Daniel P. Costa

Tracking apex marine predator movements in a dynamic ocean

Pelagic marine predators face unprecedented challenges and uncertain futures. Overexploitation and climate variability impact the abundance and distribution of top predators in ocean ecosystems. Improved understanding of ecological patterns, evolutionary constraints and ecosystem function is critical for preventing extinctions, loss of biodiversity and disruption of ecosystem services. Recent advances in electronic tagging techniques have provided the capacity to observe the movements and long-distance migrations of animals in relation to ocean processes across a range of ecological scales. Tagging of Pacific Predators, a field programme of the Census of Marine Life, deployed 4,306 tags on 23 species in the North Pacific Ocean, resulting in a tracking data set of unprecedented scale and species diversity that covers 265,386 tracking days from 2000 to 2009. Here we report migration pathways, link ocean features to multispecies hotspots and illustrate niche partitioning within and among congener guilds. Our results indicate that the California Current large marine ecosystem and the North Pacific transition zone attract and retain a diverse assemblage of marine vertebrates. Within the California Current large marine ecosystem, several predator guilds seasonally undertake north–south migrations that may be driven by oceanic processes, species-specific thermal tolerances and shifts in prey distributions. We identify critical habitats across multinational boundaries and show that top predators exploit their environment in predictable ways, providing the foundation for spatial management of large marine ecosystems.

Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer

Electronic tracking tags have revolutionized our understanding of broad-scale movements and habitat use of highly mobile marine animals, but a large gap in our knowledge still remains for a wide range of small species. Here, we report the extraordinary transequatorial postbreeding migrations of a small seabird, the sooty shearwater, obtained with miniature archival tags that log data for estimating position, dive depth, and ambient temperature. Tracks (262 ± 23 days) reveal that shearwaters fly across the entire Pacific Ocean in a figure-eight pattern while traveling 64,037 ± 9,779 km roundtrip, the longest animal migration ever recorded electronically. Each shearwater made a prolonged stopover in one of three discrete regions off Japan, Alaska, or California before returning to New Zealand through a relatively narrow corridor in the central Pacific Ocean. Transit rates as high as 910 ± 186 km·day−1 were recorded, and shearwaters accessed prey resources in both the Northern and Southern Hemisphere’s most productive waters from the surface to 68.2 m depth. Our results indicate that sooty shearwaters integrate oceanic resources throughout the Pacific Basin on a yearly scale. Sooty shearwater populations today are declining, and because they operate on a global scale, they may serve as an important indicator of climate change and ocean health.

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.

Fast and fuel efficient? Optimal use of wind by flying albatrosses.

The influence of wind patterns on behaviour and effort of free–ranging male wandering albatrosses (Diomedea exulans) was studied with miniaturized external heart–rate recorders in conjunction with satellite transmitters and activity recorders. Heart rate was used as an instantaneous index of energy expenditure. When cruising with favourable tail or side winds, wandering albatrosses can achieve high flight speeds while expending little more energy than birds resting on land. In contrast, heart rate increases concomitantly with increasing head winds, and flight speeds decrease. Our results show that effort is greatest when albatrosses take off from or land on the water. On a larger scale, we show that in order for birds to have the highest probability of experiencing favourable winds, wandering albatrosses use predictable weather systems to engage in a stereotypical flight pattern of large looping tracks. When heading north, albatrosses fly in anticlockwise loops, and to the south, movements are in a clockwise direction. Thus, the capacity to integrate instantaneous eco–physiological measures with records of largescale flight and wind patterns allows us to understand better the complex interplay between the evolution of morphological, physiological and behavioural adaptations of albatrosses in the windiest place on earth.

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.

Water and Energy Flux in Elephant Seal Pups Fasting under Natural Conditions

Total water flux, energy utilization, and mass loss were measured in fasting, newly weaned elephant seal pups, Mirounga angustirostris, in their natural habitat over a period of 32–52 days. Animals lost mass exponentially averaging 5.3 ± 0.9 g·kg−1·day−1. At weaning body water comprised 40% of the total mass while the ratio of adipose to lean body tissue was approximately 1. The mean water turnover rate in all animals was very low, ∼13.0 ± 1.20 ml·liter−1·day−1, and was not affected by entry of the animal into water, supporting the hypothesis that seawater ingestion is not required for water balance. Average metabolic rates calculated from water turnover data were 167.6 ± 19.1 kcal·kg−3/4·day−1. The biological half-time of water, 53.5 ± 5.2 days, is about 2.5 times greater than that of starved harbor seals and significantly exceeds that reported for any other mammal. We conclude that a combination of behavioral and physiological water conservation mechanisms permit these animals to fast on land for up to 3 mo, deriving necessary water and energy from the oxidation of fat stores.

