically assumed for most species. However, actual prey capture success rates are often only assumed, although we note studies that provide approaches for its estimation using current techniques. A comprehensive collation of the nutritional content of marine mammal prey species revealed a robust foundation from which prey quality (comprising prey species, size and energy density) can be assessed, though data remain unavailable for many prey species. Empirical information on various energy losses following ingestion of prey was unbalanced among marine mammal species, with considerably more literature available for pinnipeds. An increased understanding and accurate estimate of each of the components that comprise a species NE intake are an integral part of bioenergetics. Such models provide a key tool to investigate the effects of disturbance on marine mammals at an individual and population level and to support effective conservation and management.

Benthic animal-borne sensors and citizen science combine to validate ocean modelling.

Developments in animal electronic tagging and tracking have transformed the field of movement ecology, but interest is also growing in the contributions of tagged animals to oceanography. Animal-borne sensors can address data gaps, improve ocean model skill and support model validation, but previous studies in this area have focused almost exclusively on satellite-telemetered seabirds and seals. Here, for the first time, we develop the use of benthic species as animal oceanographers by combining archival (depth and temperature) data from animal-borne tags, passive acoustic telemetry and citizen-science mark-recapture records from 2016-17 for the Critically Endangered flapper skate (Dipturus intermedius) in Scotland. By comparing temperature observations to predictions from the West Scotland Coastal Ocean Modelling System, we quantify model skill and empirically validate an independent model update. The results from bottom-temperature and temperature-depth profile validation (5,324 observations) fill a key data gap in Scotland. For predictions in 2016, we identified a consistent warm bias (mean = 0.53 °C) but a subsequent model update reduced bias by an estimated 109% and improved model skill. This study uniquely demonstrates the use of benthic animal-borne sensors and citizen-science data for ocean model validation, broadening the range of animal oceanographers in aquatic environments.

Environmental drivers of population-level variation in the migratory and diving ontogeny of an Arctic top predator.

The development of migratory strategies that enable juveniles to survive to sexual maturity is critical for species that exploit seasonal niches. For animals that forage via breath-hold diving, this requires a combination of both physiological and foraging skill development. Here, we assess how migratory and dive behaviour develop over the first year of life for a migratory Arctic top predator, the harp seal Pagophilus groenlandicus, tracked using animal-borne satellite relay data loggers. We reveal similarities in migratory movements and differences in diving behaviour between 38 juveniles tracked from the Greenland Sea and Northwest Atlantic breeding populations. In both regions, periods of resident and transitory behaviour during migration were associated with proxies for food availability: sea ice concentration and bathymetric depth. However, while ontogenetic development of dive behaviour was similar for both populations of juveniles over the first 25 days, after this time Greenland Sea animals performed shorter and shallower dives and were more closely associated with sea ice than Northwest Atlantic animals. Together, these results highlight the role of both intrinsic and extrinsic factors in shaping early life behaviour. Variation in the environmental conditions experienced during early life may shape how different populations respond to the rapid changes occurring in the Arctic ocean ecosystem.

Multi-decadal environmental change in the Barents Sea recorded by seal teeth.

Multiple environmental forcings, such as warming and changes in ocean circulation and nutrient supply, are affecting the base of Arctic marine ecosystems, with cascading effects on the entire food web through bottom-up control. Stable nitrogen isotopes (δ15 N) can be used to detect and unravel the impact of these forcings on this unique ecosystem, if the many processes that affect the δ15 N values are constrained. Combining unique 60-year records from compound specific δ15 N biomarkers on harp seal teeth alongside state-of-the-art ocean modelling, we observed a significant decline in the δ15 N values at the base of the Barents Sea food web from 1951 to 2012. This strong and persistent decadal trend emerges due to the combination of anthropogenic atmospheric nitrogen deposition in the Atlantic, increased northward transport of Atlantic water through Arctic gateways and local feedbacks from increasing Arctic primary production. Our results suggest that the Arctic ecosystem has been responding to anthropogenically induced local and remote drivers, linked to changing ocean biology, chemistry and physics, for at least 60 years. Accounting for these trends in δ15 N values at the base of the food web is essential to accurately detect ecosystem restructuring in this rapidly changing environment.

Integrating disparate datasets to model the functional response of a marine predator: A case study of harbour porpoises in the southern North Sea.

