Characterizing habitat suitability for a central-place forager in a dynamic marine environment.

Characterizing habitat suitability for a marine predator requires an understanding of the environmental heterogeneity and variability over the range in which a population moves during a particular life cycle. Female California sea lions (Zalophus californianus) are central-place foragers and are particularly constrained while provisioning their young. During this time, habitat selection is a function of prey availability and proximity to the rookery, which has important implications for reproductive and population success. We explore how lactating females may select habitat and respond to environmental variability over broad spatial and temporal scales within the California Current System. We combine near-real-time remotely sensed satellite oceanography, animal tracking data (n = 72) from November to February over multiple years (2003-2009) and Generalized Additive Mixed Models (GAMMs) to determine the probability of sea lion occurrence based on environmental covariates. Results indicate that sea lion presence is associated with cool (<14°C), productive waters, shallow depths, increased eddy activity, and positive sea-level anomalies. Predictive habitat maps generated from these biophysical associations suggest winter foraging areas are spatially consistent in the nearshore and offshore environments, except during the 2004-2005 winter, which coincided with an El Niño event. Here, we show how a species distribution model can provide broadscale information on the distribution of female California sea lions during an important life history stage and its implications for population dynamics and spatial management.

Estimating dispersal rates of Steller sea lion (Eumetopias jubatus) mother-pup pairs from a natal rookery using mark-resight data.

To monitor population trends of Steller sea lions (Eumetopias jubatus) in Alaska, newborn pups are counted during aerial surveys. These surveys are scheduled to occur after the majority of pups are born, but before pups begin to spend significant time in the water. Some studies have reported dispersal of mother-pup pairs away from breeding beaches during the pupping season (July), which may influence survey results. Using a multistate mark-recapture model with state uncertainty, we estimated the amount of dispersal during the pupping season based on observations of permanently marked sea lions. Research was conducted at land-based observation sites on Marmot Island, Alaska, between 2000 and 2013. Both marked adult females with dependent pups and marked pups were observed at two rookery beaches from May to July. Cumulative dispersal rates were minimal (< 1%) prior to the planned start of the aerial survey (23 June) and increased to 11.2% by the planned survey completion date (10 July). The increased cumulative dispersal rate during the remainder of the observation period (end of July) suggests potential bias in surveys that occur beyond 10 July, however surveys past this date are rare (< 10% between 1973 and 2016). As a result, movements of mother-pup pairs during the pupping season are not likely to influence aerial survey estimates.

Evidence of localized resource depletion following a natural colonization event by a large marine predator.

For central place foragers, forming colonies can lead to extensive competition for prey around breeding areas and a zone of local prey depletion. As populations grow, this area of reduced prey can expand impacting foraging success and forcing animals to alter foraging behaviour. Here, we examine a population of marine predators, the northern fur seal (Callorhinus ursinus), which colonized a recently formed volcanic island, and assess changes in foraging behaviour associated with increasing population density. Specifically, we measured pup production and adult foraging behaviour over a 15-year period, during which the population increased 4-fold. Using measures of at-sea movements and dive behaviour, we found clear evidence that as the population expanded, animals were required to allot increasing effort to obtain resources. These changes in behaviour included longer duration foraging trips, farther distances travelled, a larger foraging range surrounding the island and deeper maximum dives. Our results suggest that as the northern fur seal population increased, local prey resources were depleted as a result of increased intraspecific competition. In addition, the recent slowing of population growth indicates that this population may be approaching carrying capacity just 31 years after a natural colonization event. Our study offers insight into the dynamics of population growth and impacts of increasing population density on a large marine predator. Such data could be vital for understanding future population fluctuations that occur in response to the dynamic environment, as natural and anthropogenic factors continue to modify marine habitats.

Cumulative human impacts on marine predators.

Stressors associated with human activities interact in complex ways to affect marine ecosystems, yet we lack spatially explicit assessments of cumulative impacts on ecologically and economically key components such as marine predators. Here we develop a metric of cumulative utilization and impact (CUI) on marine predators by combining electronic tracking data of eight protected predator species (n=685 individuals) in the California Current Ecosystem with data on 24 anthropogenic stressors. We show significant variation in CUI with some of the highest impacts within US National Marine Sanctuaries. High variation in underlying species and cumulative impact distributions means that neither alone is sufficient for effective spatial management. Instead, comprehensive management approaches accounting for both cumulative human impacts and trade-offs among multiple stressors must be applied in planning the use of marine resources.

Estimating animal resource selection from telemetry data using point process models.

