Factors affecting energy expenditure in a declining fur seal population.
ABSTRACT: Quantifying metabolic rates and the factors that influence them is key to wildlife conservation efforts because anthropogenic activities and habitat alteration can disrupt energy balance, which is critical for reproduction and survival. We investigated the effect of diving behaviour, diet and season on field metabolic rates (FMR) and foraging success of lactating northern fur seals (Callorhinus ursinus) from the Pribilof Islands during a period of population decline. Variation in at-sea FMR was in part explained by season and trip duration, with values that ranged from 5.18 to 9.68 W kg-1 (n?=?48). Fur seals experienced a 7.2% increase in at-sea FMR from summer to fall and a 1.9% decrease in at-sea FMR for each additional day spent at sea. There was no effect of foraging effort, dive depth or diet on at-sea FMR. Mass gains increased with trip duration and were greater in the fall compared with summer, but were unrelated to at-sea FMR, diving behaviour and diet. Seasonal increases in at-sea FMR may have been due to costs associated with the annual molt but did not appear to adversely impact the ability of females to gain mass on foraging trips. The overall high metabolic rates in conjunction with the lack of any diet-related effects on at-sea FMR suggests that northern fur seals may have reached a metabolic ceiling early in the population decline. This provides indirect evidence that food limitation may be contributing to the low pup growth rates observed in the Pribilof Islands, as a high metabolic overhead likely results in less available energy for lactation. The limited ability of female fur seals to cope with changes in prey availability through physiological mechanisms is particularly concerning given the recent and unprecedented environmental changes in the Bering Sea that are predicted to have ecosystem-level impacts.
Project description:Time and energy are the two most important currencies in animal bioenergetics. How much time animals spend engaged in different activities with specific energetic costs ultimately defines their likelihood of surviving and successfully reproducing. However, it is extremely difficult to determine the energetic costs of independent activities for free-ranging animals. In this study, we developed a new method to calculate activity-specific metabolic rates, and applied it to female fur seals. We attached biologgers (that recorded GPS locations, depth profiles, and triaxial acceleration) to 12 northern (Callorhinus ursinus) and 13 Antarctic fur seals (Arctocephalus gazella), and used a hierarchical decision tree algorithm to determine time allocation between diving, transiting, resting, and performing slow movements at the surface (grooming, etc.). We concomitantly measured the total energy expenditure using the doubly-labelled water method. We used a general least-square model to establish the relationship between time-activity budgets and the total energy spent by each individual during their foraging trip to predict activity-specific metabolic rates. Results show that both species allocated similar time to diving (~29%), transiting to and from their foraging grounds (~26-30%), and resting (~8-11%). However, Antarctic fur seals spent significantly more time grooming and moving slowly at the surface than northern fur seals (36% vs. 29%). Diving was the most expensive activity (~30 MJ/day if done non-stop for 24 hr), followed by transiting at the surface (~21 MJ/day). Interestingly, metabolic rates were similar between species while on land or while slowly moving at the surface (~13 MJ/day). Overall, the average field metabolic rate was ~20 MJ/day (for all activities combined). The method we developed to calculate activity-specific metabolic rates can be applied to terrestrial and marine species to determine the energetic costs of daily activities, as well as to predict the energetic consequences for animals forced to change their time allocations in response to environmental shifts.
Project description:Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at-sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at-sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep-diving foraging strategy all had similar values of at-sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade-offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.
Project description:We tagged 82 lactating northern fur seals (Callorhinus ursinus) with tri-axial accelerometers and magnetometers on two eastern Bering Sea islands (Bogoslof and St. Paul) with contrasting population trajectories. Using depth data, accelerometer data and spectral analysis we classified time spent diving (30%), resting (~7%), shaking and grooming their pelage (9%), swimming in the prone position (~10%) and two types of previously undocumented rolling behavior (29%), with the remaining time (~15%) unspecified. The reason for the extensive rolling behavior is not known. We ground-truthed the accelerometry signals for shaking and grooming and rolling behaviors--and identified the acceleration signal for porpoising--by filming tagged northern fur seals in captivity. Speeds from GPS interpolated data indicated that animals traveled fastest while in the prone position, suggesting that this behavior is indicative of destination-based swimming. Very little difference was found in the percentages of time spent in the categorical behaviors with respect to breeding islands (Bogoslof or St. Paul Island), forager type (cathemeral or nocturnal), and the region where the animals foraged (primarily on-shelf <200 m, or off-shelf > 200 m). The lack of significant differences between islands, regions and forager type may indicate that behaviors summarized over a trip are somewhat hardwired even though foraging trip length and when and where animals dive are known to vary with island, forager type and region.
