Seasonal variation in blood and muscle oxygen stores attributed to diving behavior, environmental temperature and pregnancy in a marine predator, the California sea lion.

Survival depends on an animal's ability to find and acquire prey. In diving vertebrates, this ability is directly related to their physiological capability (e.g. oxygen stores). We studied the seasonal variation in oxygen stores, body temperature and body condition in California sea lions (Zalophus californianus) (CSL) as a function of seasonal variation in temperature, primary productivity, diving behavior and reproductive stage. During summer, blood oxygen stores were significantly greater and muscle oxygen stores were significantly lower than in winter. Total oxygen stores, body condition and body temperature did not change between seasons but variations in body temperature were greater during summer. Changes in oxygen stores are partly attributed to diving behavior, temperature and pregnancy that could increase oxygen consumption. Blood and muscle oxygen stores appear to be influenced by reproductive state. Blood oxygen stores are more likely influenced by diving behavior and temperature than muscle oxygen stores.

Key questions in marine mammal bioenergetics.

Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as 'key' questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

Influence of hunting strategy on foraging efficiency in Galapagos sea lions.

The endangered Galapagos sea lion (GSL, Zalophus wollebaeki) exhibits a range of foraging strategies utilising various dive types including benthic, epipelagic and mesopelagic dives. In the present study, potential prey captures (PPC), prey energy consumption and energy expenditure in lactating adult female GSLs (n = 9) were examined to determine their foraging efficiency relative to the foraging strategy used. Individuals displayed four dive types: (a) epipelagic (<100 m; EP); or (b) mesopelagic (>100 m; MP) with a characteristic V-shape or U-shape diving profile; and (c) shallow benthic (<100 m; SB) or (d) deep benthic (>100 m; DB) with square or flat-bottom dive profiles. These dive types varied in the number of PPC, assumed prey types, and the energy expended. Prey items and their energetic value were assumed from previous GSL diet studies in combination with common habitat and depth ranges of the prey. In comparison to pelagic dives occurring at similar depths, when diving benthically, GSLs had both higher prey energy consumption and foraging energy expenditure whereas PPC rate was lower. Foraging efficiency varied across dive types, with benthic dives being more profitable than pelagic dives. Three foraging trip strategies were identified and varied relative to prey energy consumed, energy expended, and dive behaviour. Foraging efficiency did not significantly vary among the foraging trip strategies suggesting that, while individuals may diverge into different foraging habitats, they are optimal within them. These findings indicate that these three strategies will have different sensitivities to habitat-specific fluctuations due to environmental change.

Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

Intraspecific variation in feeding strategies of Galapagos sea lions: A case of trophic specialization.

The trophic behavior of marine predators varies according to the level of competition to which they are exposed. In general, populations that inhabit lower productivity systems face a strong intraspecific competition, which contributes to the development of different foraging strategies to maximize nutritional efficiency. Given the high trophic flexibility of Zalophus wollebaeki, this species is considered appropriate for the analysis of such behavior. Furthermore, this trophic flexibility has allowed them to persist in a seemingly marginal ecosystem. In this study, we used a comparative analysis of variables (diet and dive behavior) related to Z. wollebaeki trophic niche plasticity to better understand their foraging ecology, using techniques such scat analysis, satellite telemetry and complementarily an isotopic analysis. Scat analysis revealed intra-population variation in their diet, represented by prey from different environments (epipelagic and benthic). These results are supported by the animals' locations at sea and diving profiles. Global Positioning System (GPS) and time-depth recorder (TDR) records showed the existence of two groups, with differing feeding areas and diving behavior. Also the δ15N values showed differences in the trophic level at which the species fed. These results constitute a relevant finding in the evolutionary behavior of the species, showing that Z. wollebaeki has developed a high degree of foraging flexibility, thus increasing its survival rate in an ecosystem that is highly demanding in terms of resource availability.

Comparisons and Uncertainty in Fat and Adipose Tissue Estimation Techniques: The Northern Elephant Seal as a Case Study.

