Daniel E. Crocker

FORAGING ECOLOGY OF NORTHERN ELEPHANT SEALS

Sexual segregation in foraging is predicted from the great size disparity of male and female northern elephant seals, Mirounga angustirostris. Our aim was to test this prediction by measuring diving and foraging behavior, foraging locations, and distribution of the sexes during biannual migrations in the northeastern Pacific Ocean. Daily movements of 27 adult males and 20 adult females, during 56 migrations from Afio Nuevo, California, USA, were determined by Argos satellite telemetry via head-mounted platform transmitter terminals. Diving records were obtained with archival time-depth-speed recorders attached to the backs of seals that were recovered when the seals returned to the rookery. Pronounced sex differences were found in foraging location and foraging pattern, as reflected by hor- izontal transit speed and diving behavior. Males moved directly north or northwest at a mean speed of 90 ? 27 km/d to focal foraging areas along the continental margin ranging from coastal Oregon (534 km away) to the western Aleutian Islands (4775 km away). Males remained in these areas (mean size = 7892 ki2) for 21-84% of their 4-mo stays at sea. The predominance of flat-bottom dives in these areas suggests concentrated feeding on benthic prey. Migration distance and estimated mass gain were positively correlated with male size, and individual males returned to the same area to forage on subsequent migrations. In contrast, females ranged across a wider area of the northeastern Pacific, from 380 to 600 N and from the coast to 172.5? E. Focal foraging areas, indicated by a reduction in swim speed to <0.4 m/s, were distributed over deep water along the migratory path, with females remaining on them a mean of 3.5 d before moving to another one. Jagged-bottom dives that tracked the deep scattering layer prevailed in these areas, suggesting that females were feeding on pelagic prey in the water column. Females took roughly similar initial paths in subsequent migrations, but large deviations from the previous route were observed. We conclude that there is habitat segregation between the sexes. Females range widely over deep water, apparently foraging on patchily distributed, vertically migrating, pelagic prey, whereas males forage along the continental margin at the distal end of their migration in a manner consistent with feeding on benthic prey.

Variations in behavior and condition of a Southern Ocean top predator in relation to in situ oceanographic conditions

Responses by marine top predators to environmental variability have previously been almost impossible to observe directly. By using animal-mounted instruments simultaneously recording movements, diving behavior, and in situ oceanographic properties, we studied the behavioral and physiological responses of southern elephant seals to spatial environmental variability throughout their circumpolar range. Improved body condition of seals in the Atlantic sector was associated with Circumpolar Deep Water upwelling regions within the Antarctic Circumpolar Current, whereas High-Salinity Shelf Waters or temperature/salinity gradients under winter pack ice were important in the Indian and Pacific sectors. Energetic consequences of these variations could help explain recently observed population trends, showing the usefulness of this approach in examining the sensitivity of top predators to global and regional-scale climate variability.

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.

Interpolation of animal tracking data in a fluid environment

SUMMARY 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.

Maternal Traits and Reproductive Effort in Northern Elephant Seals

The aim of this study was to determine the effects of maternal traits on reproductive expenditure and energy delivery to the offspring in a capital breeder, the northern elephant seal (Mirounga angustirostris). Changes in maternal and offspring energy reserves and milk-energy delivery were examined in relation to maternal parturition mass, body composition, and age in females and pups breeding at Ano Nuevo State Reserve, California. Maternal body mass and composition had significant effects on maternal energy expenditure over lactation. Path analysis suggested no significant effects of maternal age on reproductive effort of parous females. The efficiency of milk production increased significantly with maternal age. Offspring metabolism was a relatively small component of maternal energy expenditure, with pups storing 84% of the energy obtained from milk. These effects are an important consequence of the phocid strategy for enabling terrestrial parturition despite marine feeding. This strategy has resulted in an abbreviated and highly efficient lactation system that is strongly impacted by body reserves, linking foraging success at sea with reproductive success on land. Maternal size, body composition, and age were important features of reproduction in northern elephant seals. These characteristics are rarely considered concurrently in life history studies.

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.