Quantifying consumption and prey choice for marine predator species is key to understanding their interaction with prey species, fisheries, and the ecosystem as a whole. However, parameterizing a functional response for large predators can be challenging because of the difficulty in obtaining the required data on predator diet and on the availability of multiple prey species.This study modeled a multi-species functional response (MSFR) to describe the relationship between consumption by harbour porpoises (Phocoena phocoena) and the availability of multiple prey species in the southern North Sea. Bayesian methodology was employed to estimate MSFR parameters and to incorporate uncertainties in diet and prey availability estimates. Prey consumption was estimated from stomach content data from stranded harbour porpoises. Prey availability to harbour porpoises was estimated based on the spatial overlap between prey distributions, estimated from fish survey data, and porpoise foraging range in the days prior to stranding predicted from telemetry data.Results indicated a preference for sandeels in the study area. Prey switching behavior (change in preference dependent on prey abundance) was confirmed by the favored type III functional response model. Variation in the size of the foraging range (estimated area where harbour porpoises could have foraged prior to stranding) did not alter the overall pattern of the results or conclusions.Integrating datasets on prey consumption from strandings, predator foraging distribution using telemetry, and prey availability from fish surveys into the modeling approach provides a methodological framework that may be appropriate for fitting MSFRs for other predators.

Environment-sensitive mass changes influence breeding frequency in a capital breeding marine top predator.

The trade-off between survival and reproduction in resource-limited iteroparous animals can result in some individuals missing some breeding opportunities. In practice, even with the best observation regimes, deciding whether 'missed' years represent real pauses in breeding or failures to detect breeding can be difficult, posing problems for the estimation of individual reproductive output and overall population fecundity. We corrected fecundity estimates by determining whether breeding had occurred in skipped years, using long-term capture-recapture observation datasets with parallel longitudinal mass measurements, based on informative underlying relationships between individuals' mass, breeding status and environmental drivers in a capital breeding phocid, the grey seal. Bayesian modelling considered interacting processes jointly: temporal changes in a phenotypic covariate (mass); relationship of mass to breeding probability; effects of maternal breeding state and mark type on resighting. Full reproductive histories were imputed, with the status of unobserved animals estimated as breeding or non-breeding, accounting for local environmental variation. Overall fecundity was then derived for Scottish breeding colonies with contrasting pup production trends. Maternal mass affected breeding likelihood. Mothers with low body mass at the end of breeding were less likely to bear a pup the following year. Successive breeding episodes incurred a cost in reduced body mass which was more pronounced for North Rona, Outer Hebrides (NR) mothers. Skipping breeding increased subsequent pupping probability substantially for low mass females. Poor environmental conditions were associated with declines in breeding probability at both colonies. Seal mass gain between breeding seasons was (a) negatively associated with lagged North Atlantic Oscillation for seals at NR and (b) positively associated with an index of seal prey (Ammodytes spp) abundance at Isle of May, Firth of Forth (IM). Overall fecundity was marginally greater at IM (increasing/stable pup production) than at NR (decreasing). No effects of mass were detected on maternal survival. Skipping breeding in female grey seals appears to be an individual mass-dependent constraint moderated by previous reproductive output and local environmental conditions. Different demographic trends at breeding colonies were consistent with the fecundities estimated using this method, which is general and adaptable to other situations.

Identifying fishing grounds from vessel tracks: model-based inference for small scale fisheries.

Recent technological developments facilitate the collection of location data from fishing vessels at an increasing rate. The development of low-cost electronic systems allows tracking of small-scale fishing vessels, a sector of fishing fleets typically characterized by many, relatively small vessels. The imminent production of large spatial datasets for this previously data-poor sector creates a challenge in terms of data analysis. Several methods have been used to infer the spatial distribution of fishing activities from positional data. Here, we compare five approaches using either vessel speed, or speed and turning angle, to infer fishing activity in the Scottish inshore fleet. We assess the performance of each approach using observational records of true vessel activity. Although results are similar across methods, a trip-based Gaussian mixture model provides the best overall performance and highest computational efficiency for our use-case, allowing accurate estimation of the spatial distribution of active fishing (97% of true area captured). When vessel movement data can be validated, we recommend assessing the performance of different methods. These results illustrate the feasibility of designing a monitoring system to efficiently generate information on fishing grounds, fishing intensity, or monitoring of compliance to regulations at a nationwide scale in near-real-time.

Sensitivity of multispecies maximum sustainable yields to trends in the top (marine mammals) and bottom (primary production) compartments of the southern North Sea food-web.