Project description:Mercury contamination of oceans is prevalent worldwide and methylmercury concentrations in the mesopelagic zone (200-1000 m) are increasing more rapidly than in surface waters. Yet mercury bioaccumulation in mesopelagic predators has been understudied. Northern elephant seals (Mirounga angustirostris) biannually travel thousands of kilometres to forage within coastal and open-ocean regions of the northeast Pacific Ocean. We coupled satellite telemetry, diving behaviour and stable isotopes (carbon and nitrogen) from 77 adult females, and showed that variability among individuals in foraging location, diving depth and ?(13)C values were correlated with mercury concentrations in blood and muscle. We identified three clusters of foraging strategies, and these resulted in substantially different mercury concentrations: (i) deeper-diving and offshore-foraging seals had the greatest mercury concentrations, (ii) shallower-diving and offshore-foraging seals had intermediate levels, and (iii) coastal and more northerly foraging seals had the lowest mercury concentrations. Additionally, mercury concentrations were lower at the end of the seven-month-long foraging trip (n = 31) than after the two-month- long post-breeding trip (n = 46). Our results indicate that foraging behaviour influences mercury exposure and mesopelagic predators foraging in the northeast Pacific Ocean may be at high risk for mercury bioaccumulation.
Project description:Antarctic coastal polynyas are regions of persistent open water and are thought to be key bio-physical features within the sea-ice zone. However, their use by the upper trophic levels of ecosystems remains unclear. A unique bio-physical dataset recorded by southern elephant seals reveals that East Antarctic polynyas are a key winter foraging habitat for male seals. During their post-moult trips from Isles Kerguelen to the Antarctic continental shelf, a total of 18 out of 23 seals visited 9 different polynyas, spending on average 25?±?20% (up to 75%) of their total trip time inside polynyas. Changes in seal foraging and diving behaviours are observed inside polynyas as compared to outside polynyas. Two polynya usages by seals are observed for the inactive and active polynya phases, pointing to different seasonal peaks in prey abundance. During the active polynya phase, we link seal foraging behaviour to changes in the physical stability of the water-column, which likely impact the seasonal biological dynamics within polynyas.
Project description:BACKGROUND: The mammary gland undergoes a sophisticated programme of developmental changes during pregnancy/lactation. However, little is known about processes involving initiation of apoptosis at involution following weaning. We used fur seals as models to study the molecular process of involution as these animals display a unique mammary gland phenotype. Fur seals have long lactation periods whereby mothers cycle between secreting copious quantities of milk for 2 to 3 days suckling pups on land, with trips to sea alone to forage for up to 23 days during which time mammary glands remain active without initiating apoptosis/involution. RESULTS: We show the molecular basis by which alpha-lactalbumin (LALBA), a secreted milk protein, is absent in Cape fur seals and demonstrate an apoptotic function for LALBA when exposed to mammary cells. CONCLUSION: We propose that apoptosis does not occur in fur seal mammary glands due to lack of LALBA in fur seal milk, allowing evasion of involution during a foraging trip. Our work identifies LALBA as a milk factor that feeds back on the mammary gland to regulate involution.
Project description:In capital-breeding marine mammals, prey acquisition during the foraging trip coinciding with gestation must provide energy to meet the immediate needs of the growing fetus and also a store to meet the subsequent demands of lactation. Weddell seals (Leptonychotes weddellii) that give birth following the gestational (winter) foraging period gain similar proportions of mass and lipid as compared to females that fail to give birth. Therefore, any changes in foraging behavior can be attributed to gestational costs. To investigate differences in foraging effort associated with successful reproduction, twenty-three satellite tags were deployed on post-molt female Weddell seals in the Ross Sea. Of the 20 females that returned to the area the following year, 12 females gave birth and eight did not. Females that gave birth the following year began the winter foraging period with significantly longer and deeper dives, as compared to non-reproductive seals. Mid- to late winter, reproductive females spent a significantly greater proportion of the day diving, and either depressed their diving metabolic rates (DMR), or exceeded their calculated aerobic dive limit (cADL) more frequently than females that returned without a pup. Moreover, non-reproductive females organized their dives into 2-3 short bouts per day on average (BOUTshort; 7.06 ± 1.29 hr; mean ± 95% CI), whereas reproductive females made 1-2 BOUTshort per day (10.9 ± 2.84 hr), comprising one long daily foraging bout without rest. The magnitude of the increase in dive activity budgets and depression in calculated DMR closely matched the estimated energetic requirements of supporting a fetus. This study is one of the first to identify increases in foraging effort that are associated with successful reproduction in a top predator and indicates that reproductive females must operate closer to their physiological limits to support gestational costs.