Autonomous Pinniped Environmental Samplers: Using Instrumented Animals as Oceanographic Data Collectors

Data-recording tags applied to marine animals store data for later retrieval and can return valuable information on animal behavior and ecology, including habitat preference, physiology, and movement patterns, as well as environmental data. If properly instrumented, calibrated, and archived, data from these tags can add to the oceanographic datastream for parts of the ocean where data are sparse or lacking. Such data, from northern elephant seals instrumented with time‐temperature‐depth recorders (TTDR) and ARGOS platform terminal transmitters, is examined in this study. Northern elephant seals range widely over the northeastern Pacific on long foraging trips. The seals dive continuously on these trips to depths of 400‐600 m. Between March 1998 and March 1999, six female and three male elephant seals were tagged in central California and data were collected during subsequent foraging trips. Temperature and depth were measured and stored every 30 s and retrieved after the animals returned to the rookery months later. Portions of the track where both ARGOS and TTDR data were available from these nine animals averaged 4634 km over 67 days with 2.4 ARGOS positions per day. Mean dive duration was 20 min and mean dive depth was 428 m. A comparison of temperature profiles from seal TTDR with Global Temperature‐Salinity Profile Program (GTSPP) subsurface data showed very good agreement, as did surface temperatures to other sources of SST. Quality control of the data and entry into the World Ocean Database (WOD) is described. A total of 75 665 autonomous pinniped bathythermograph (APBT) profiles over the 41 702 km of seal trackline were added to the WOD. Biological autonomous sampling systems have immense potential to contribute oceanographic data in a costeffective manner. The northern elephant seal represents but one species covering portions of the northeast Pacific Ocean. Research programs presently exist on a variety of species, including southern elephant seals and other pinnipeds, tunas and billfish, sharks, seabirds, marine turtles, and whales. With improving technology, such tags will be applied to even more marine animals and the approach described here can be applied to other species to improve ocean data availability.

Protein Catabolism and Renal Function in Lactating Northern Elephant Seals

Northern elephant seals, Mirounga angustirostris, fast completely from food and water during lactation. Previous investigations of maternal investment suggested physiological constraints on the level of energy expenditure during lactation. In this study, two components of phocid fasting physiology, protein sparing and reduced glomerular filtration rate, were examined for effects of changing body composition and lactation duration. Protein catabolism was estimated from 14C‐urea turnover in five mid‐ and five late‐lactation females. Body composition was determined by using an ultrasound scanner to measure blubber depth coupled with morphometrics. Glo‐merular filtration rate was measured in five females at mid‐and late‐lactation using plasma clearance of 3H‐inulin. Protein catabolism increased significantly between measurements. The contribution of protein to metabolism varied with body composition and lactation duration. Mass‐proportional glomerular filtration rate increased significantly between measurements. These data suggest that conflicting metabolic demands of lactation and fasting might constrain the duration and magnitude of maternal investment in northern elephant seals.

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.

Prolonged fasting does not increase oxidative damage or inflammation in postweaned northern elephant seal pups

SUMMARY Elephant seals are naturally adapted to survive up to three months of absolute food and water deprivation (fasting). Prolonged food deprivation in terrestrial mammals increases reactive oxygen species (ROS) production, oxidative damage and inflammation that can be induced by an increase in the renin–angiotensin system (RAS). To test the hypothesis that prolonged fasting in elephant seals is not associated with increased oxidative stress or inflammation, blood samples and muscle biopsies were collected from early (2–3 weeks post-weaning) and late (7–8 weeks post-weaning) fasted seals. Plasma levels of oxidative damage, inflammatory markers and plasma renin activity (PRA), along with muscle levels of lipid and protein oxidation, were compared between early and late fasting periods. Protein expression of angiotensin receptor 1 (AT1), pro-oxidant (Nox4) and antioxidant enzymes (CuZn- and Mn-superoxide dismutases, glutathione peroxidase and catalase) was analyzed in muscle. Fasting induced a 2.5-fold increase in PRA, a 50% increase in AT1, a twofold increase in Nox4 and a 70% increase in NADPH oxidase activity. By contrast, neither tissue nor systemic indices of oxidative damage or inflammation increased with fasting. Furthermore, muscle antioxidant enzymes increased 40–60% with fasting in parallel with an increase in muscle and red blood cell antioxidant enzyme activities. These data suggest that, despite the observed increases in RAS and Nox4, an increase in antioxidant enzymes appears to be sufficient to suppress systemic and tissue indices of oxidative damage and inflammation in seals that have fasted for a prolonged period. The present study highlights the importance of antioxidant capacity in mammals during chronic periods of stress to help avoid deleterious systemic consequences.