In marine ecosystems, maximum sustainable yield considerations are affected by any substantial changes that occur in the top and bottom compartments of the food-web. This study explores how the southern North Sea's fisheries may need to adjust their fishing efforts to maintain optimum yields of sole, plaice, cod and brown shrimps under increased marine mammal populations and a reduced primary productivity. We constructed plausible scenarios of ongoing food-web changes using the results of Bayesian age-structured population models to estimate carrying capacities of harbour porpoises (Phocoena phocoena) and grey seals (Halichoerus grypus). Losses in primary productivity were predicted by lower trophic level ecosystem models. These scenarios were implemented in a food-web model of the southern North Sea. For each scenario, we sought mixed-fleet fishing efforts that would deliver maximum yields of sole, plaice, cod and brown shrimp combined. We also did so for a baseline run with unaltered mammal and primary production, and compared the differences in optimal fishing strategies, predicted yields, and states of the stocks between the scenarios. We found stocks and yields to be far more sensitive to changes in primary productivity than to increased marine mammal predation. The latter predominantly impacted cod, and even benefitted brown shrimps compared to the baseline run. Under 30% reduced primary productivity, fishing efforts had to be reduced by 50% to still provide maximum yields, whereas the marine mammal scenario induced no need to adjust the fishing regime. This draws attention to the potential gains of incorporating bottom-up processes into long-term management considerations, while marine mammal predation may be less of a concern, in particular for flatfish fisheries in the North Sea, and may even benefit shrimp trawlers because of reduced predation on shrimp from fish predators.

Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance.

Many baleen whales undertake annual fasting and feeding cycles, resulting in substantial changes in their body condition, an important factor affecting fitness. As a measure of lipid-store body condition, tissue density of a few deep diving marine mammals has been estimated using a hydrodynamic glide model of drag and buoyancy forces. Here, we applied the method to shallow-diving humpback whales (Megaptera novaeangliae) in North Atlantic and Antarctic feeding aggregations. High-resolution 3-axis acceleration, depth and speed data were collected from 24 whales. Measured values of acceleration during 5 s glides were fitted to a hydrodynamic glide model to estimate unknown parameters (tissue density, drag term and diving gas volume) in a Bayesian framework. Estimated species-average tissue density (1031.6 ± 2.1 kg m-3, ±95% credible interval) indicates that humpback whale tissue is typically negatively buoyant although there was a large inter-individual variation ranging from 1025.2 to 1043.1 kg m-3. The precision of the individual estimates was substantially finer than the variation across different individual whales, demonstrating a progressive decrease in tissue density throughout the feeding season and comparably high lipid-store in pregnant females. The drag term (CDAm-1) was estimated to be relatively high, indicating a large effect of lift-related induced drag for humpback whales. Our results show that tissue density of shallow diving baleen whales can be estimated using the hydrodynamic gliding model, although cross-validation with other techniques is an essential next step. This method for estimating body condition is likely to be broadly applicable across a range of aquatic animals and environments.

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.

Impact of wild prey availability on livestock predation by snow leopards.

An increasing proportion of the world's poor is rearing livestock today, and the global livestock population is growing. Livestock predation by large carnivores and their retaliatory killing is becoming an economic and conservation concern. A common recommendation for carnivore conservation and for reducing predation on livestock is to increase wild prey populations based on the assumption that the carnivores will consume this alternative food. Livestock predation, however, could either reduce or intensify with increases in wild prey depending on prey choice and trends in carnivore abundance. We show that the extent of livestock predation by the endangered snow leopard Panthera uncia intensifies with increases in the density of wild ungulate prey, and subsequently stabilizes. We found that snow leopard density, estimated at seven sites, was a positive linear function of the density of wild ungulates-the preferred prey-and showed no discernible relationship with livestock density. We also found that modelled livestock predation increased with livestock density. Our results suggest that snow leopard conservation would benefit from an increase in wild ungulates, but that would intensify the problem of livestock predation for pastoralists. The potential benefits of increased wild prey abundance in reducing livestock predation can be overwhelmed by a resultant increase in snow leopard populations. Snow leopard conservation efforts aimed at facilitating increases in wild prey must be accompanied by greater assistance for better livestock protection and offsetting the economic damage caused by carnivores.

Body density and diving gas volume of the northern bottlenose whale (Hyperoodon ampullatus).

Diving lung volume and tissue density, reflecting lipid store volume, are important physiological parameters that have only been estimated for a few breath-hold diving species. We fitted 12 northern bottlenose whales with data loggers that recorded depth, 3-axis acceleration and speed either with a fly-wheel or from change of depth corrected by pitch angle. We fitted measured values of the change in speed during 5 s descent and ascent glides to a hydrodynamic model of drag and buoyancy forces using a Bayesian estimation framework. The resulting estimate of diving gas volume was 27.4±4.2 (95% credible interval, CI) ml kg(-1), closely matching the measured lung capacity of the species. Dive-by-dive variation in gas volume did not correlate with dive depth or duration. Estimated body densities of individuals ranged from 1028.4 to 1033.9 kg m(-3) at the sea surface, indicating overall negative tissue buoyancy of this species in seawater. Body density estimates were highly precise with ±95% CI ranging from 0.1 to 0.4 kg m(-3), which would equate to a precision of <0.5% of lipid content based upon extrapolation from the elephant seal. Six whales tagged near Jan Mayen (Norway, 71°N) had lower body density and were closer to neutral buoyancy than six whales tagged in the Gully (Nova Scotia, Canada, 44°N), a difference that was consistent with the amount of gliding observed during ascent versus descent phases in these animals. Implementation of this approach using longer-duration tags could be used to track longitudinal changes in body density and lipid store body condition of free-ranging cetaceans.

