Forced into an ecological corner: Round-the-clock deep foraging on small prey by elephant seals

Abstract

Small mesopelagic fishes dominate the world's total fish biomass, yet their ecological importance as prey for large marine animals is poorly understood. To reveal the little-known ecosystem dynamics, we identified prey, measured feeding events, and quantified the daily energy balance of 48 deep-diving elephant seals throughout their oceanic migrations by leveraging innovative technologies: animal-borne smart accelerometers and video cameras. Seals only attained positive energy balance after feeding 1000 to 2000 times per day on small fishes, which required continuous deep diving (80 to 100% of each day). Interspecies allometry suggests that female elephant seals have exceptional diving abilities relative to their body size, enabling them to exploit a unique foraging niche on small but abundant mesopelagic fish. This unique foraging niche requires extreme round-the-clock deep diving, limiting the behavioral plasticity of elephant seals to a changing mesopelagic ecosystem.

Fig. 1. Mandible accelerometers with satellite tracking quantify spatiotemporal foraging intensity in ocean-migrating female northern elephant seals.

(A) Geographic distribution of number of feeding event along migration routes (n = 48 in 2011 to 2018 for this study), which is representative of our previously collected large dataset [n = 209 in 2004 to 2010; shown as yellow lines in the circular inset, replicated with permission from (69)]. Density distribution of foraging depths plotted against (B) time of the day and (C) bathymetry, and (D) aligned with water temperature and dissolved oxygen concentration. Density distribution of time-series (E) daily total number and (F) daily change in number of feeding event throughout migrations.

Fig. 2. Smart animal-borne video system confirms that seals predominantly forage on small fish in pelagic waters.

(A) Pelagic foragers in red [observed in n = 45 of 48 seals, representative data for one seal (2017_U20)] encountered small fish, whereas benthic foragers in blue [observed in only n = 3 of 48 seals, representative data for one seal (2017_5712)] encountered large fish (table S1). (B) Along migration routes, the video recording locations (larger open circles) were located at the farthest points from the colony due to the delay timer of 36 days. As in (A), note that video was recorded for only 1 min per dive (red or blue segments on depth plot), when the criteria of depth (400 m) and acceleration triggers (black lines) were met. These trigger settings maximized the video coverage of foraging dives, under the limited video recording capacity of each tag (4 hours). See movies S1 to S5 for original movies, where seal’s snout and whiskers are present in the camera frame, as noted in the bottom left still image. All prey footage lists are available in the Supplementary Materials (movies S2 and S5); the lists with higher resolution images are also available in the ADS (Arctic Data archive System) of the National Institute of Polar Research (https://ads.nipr.ac.jp/dataset/A20210316-001).

Fig. 3. Seals must spend most of the day foraging to achieve a sufficient number of feeding event for positive energy balance.

(A) Density plot of foraging time versus number of feeding event, together with a fitted exponential curve from the 45 seals that adopted pelagic foraging on small fish. (B) 3D relationship of drift rate changes (i.e., index of lipid gain rate; z axis) projected against daily foraging time and the number of feeding event, showing how lipid gain depends on foraging time and success.

Fig. 4. Interspecies allometry highlights that female northern elephant seals have high physiological diving capacity relative to body mass.

The maximum dive depth [as an index of physiological diving capacity (15)] of female northern elephant seals is (A) listed with all other diving mammals known to forage in the North Pacific and (B) plotted against body mass. A full species list and references are available in table S3.