1. Analyses of animal resource selection functions (RSF) using data collected from relocations of individuals via remote telemetry devices have become commonplace. Increasing technological advances, however, have produced statistical challenges in analysing such highly autocorrelated data. Weighted distribution methods have been proposed for analysing RSFs with telemetry data. However, they can be computationally challenging due to an intractable normalizing constant and cannot be aggregated (i.e. collapsed) over time to make space-only inference. 2. In this study, we take a conceptually different approach to modelling animal telemetry data for making RSF inference. We consider the telemetry data to be a realization of a space-time point process. Under the point process paradigm, the times of the relocations are also considered to be random rather than fixed. 3. We show the point process models we propose are a generalization of the weighted distribution telemetry models. By generalizing the weighted model, we can access several numerical techniques for evaluating point process likelihoods that make use of common statistical software. Thus, the analysis methods can be readily implemented by animal ecologists. 4. In addition to ease of computation, the point process models can be aggregated over time by marginalizing over the temporal component of the model. This allows a full range of models to be constructed for RSF analysis at the individual movement level up to the study area level. 5. To demonstrate the analysis of telemetry data with the point process approach, we analysed a data set of telemetry locations from northern fur seals (Callorhinus ursinus) in the Pribilof Islands, Alaska. Both a space-time and an aggregated space-only model were fitted. At the individual level, the space-time analysis showed little selection relative to the habitat covariates. However, at the study area level, the space-only model showed strong selection relative to the covariates.

Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal.

The mesopelagic zone of the northeast Pacific Ocean is an important foraging habitat for many predators, yet few studies have addressed the factors driving basin-scale predator distributions or inter-annual variability in foraging and breeding success. Understanding these processes is critical to reveal how conditions at sea cascade to population-level effects. To begin addressing these challenging questions, we collected diving, tracking, foraging success, and natality data for 297 adult female northern elephant seal migrations from 2004 to 2010. During the longer post-molting migration, individual energy gain rates were significant predictors of pregnancy. At sea, seals focused their foraging effort along a narrow band corresponding to the boundary between the sub-arctic and sub-tropical gyres. In contrast to shallow-diving predators, elephant seals target the gyre-gyre boundary throughout the year rather than follow the southward winter migration of surface features, such as the Transition Zone Chlorophyll Front. We also assessed the impact of added transit costs by studying seals at a colony near the southern extent of the species' range, 1,150 km to the south. A much larger proportion of seals foraged locally, implying plasticity in foraging strategies and possibly prey type. While these findings are derived from a single species, the results may provide insight to the foraging patterns of many other meso-pelagic predators in the northeast Pacific Ocean.

Latitudinal range influences the seasonal variation in the foraging behavior of marine top predators.

Non-migratory resident species should be capable of modifying their foraging behavior to accommodate changes in prey abundance and availability associated with a changing environment. Populations that are better adapted to change will have higher foraging success and greater potential for survival in the face of climate change. We studied two species of resident central place foragers from temperate and equatorial regions with differing population trends and prey availability associated to season, the California sea lion (Zalophus californianus) (CSL) whose population is increasing and the endangered Galapagos sea lion (Zalophus wollebaeki) (GSL) whose population is declining. To determine their response to environmental change, we studied and compared their diving behavior using time-depth recorders and satellite location tags and their diet by measuring C and N isotope ratios during a warm and a cold season. Based on latitudinal differences in oceanographic productivity, we hypothesized that the seasonal variation in foraging behavior would differ for these two species. CSL exhibited greater seasonal variability in their foraging behavior as seen in changes to their diving behavior, foraging areas and diet between seasons. Conversely, GSL did not change their diving behavior between seasons, presenting three foraging strategies (shallow, deep and bottom divers) during both. GSL exhibited greater dive and foraging effort than CSL. We suggest that during the warm and less productive season a greater range of foraging behaviors in CSL was associated with greater competition for prey, which relaxed during the cold season when resource availability was greater. GSL foraging specialization suggests that resources are limited throughout the year due to lower primary production and lower seasonal variation in productivity compared to CSL. These latitudinal differences influence their foraging success, pup survival and population growth reflected in contrasting population trends in which CSL are more successful and potentially more resilient to climate change.

Time to eat: measurements of feeding behaviour in a large marine predator, the northern elephant seal Mirounga angustirostris.

1. The at-sea behaviour of marine predators is often described based on changes in behavioural states, such as transit, searching, and feeding. However, to distinguish between these behaviours, it is necessary to know the actual functions of the behaviours recorded. Specifically, to understand the foraging behaviour of marine predators, it is necessary to measure prey consumption. Therefore, the at-sea feeding behaviour of northern elephant seals (N = 13) was examined using satellite transmitters, time-depth recorders, and stomach temperature recorders. In addition, stomach temperature telemetry allowed for the validation of indirect measures of feeding behaviour used for marine predators, including decreases in transit rate and changes in dive shape. 2. Feeding data were recorded for the early phase of the migration (2.2-21 days). The first feeding events occurred shortly after animals departed (4.0 +/- 1.5 h) and close to the rookery (58.6 +/- 21.9 km), but these feedings were followed by extended periods without prey consumption (14.5 +/- 2.5 h). Continuous (bout) feeding did not occur until on average 7.5 +/- 1.8 days after the females left the rookery. Females showed significant differences in the feeding rate while feeding in a bout (1.3-2.1 feeding events hour(-1)). 3. There was a significant negative relationship between interpolated transit rate and feeding events (r(2) = 0.62, P < 0.01). Feeding, which was associated with all dive types, occurred most often during the foraging type dive shape (74.2%). Finally, successful feeding only occurred between 18-24% of the time when females displayed the foraging type dive shape suggesting that the use of dive shape alone, while indicative of behaviours associated with foraging (searching and catching prey) overestimates actual feeding behaviour. 4. This study showed females not only feed extensively during the early migration, but there was individual variation in both foraging locations and foraging success. In addition, by combining direct and indirect measures of feeding, this study has provided support for the use of foraging indicators in marine predators.