State-space modelling reveals proximate causes of harbour seal population declines.

Declines in large vertebrate populations are widespread but difficult to detect from monitoring data and hard to understand due to a multiplicity of plausible biological explanations. In parts of Scotland, harbour seals (Phoca vitulina) have been in decline for 10 years. To evaluate the contributions of different proximate causes (survival, fecundity, observation artefacts) to this decline, we collated behavioural, demographic and population data from one intensively studied population in part of the Moray Firth (north-east Scotland). To these, we fit a state-space model comprising age-structured dynamics and a detailed account of observation errors. After accounting for culling (estimated by our model as 14% of total mortality), the main driver of the historical population decline was a decreasing trend in survival of young individuals combined with (previously unrecognised) low levels of pupping success. In more recent years, the model provides evidence for considerable increases in breeding success and consistently high levels of adult survival. However, breeding success remains the most volatile demographic component of the population. Forecasts from the model indicate a slow population recovery, providing cautious support for recent management measures. Such investigations of the proximate causes of population change (survival, fecundity and observation errors) provide valuable short-term support for the management of population declines, helping to focus future data collection on those ultimate causal mechanisms that are not excluded by the demographic evidence. The contribution of specific ultimate drivers (e.g. shooting mortality or competitors) can also be quantified by including them as covariates to survival or fecundity.

The functional response of a generalist predator.

BACKGROUND: Predators can have profound impacts on the dynamics of their prey that depend on how predator consumption is affected by prey density (the predator's functional response). Consumption by a generalist predator is expected to depend on the densities of all its major prey species (its multispecies functional response, or MSFR), but most studies of generalists have focussed on their functional response to only one prey species. METHODOLOGY AND PRINCIPAL FINDINGS: Using Bayesian methods, we fit an MSFR to field data from an avian predator (the hen harrier Circus cyaneus) feeding on three different prey species. We use a simple graphical approach to show that ignoring the effects of alternative prey can give a misleading impression of the predator's effect on the prey of interest. For example, in our system, a "predator pit" for one prey species only occurs when the availability of other prey species is low. CONCLUSIONS AND SIGNIFICANCE: The Bayesian approach is effective in fitting the MSFR model to field data. It allows flexibility in modelling over-dispersion, incorporates additional biological information into the parameter priors, and generates estimates of uncertainty in the model's predictions. These features of robustness and data efficiency make our approach ideal for the study of long-lived predators, for which data may be sparse and management/conservation priorities pressing.

Sensitivity to assumptions in models of generalist predation on a cyclic prey.

Ecological theory predicts that generalist predators should damp or suppress long-term periodic fluctuations (cycles) in their prey populations and depress their average densities. However, the magnitude of these impacts is likely to vary depending on the availability of alternative prey species and the nature of ecological mechanisms driving the prey cycles. These multispecies effects can be modeled explicitly if parameterized functions relating prey consumption to prey abundance, and realistic population dynamical models for the prey, are available. These requirements are met by the interaction between the Hen Harrier (Circus cyaneus) and three of its prey species in the United Kingdom, the Meadow Pipit (Anthus pratensis), the field vole (Microtus agrestis), and the Red Grouse (Lagopus lagopus scoticus). We used this system to investigate how the availability of alternative prey and the way in which prey dynamics are modeled might affect the behavior of simple trophic networks. We generated cycles in one of the prey species (Red Grouse) in three different ways: through (1) the interaction between grouse density and macroparasites, (2) the interaction between grouse density and male grouse aggressiveness, and (3) a generic, delayed density-dependent mechanism. Our results confirm that generalist predation can damp or suppress grouse cycles, but only when the densities of alternative prey are low. They also demonstrate that diametrically opposite indirect effects between pairs of prey species can occur together in simple systems. In this case, pipits and grouse are apparent competitors, whereas voles and grouse are apparent facilitators. Finally, we found that the quantitative impacts of the predator on prey density differed among the three models of prey dynamics, and these differences were robust to uncertainty in parameter estimation and environmental stochasticity.