Patrick W. Robinson

Accuracy of ARGOS locations of Pinnipeds at-sea estimated using Fastloc GPS.

Background ARGOS satellite telemetry is one of the most widely used methods to track the movements of free-ranging marine and terrestrial animals and is fundamental to studies of foraging ecology, migratory behavior and habitat-use. ARGOS location estimates do not include complete error estimations, and for many marine organisms, the most commonly acquired locations (Location Class 0, A, B, or Z) are provided with no declared error estimate. Methodology/Principal Findings We compared the accuracy of ARGOS locations to those obtained using Fastloc GPS from the same electronic tags on five species of pinnipeds: 9 California sea lions (Zalophus californianus), 4 Galapagos sea lions (Zalophus wollebaeki), 6 Cape fur seals (Arctocephalus pusillus pusillus), 3 Australian fur seals (A. p. doriferus) and 5 northern elephant seals (Mirounga angustirostris). These species encompass a range of marine habitats (highly pelagic vs coastal), diving behaviors (mean dive durations 2–21 min) and range of latitudes (equator to temperate). A total of 7,318 ARGOS positions and 27,046 GPS positions were collected. Of these, 1,105 ARGOS positions were obtained within five minutes of a GPS position and were used for comparison. The 68th percentile ARGOS location errors as measured in this study were LC-3 0.49 km, LC-2 1.01 km, LC-1 1.20 km, LC-0 4.18 km, LC-A 6.19 km, LC-B 10.28 km. Conclusions/Significance The ARGOS errors measured here are greater than those provided by ARGOS, but within the range of other studies. The error was non-normally distributed with each LC highly right-skewed. Locations of species that make short duration dives and spend extended periods on the surface (sea lions and fur seals) had less error than species like elephant seals that spend more time underwater and have shorter surface intervals. Supplemental data (S1) are provided allowing the creation of density distributions that can be used in a variety of filtering algorithms to improve the quality of ARGOS tracking data.

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.

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.

Measurements of foraging success in a highly pelagic marine predator, the northern elephant seal

1. Identification of foraging behaviour and the ability to assess foraging success is critical to understanding individual and between-species variation in habitat use and foraging ecology. For pelagic predators, behaviour-dependent foraging metrics are commonly used to identify important foraging areas, yet few of these metrics have been validated. 2. Using the northern elephant seal as a model species, we validated the use of a behaviour-independent measure of foraging success (changes in drift rate) at the scale of the entire foraging migration, and then used this to assess a variety of common foraging metrics that are based on movement patterns and dive behaviour. Transit rate consistently provided the best estimate of daily foraging success, although the addition of other metrics provides insight into different foraging behaviours or strategies. 3. While positive changes in buoyancy occurred throughout most of the migrations, implying successful feeding across much of the north Pacific, the areas of most rapid changes in buoyancy occurred along a latitudinal band (40-50° N) corresponding to a dynamic hydrographic region including Subarctic Gyre and Transition Zone waters. 4. These results support the use of transit rate as an index of foraging success: a metric that is easily derived from tracking measurements on a wide range of marine species.

A parsimonious approach to modeling animal movement data.

Animal tracking is a growing field in ecology and previous work has shown that simple speed filtering of tracking data is not sufficient and that improvement of tracking location estimates are possible. To date, this has required methods that are complicated and often time-consuming (state-space models), resulting in limited application of this technique and the potential for analysis errors due to poor understanding of the fundamental framework behind the approach. We describe and test an alternative and intuitive approach consisting of bootstrapping random walks biased by forward particles. The model uses recorded data accuracy estimates, and can assimilate other sources of data such as sea-surface temperature, bathymetry and/or physical boundaries. We tested our model using ARGOS and geolocation tracks of elephant seals that also carried GPS tags in addition to PTTs, enabling true validation. Among pinnipeds, elephant seals are extreme divers that spend little time at the surface, which considerably impact the quality of both ARGOS and light-based geolocation tracks. Despite such low overall quality tracks, our model provided location estimates within 4.0, 5.5 and 12.0 km of true location 50% of the time, and within 9, 10.5 and 20.0 km 90% of the time, for above, equal or below average elephant seal ARGOS track qualities, respectively. With geolocation data, 50% of errors were less than 104.8 km (<0.94°), and 90% were less than 199.8 km (<1.80°). Larger errors were due to lack of sea-surface temperature gradients. In addition we show that our model is flexible enough to solve the obstacle avoidance problem by assimilating high resolution coastline data. This reduced the number of invalid on-land location by almost an order of magnitude. The method is intuitive, flexible and efficient, promising extensive utilization in future research.

