Summing the strokes: energy economy in northern elephant seals during large-scale foraging migrations

Abstract

Background: The energy requirements of free-ranging marine mammals are challenging to measure due to cryptic and far-ranging feeding habits, but are important to quantify given the potential impacts of high-level predators on ecosystems. Given their large body size and carnivorous lifestyle, we would predict that northern elephant seals (Mirounga angustirostris) have elevated field metabolic rates (FMRs) that require high prey intake rates, especially during pregnancy. Disturbance associated with climate change or human activity is predicted to further elevate energy requirements due to an increase in locomotor costs required to accommodate a reduction in prey or time available to forage. In this study, we determined the FMRs, total energy requirements, and energy budgets of adult, female northern elephant seals. We also examined the impact of increased locomotor costs on foraging success in this species.

Results: Body size, time spent at sea and reproductive status strongly influenced FMR. During the short foraging migration, FMR averaged 90.1 (SE = 1.7) kJ kg(-1)d(-1) - only 36 % greater than predicted basal metabolic rate. During the long migration, when seals were pregnant, FMRs averaged 69.4 (±3.0) kJ kg(-1)d(-1) - values approaching those predicted to be necessary to support basal metabolism in mammals of this size. Low FMRs in pregnant seals were driven by hypometabolism coupled with a positive feedback loop between improving body condition and reduced flipper stroking frequency. In contrast, three additional seals carrying large, non-streamlined instrumentation saw a four-fold increase in energy partitioned toward locomotion, resulting in elevated FMRs and only half the mass gain of normally-swimming study animals.

Conclusions: These results highlight the importance of keeping locomotion costs low for successful foraging in this species. In preparation for lactation and two fasting periods with high demands on energy reserves, migrating elephant seals utilize an economical foraging strategy whereby energy savings from reduced locomotion costs are shuttled towards somatic growth and fetal gestation. Remarkably, the energy requirements of this species, particularly during pregnancy, are 70-80 % lower than expected for mammalian carnivores, approaching or even falling below values predicted to be necessary to support basal metabolism in mammals of this size.

Keywords: Accelerometer; Aerobic dive limit; Body size; Disturbance; Field metabolic rate; Foraging; Hypometabolism; Locomotion; Pregnancy.

Fig. 1

Northern elephant seal (Mirounga angustirostris) mother with a young pup (1–2 d) and b pup just before weaning (25–28 d). Photo credits: D. Costa, M. Fowler

Fig. 2

Mass-specific field metabolic rates of northern elephant seals (Mirounga angustirostris) based on total number of flipper strokes executed during their foraging migrations, as a function of mass. Filled circles indicate seals carrying added drag during their short migrations. See text for equations

Fig. 3

Field metabolic rates of northern elephant seals (Mirounga angustirostris) compared to Kleiber [43] predictions of mammalian basal metabolic rate (BMR) (dashed red line) and Boyd [12] predictions of marine mammal field metabolic rate (FMR) (dashed grey line), as a function of mass. Compared to seals during their short migration, seals of similar average body mass had 23 % lower FMRs during the long migration according to the equation FMR*_LT = 5818 M^0.26

Fig. 4

Partitioning of ingested energy among work costs (grey tones) and production (warm tones) in foraging elephant seals (Mirounga angustirostris). Absolute costs for each seal are shown in the white panels (a), while proportions of total costs are averaged across the three groups in the grey panel (b), where ST = seals during the short foraging trip, LT = seals during the long foraging trip, and DG = seals with added drag during the short trip. Within each group, seals are listed from left to right in order of increasing body size. If locomotion costs in LT seals are similar to those of ST seals, basal metabolism would have to be suppressed by approximately 22 % in pregnant seals (see text)

Fig. 5

Flipper stroke rates were higher for northern elephant seals (Mirounga angustirostris) swimming normally during the short foraging trip (N = 13) than during the long foraging trip (N = 6). In comparison, seals swimming with added drag during their short trips (N = 3) stroked consistently faster than normally swimming seals during the same time (Welch two-sample t-test, t = −10.9982, df = 7.471, p < 0.001). Dark horizontal bars represent median (50^th percentile) values while the lower and upper limits of the boxes represent the 25^th and 75^th percentiles, respectively. Whiskers correspond to the 1.5 interquartile range, and points represent outliers

Fig. 6

Flipper stroking of northern elephant seals (Mirounga angustirostris) follows a predictable pattern along the course of each dive. The top panel shows one foraging dive during the short migration of seal X851, where depth is shown with corresponding swaying acceleration. Grey boxes outline approximately 2.5-min segments of flipper stroking, each representing one of the three main phases of a dive cycle: (a) descent, (b) foraging at depth, and (c) ascent. Note the consistent, high-frequency flipper stroking occurring during ascent, when elephant seals are working against their negative buoyancy at depth in order to surface