Foraging Energetics of Antartic Fur Seals in Relation to Changes in Prey Availability

This research examines the energy budget of breeding female Antarctic fur seals, both when food was plentiful and when it was scarce. The energy expenditure and change in body mass of lactating female Antarctic fur seals, Arctocephalus gazella, foraging at sea was measured in two years using doubly labeled water at South Georgia Island. There was no difference between years in mass gain, water influx, mass-specific field metabolic rate (FMR), or absolute FMR. Mean at-sea FMR over both years was 9.52 ? 0.55 W/kg (n = 22), a value that is 6.7 times the predicted basal rate but only 1.9 times the FMR measured onshore. Comparable results have been reported for similar-sized northern fur seals. Krill, the nearly exclusive prey of breeding females, were very scarce in 1984 at South Georgia. Fur seal foraging trips were twice as long in 1984 as in 1985 and total mass- specific energy expended by females during these trips was significantly greater. In addition, females were significantly lighter at parturition in 1984, and both pup mortality and the proportion of pups that died from starvation were double the 1985 values. Female condition at parturition and average foraging-trip duration (i.e., offspring-pro- visioning rate) appear to reflect prey availability. The similarity between years in mass increase suggests that females do not return to feed their pups until they replenish their own reserves. Antarctic fur seal females may have a limited ability to increase the relative time spent foraging because even in normal years only 5% of their time at sea is spent resting. This contrasts with northern fur seals, Callorhinus ursinus, which typically spend 17% of their time at sea inactive. Apparently these northern seals can increase their foraging effort by increasing the proportion of time spent foraging. This would account for the observed between-year difference in at-sea FMR of C. ursinus while foraging-trip duration remained fairly constant.

Reproductive and foraging energetics of pinnipeds: Implications for life history patterns

In his classic treatise on the evolution of pinniped breeding systems, Bartholomew (1970) identified terrestrial parturition and marine feeding as prerequisites for the evolution of polygyny. Such spatial and/or temporal separation of feeding from reproduction is a fundamental component of the reproductive biology of all pinnipeds, regardless of their breeding system. Adaptation to this constraint has resulted in reproductive patterns that incorporate varying periods of time spent fasting on the rookery and feeding at sea (Bonner, 1984; Kovacs and Lavigne, 1986). This chapter will examine the partitioning of energy during lactation and its acquisition while foraging. In this way the fundamental relationship between the foraging ecology and reproductive pattern of pinnipeds can be examined. Information about feeding is difficult to acquire, and conclusions are often of necessity inferred from records from relatively new instruments like time/depth recorders. Previous to the development of this technology, our understanding of foraging was based on measures such as the animal’s partitioning of time on land and at sea, and simple indices of feeding such as stomach content and scat analyses. Because of these constraints, much of what follows is speculative and must sometimes be based on a small number of species.

ENERGETICS OF A BENTHIC DIVER: SEASONAL FORAGING ECOLOGY OF THE AUSTRALIAN SEA LION,NEOPHOCA CINEREA

This research examines the foraging energetics and diving behavior of the Australian sea lion, Neophoca cinerea. We examine whether the foraging ecology of the Australian sea lion is typical for an animal that has evolved to exploit benthic habitats. Such a strategy is in marked contrast to those utilized by some seabirds and other pinnipeds that feed in the midwater, where travel and search components of the time at sea become more important. Onshore and at-sea field metabolic rates (FMR) were measured using doubly labeled water in lactating sea lions at Kangaroo Island, South Australia, during the winter of 1988 (early lactation, breeding season 1) and the summer of 1990 (early lactation, breeding season 2). Dive behavior was also measured with dataloggers during these seasons, as well as in the summer of 1991 (late lactation, breeding season 2). The foraging behavior of Neophoca cinerea indicated that it works hard to exploit benthic habitats in the waters around its breeding site. Sea lions maximized ...

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.