Northern elephant seals adjust gliding and stroking patterns with changes in buoyancy: validation of at-sea metrics of body density

SUMMARY Many diving animals undergo substantial changes in their body density that are the result of changes in lipid content over their annual fasting cycle. Because the size of the lipid stores reflects an integration of foraging effort (energy expenditure) and foraging success (energy assimilation), measuring body density is a good way to track net resource acquisition of free-ranging animals while at sea. Here, we experimentally altered the body density and mass of three free-ranging elephant seals by remotely detaching weights and floats while monitoring their swimming speed, depth and three-axis acceleration with a high-resolution data logger. Cross-validation of three methods for estimating body density from hydrodynamic gliding performance of freely diving animals showed strong positive correlation with body density estimates obtained from isotope dilution body composition analysis over density ranges of 1015 to 1060 kg m–3. All three hydrodynamic models were within 1% of, but slightly greater than, body density measurements determined by isotope dilution, and therefore have the potential to track changes in body condition of a wide range of freely diving animals. Gliding during ascent and descent clearly increased and stroke rate decreased when buoyancy manipulations aided the direction of vertical transit, but ascent and descent speed were largely unchanged. The seals adjusted stroking intensity to maintain swim speed within a narrow range, despite changes in buoyancy. During active swimming, all three seals increased the amplitude of lateral body accelerations and two of the seals altered stroke frequency in response to the need to produce thrust required to overcome combined drag and buoyancy forces.

Condition and mass impact oxygen stores and dive duration in adult female northern elephant seals

SUMMARY The range of foraging behaviors available to deep-diving, air-breathing marine vertebrates is constrained by their physiological capacity to breath-hold dive. We measured body oxygen stores (blood volume and muscle myoglobin) and diving behavior in adult female northern elephant seals, Mirounga angustirostris, to investigate age-related effects on diving performance. Blood volume averaged 74.4±17.0 liters in female elephant seals or 20.2±2.0% of body mass. Plasma volume averaged 32.2±7.8 liters or 8.7±0.7% of body mass. Absolute plasma volume and blood volume increased independently with mass and age. Hematocrit decreased weakly with mass but did not vary with age. Muscle myoglobin concentration, while higher than previously reported (7.4±0.7 g%), did not vary with mass or age. Pregnancy status did not influence blood volume. Mean dive duration, a proxy for physiological demand, increased as a function of how long seals had been at sea, followed by mass and hematocrit. Strong effects of female body mass (range, 218-600 kg) on dive duration, which were independent of oxygen stores, suggest that larger females had lower diving metabolic rates. A tendency for dives to exceed calculated aerobic limits occurred more frequently later in the at-sea migration. Our data suggest that individual physiological state variables and condition interact to determine breath-hold ability and that both should be considered in life-history studies of foraging behavior.

Electronic tracking tag programming is critical to data collection for behavioral time-series analysis

Electronic tracking tags are major tools of ecological research and management, but programming sophisticated tags can be challenging. We discovered that a common programming scheme can negatively affect the quality of tracks collected by Argos tags. Here we describe the problem and how it occurred. We then simulated a series of tracks with different data collection schemes to investigate how spatial precision and temporal frequency affect the overall quality of tracking data. Tracks were simulated using a two-state composite correlated random walk (CCRW). Tracks were simulated with two spatial scales, using parameters estimated from northern elephant seal (large scale) and California sea lion (small scale) tracking data. Onto each simulated track, observations of varying precision, frequency, and censoring were imposed. We then fit the CCRW in a state-space model (SSM) to the simulated observations in order to assess how data quality and frequency affected recovery of known behavioral state and location. We show that when movement scales are small, regular observations were critical to recover behavior and location. In addition, tracks with frequent regular locations (increasing N) overcame low spatial accuracy (e.g., Argos) to detect small-scale movement patterns, suggesting frequently collected Argos locations may be as good as infrequently collected GPS in some circumstances. From these results and our experience tracking animals generally, we produce a set of guidelines for those manufacturing, programming, and deploying electronic tracking tags to maximize the utility of the data they produce.