Project description:While marine top predators can play a critical role in ecosystem structure and dynamics through their effects on prey populations, how the predators function in this role is often not well understood. In the Benguela region of southern Africa, the Cape fur seal (Arctocephalus pusillus pusillus) population constitutes the largest marine top predator biomass, but little is known of its foraging ecology other than its diet and some preliminary dive records. Dive information was obtained from 32 adult females instrumented with dive recorders at the Kleinsee colony (29°34.17' S, 16°59.80' E) in South Africa during 2006-2008. Most dives were in the depth range of epipelagic prey species (less than 50 m deep) and at night, reflecting the reliance of Cape fur seals on small, vertically migrating, schooling prey. However, most females also performed benthic dives, and benthic diving was prevalent in some individuals. Benthic diving was significantly associated with the frequency with which females exceeded their aerobic dive limit. The greater putative costs of benthic diving highlight the potential detrimental effects to Cape fur seals of well-documented changes in the availability of epipelagic prey species in the Benguela.
Project description:Background:Accurate time-energy budgets summarise an animal's energy expenditure in a given environment, and are potentially a sensitive indicator of how an animal responds to changing resources. Deriving accurate time-energy budgets requires an estimate of time spent in different activities and of the energetic cost of that activity. Bio-loggers (e.g., accelerometers) may provide a solution for monitoring animals such as fur seals that make long-duration foraging trips. Using low resolution to record behaviour may aid in the transmission of data, negating the need to recover the device. Methods:This study used controlled captive experiments and previous energetic research to derive time-energy budgets of juvenile Australian fur seals (Arctocephalus pusillus) equipped with tri-axial accelerometers. First, captive fur seals and sea lions were equipped with accelerometers recording at high (20 Hz) and low (1 Hz) resolutions, and their behaviour recorded. Using this data, machine learning models were trained to recognise four states-foraging, grooming, travelling and resting. Next, the energetic cost of each behaviour, as a function of location (land or water), season and digestive state (pre- or post-prandial) was estimated. Then, diving and movement data were collected from nine wild juvenile fur seals wearing accelerometers recording at high- and low- resolutions. Models developed from captive seals were applied to accelerometry data from wild juvenile Australian fur seals and, finally, their time-energy budgets were reconstructed. Results:Behaviour classification models built with low resolution (1 Hz) data correctly classified captive seal behaviours with very high accuracy (up to 90%) and recorded without interruption. Therefore, time-energy budgets of wild fur seals were constructed with these data. The reconstructed time-energy budgets revealed that juvenile fur seals expended the same amount of energy as adults of similar species. No significant differences in daily energy expenditure (DEE) were found across sex or season (winter or summer), but fur seals rested more when their energy expenditure was expected to be higher. Juvenile fur seals used behavioural compensatory techniques to conserve energy during activities that were expected to have high energetic outputs (such as diving). Discussion:As low resolution accelerometry (1 Hz) was able to classify behaviour with very high accuracy, future studies may be able to transmit more data at a lower rate, reducing the need for tag recovery. Reconstructed time-energy budgets demonstrated that juvenile fur seals appear to expend the same amount of energy as their adult counterparts. Through pairing estimates of energy expenditure with behaviour this study demonstrates the potential to understand how fur seals expend energy, and where and how behavioural compensations are made to retain constant energy expenditure over a short (dive) and long (season) period.
Project description:Across an individual's life, foraging decisions will be affected by multiple intrinsic and extrinsic drivers that act at differing timescales. This study aimed to assess how female Australian fur seals allocated foraging effort and the behavioural changes used to achieve this at three temporal scales: within a day, across a foraging trip and across the final six months of the lactation period. Foraging effort peaked during daylight hours (57% of time diving) with lulls in activity just prior to and after daylight. Dive duration reduced across the day (196 s to 168 s) but this was compensated for by an increase in the vertical travel rate (1500-1600 m·h(-1)) and a reduction in postdive duration (111-90 s). This suggests physiological constraints (digestive costs) or prey availability may be limiting mean dive durations as a day progresses. During short trips (<2.9 d), effort remained steady at 55% of time diving, whereas, on long trips (>2.9 d) effort increased up to 2-3 d and then decreased. Dive duration decreased at the same rate in short and long trips, respectively, before stabilising (long trips) between 4-5 d. Suggesting that the same processes (digestive costs or prey availability) working at the daily scale may also be present across a trip. Across the lactation period, foraging effort, dive duration and vertical travel rate increased until August, before beginning to decrease. This suggests that as the nutritional demands of the suckling pup and developing foetus increase, female effort increases to accommodate this, providing insight into the potential constraints of maternal investment in this species.