Identifying and quantifying prey consumption using stomach temperature change in pinnipeds.

For many marine predators knowledge of foraging behavior is limited to inferences based on changes in diving or movement patterns at sea. This results in an incomplete and potentially inaccurate view of the foraging ecology of a species. This study examined the use of stomach temperature telemetry to identify and quantify prey consumed in both a phocid (northern elephant seal Mirounga angustirostris) and an otariid (California sea lion Zalophus californianus) species. In addition, we used opportunistic water consumption by northern elephant seals to test a method to distinguish between prey and water ingestion. Over 96% of feedings could be identified based on a decline in stomach temperature, even when meals were separated by as little as 70 min. Water consumption was distinguishable from prey consumption, as the rate of recovery in stomach temperature was significantly faster for water (F(1,142) = 79.2, P < 0.01). However, using this method, the overlap in recovery rates between prey and water resulted in 30.6% of water ingestion events being misclassified as prey ingestion. For both species, the integral calculated from the decline in stomach temperature over time (area above the curve) could be used to estimate mass consumed, when adjusted for the temperature difference between the prey and core body temperature. For California sea lions, there was a significant effect of individual on the ability to quantify prey consumed, which was not related to their mass or sex. Although many factors may influence the ability to use stomach temperature change to identify and quantify prey consumed, this study has shown measures of stomach temperature can accurately identify prey consumption and provide an estimate of meal mass, allowing for a greater understanding of the feeding behavior of marine mammals.

Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer.

1. Foraging behaviours of the Australian sea lion (Neophoca cinerea) reflect an animal working hard to exploit benthic habitats. Lactating females demonstrate almost continuous diving, maximize bottom time, exhibit elevated field metabolism and frequently exceed their calculated aerobic dive limit. Given that larger animals have disproportionately greater diving capabilities, we wanted to examine how pups and juveniles forage successfully. 2. Time/depth recorders were deployed on pups, juveniles and adult females at Seal Bay Conservation Park, Kangaroo Island, South Australia. Ten different mother/pup pairs were equipped at three stages of development (6, 15 and 23 months) to record the diving behaviours of 51 (nine instruments failed) animals. 3. Dive depth and duration increased with age. However, development was slow. At 6 months, pups demonstrated minimal diving activity and the mean depth for 23-month-old juveniles was only 44 +/- 4 m, or 62% of adult mean depth. 4. Although pups and juveniles did not reach adult depths or durations, dive records for young sea lions indicate benthic diving with mean bottom times (2.0 +/- 0.2 min) similar to those of females (2.1 +/- 0.2 min). This was accomplished by spending higher proportions of each dive and total time at sea on or near the bottom than adults. Immature sea lions also spent a higher percentage of time at sea diving. 5. Juveniles may have to work harder because they are weaned before reaching full diving capability. For benthic foragers, reduced diving ability limits available foraging habitat. Furthermore, as juveniles appear to operate close to their physiological maximum, they would have a difficult time increasing foraging effort in response to reductions in prey. Although benthic prey are less influenced by seasonal fluctuations and oceanographic perturbations than epipelagic prey, demersal fishery trawls may impact juvenile survival by disrupting habitat and removing larger size classes of prey. These issues may be an important factor as to why the Australian sea lion population is currently at risk.

Interpolation of animal tracking data in a fluid environment.

Interpolation of geolocation or Argos tracking data is a necessity for habitat use analyses of marine vertebrates. In a fluid marine environment, characterized by curvilinear structures, linearly interpolated track data are not realistic. Based on these two facts, we interpolated tracking data from albatrosses, penguins, boobies, sea lions, fur seals and elephant seals using six mathematical algorithms. Given their popularity in mathematical computing, we chose Bézier, hermite and cubic splines, in addition to a commonly used linear algorithm to interpolate data. Performance of interpolation methods was compared with different temporal resolutions representative of the less-precise geolocation and the more-precise Argos tracking techniques. Parameters from interpolated sub-sampled tracks were compared with those obtained from intact tracks. Average accuracy of the interpolated location was not affected by the interpolation method and was always within the precision of the tracking technique used. However, depending on the species tested, some curvilinear interpolation algorithms produced greater occurrences of more accurate locations, compared with the linear interpolation method. Total track lengths were consistently underestimated but were always more accurate using curvilinear interpolation than linear interpolation. Curvilinear algorithms are safe to use because accuracy, shape and length of the tracks are either not different or are slightly enhanced and because analyses always remain conservative. The choice of the curvilinear algorithm does not affect the resulting track dramatically so it should not preclude their use. We thus recommend using curvilinear interpolation techniques because of the more realistic fluid movements of animals. We also provide some guidelines for choosing an algorithm that is most likely to maximize track quality for different types of marine vertebrates.