Pandemic H1N1 Influenza Isolated from Free-Ranging Northern Elephant Seals in 2010 off the Central California Coast

Interspecies transmission of influenza A is an important factor in the evolution and ecology of influenza viruses. Marine mammals are in contact with a number of influenza reservoirs, including aquatic birds and humans, and this may facilitate transmission among avian and mammalian hosts. Virus isolation, whole genome sequencing, and hemagluttination inhibition assay confirmed that exposure to pandemic H1N1 influenza virus occurred among free-ranging Northern Elephant Seals (Mirounga angustirostris) in 2010. Nasal swabs were collected from 42 adult female seals in April 2010, just after the animals had returned to the central California coast from their short post-breeding migration in the northeast Pacific. Swabs from two seals tested positive by RT-PCR for the matrix gene, and virus was isolated from each by inoculation into embryonic chicken eggs. Whole genome sequencing revealed greater than 99% homology with A/California/04/2009 (H1N1) that emerged in humans from swine in 2009. Analysis of more than 300 serum samples showed that samples collected early in 2010 (n = 100) were negative and by April animals began to test positive for antibodies against the pH1N1 virus (HI titer of ≥1∶40), supporting the molecular findings. In vitro characterizations studies revealed that viral replication was indistinguishable from that of reference strains of pH1N1 in canine kidney cells, but replication was inefficient in human epithelial respiratory cells, indicating these isolates may be elephant seal adapted viruses. Thus findings confirmed that exposure to pandemic H1N1 that was circulating in people in 2009 occurred among free-ranging Northern Elephant Seals in 2010 off the central California coast. This is the first report of pH1N1 (A/Elephant seal/California/1/2010) in any marine mammal and provides evidence for cross species transmission of influenza viruses in free-ranging wildlife and movement of influenza viruses between humans and wildlife.

Estimating resource acquisition and at-sea body condition of a marine predator

Body condition plays a fundamental role in many ecological and evolutionary processes at a variety of scales and across a broad range of animal taxa. An understanding of how body condition changes at fine spatial and temporal scales as a result of interaction with the environment provides necessary information about how animals acquire resources. However, comparatively little is known about intra- and interindividual variation of condition in marine systems. Where condition has been studied, changes typically are recorded at relatively coarse time-scales. By quantifying how fine-scale interaction with the environment influences condition, we can broaden our understanding of how animals acquire resources and allocate them to body stores. Here we used a hierarchical Bayesian state-space model to estimate the body condition as measured by the size of an animals lipid store in two closely related species of marine predator that occupy different hemispheres: northern elephant seals (Mirounga angustirostris) and southern elephant seals (Mirounga leonina). The observation model linked drift dives to lipid stores. The process model quantified daily changes in lipid stores as a function of the physiological condition of the seal (lipid:lean tissue ratio, departure lipid and departure mass), its foraging location, two measures of behaviour and environmental covariates. We found that physiological condition significantly impacted lipid gain at two time-scales – daily and at departure from the colony – that foraging location was significantly associated with lipid gain in both species of elephant seals and that long-term behavioural phase was associated with positive lipid gain in northern and southern elephant seals. In northern elephant seals, the occurrence of short-term behavioural states assumed to represent foraging were correlated with lipid gain. Lipid gain was a function of covariates in both species. Southern elephant seals performed fewer drift dives than northern elephant seals and gained lipids at a lower rate. We have demonstrated a new way to obtain time series of body condition estimates for a marine predator at fine spatial and temporal scales. This modelling approach accounts for uncertainty at many levels and has the potential to integrate physiological and movement ecology of top predators. The observation model we used was specific to elephant seals, but the process model can readily be applied to other species, providing an opportunity to understand how animals respond to their environment at a fine spatial scale.