Fat mass and body condition are important metrics in bioenergetics and physiological studies. They can also link foraging success with demographic rates, making them key components of models that predict population-level outcomes of environmental change. Therefore, it is important to incorporate uncertainty in physiological indicators if results will lead to species management decisions. Maternal fat mass in elephant seals (Mirounga spp) can predict reproductive rate and pup survival, but no one has quantified or identified the sources of uncertainty for the two fat mass estimation techniques (labeled-water and truncated cones). The current cones method can provide estimates of proportion adipose tissue in adult females and proportion fat of juveniles in northern elephant seals (M. angustirostris) comparable to labeled-water methods, but it does not work for all cases or species. We reviewed components and assumptions of the technique via measurements of seven early-molt and seven late-molt adult females. We show that seals are elliptical on land, rather than the assumed circular shape, and skin may account for a high proportion of what is often defined as blubber. Also, blubber extends past the neck-to-pelvis region, and comparisons of new and old ultrasound instrumentation indicate previous measurements of sculp thickness may be biased low. Accounting for such differences, and incorporating new measurements of blubber density and proportion of fat in blubber, we propose a modified cones method that can isolate blubber from non-blubber adipose tissue and separate fat into skin, blubber, and core compartments. Lastly, we found that adipose tissue and fat estimates using tritiated water may be biased high during the early molt. Both the tritiated water and modified cones methods had high, but reducible, uncertainty. The improved cones method for estimating body condition allows for more accurate quantification of the various tissue masses and may also be transferrable to other species.

Individual foraging strategies reveal niche overlap between endangered galapagos pinnipeds.

Most competition studies between species are conducted from a population-level approach. Few studies have examined inter-specific competition in conjunction with intra-specific competition, with an individual-based approach. To our knowledge, none has been conducted on marine top predators. Sympatric Galapagos fur seals (Arctocephalus galapagoensis) and sea lions (Zalophus wollebaeki) share similar geographic habitats and potentially compete. We studied their foraging niche overlap at Cabo Douglas, Fernandina Island from simultaneously collected dive and movement data to examine spatial and temporal inter- and intra-specific competition. Sea lions exhibited 3 foraging strategies (shallow, intermediate and deep) indicating intra-specific competition. Fur seals exhibited one foraging strategy, diving predominantly at night, between 0-80 m depth and mostly at 19-22 h. Most sea lion dives also occurred at night (63%), between 0-40 m, within fur seals' diving depth range. 34% of sea lions night dives occurred at 19-22 h, when fur seals dived the most, but most of them occurred at dawn and dusk, when fur seals exhibited the least amount of dives. Fur seals and sea lions foraging behavior overlapped at 19 and 21 h between 0-30 m depths. Sea lions from the deep diving strategy exhibited the greatest foraging overlap with fur seals, in time (19 h), depth during overlapping time (21-24 m), and foraging range (37.7%). Fur seals foraging range was larger. Cabo Douglas northwest coastal area, region of highest diving density, is a foraging "hot spot" for both species. Fur seals and sea lions foraging niche overlap occurred, but segregation also occurred; fur seals primarily dived at night, while sea lions exhibited night and day diving. Both species exploited depths and areas exclusive to their species. Niche breadth generally increases with environmental uncertainty and decreased productivity. Potential competition between these species could be greater during warmer periods when prey availability is reduced.

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.

DDT in endangered Galapagos sea lions (Zalophus wollebaeki).

We characterize for the first time the presence of DDT and its metabolites in tropical Galapagos sea lions (Zalophus wolleabeki). ∑DDT concentrations in Galapagos sea lion pups sampled in 2005 and 2008 ranged from 16 to 3070 µg/kg lipid. Concentrations of ∑DDT in pups in 2008 averaged 525 µg/kg lipid and were 1.9 times higher than that (281 µg/kg lipid) detected in pups in 2005. These concentrations are lower than those reported in many pinnipeds elsewhere, comparable to those in Hawaiian monk seals, and higher than those in southern elephant seals. The health risk characterization showed that 1% of the male pups exceeded the p,p'-DDE toxic effect concentration associated with anti-androgenic effects reported in rats. The findings provide preliminary guidance on the relationship between DDT use and ecological impacts, serving as a reference point against which possible future impact of tropical DDT use can be assessed.

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 68(th) 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.