Blood Oxygen Depletion Is Independent of Dive Function in a Deep Diving Vertebrate, the Northern Elephant Seal

Jessica U Meir,Paul J Ponganis,Patrick W Robinson,L Ignacio Vilchis,Gerald L Kooyman,Daniel P Costa

doi:10.1371/journal.pone.0083248

Abstract

Although energetics is fundamental to animal ecology, traditional methods of determining metabolic rate are neither direct nor instantaneous. Recently, continuous blood oxygen (O2) measurements were used to assess energy expenditure in diving elephant seals (Mirounga angustirostris), demonstrating that an exceptional hypoxemic tolerance and exquisite management of blood O2 stores underlie the extraordinary diving capability of this consummate diver. As the detailed relationship of energy expenditure and dive behavior remains unknown, we integrated behavior, ecology, and physiology to characterize the costs of different types of dives of elephant seals. Elephant seal dive profiles were analyzed and O2 utilization was classified according to dive type (overall function of dive: transit, foraging, food processing/rest). This is the first account linking behavior at this level with in vivo blood O2 measurements in an animal freely diving at sea, allowing us to assess patterns of O2 utilization and energy expenditure between various behaviors and activities in an animal in the wild. In routine dives of elephant seals, the blood O2 store was significantly depleted to a similar range irrespective of dive function, suggesting that all dive types have equal costs in terms of blood O2 depletion. Here, we present the first physiological evidence that all dive types have similarly high blood O2 demands, supporting an energy balance strategy achieved by devoting one major task to a given dive, thereby separating dive functions into distinct dive types. This strategy may optimize O2 store utilization and recovery, consequently maximizing time underwater and allowing these animals to take full advantage of their underwater resources. This approach may be important to optimizing energy expenditure throughout a dive bout or at-sea foraging trip and is well suited to the lifestyle of an elephant seal, which spends > 90% of its time at sea submerged making diving its most “natural” state.

Highlights

Energy expenditure is critical to determining an animal’s role within its ecosystem, from establishing a species’ overall activity budget to assessing reproductive and foraging costs or physiological capabilities
For each electrode site, the models assessing the fixed effect of dive type alone had an Akaike weight below the confidence set, resulting in exclusion as a candidate model and indicating that dive type alone cannot be considered a plausible explanation for blood O2 depletion
Our results demonstrate that in routine dives (. 10 min in duration) of elephant seals, the blood O2 store is significantly depleted to a similar range, irrespective of dive type or dive duration (Fig 1)

Summary

Introduction

Energy expenditure (metabolic rate) is critical to determining an animal’s role within its ecosystem, from establishing a species’ overall activity budget to assessing reproductive and foraging costs or physiological capabilities. Methods ranging from doubly-labeled water techniques [1] or proxies including indices of activity level (e.g. accelerometry) [2] and correlations to alternative parameters (e.g. heart rate) [3] have been used in numerous species to assess energetic costs. None of these methods, provide a direct and instantaneous measure of metabolic rate. Despite numerous reports on the behavior and ecology of diverse divers and a growing body of physiological diving data, we still do not have a clear understanding of how diving behavior affects energy expenditure and metabolic rate in air-breathing vertebrates. A more comprehensive strategy integrating dive behavior and physiology will provide a more complete understanding of the ecology and conservation needs of these remarkable organisms

Methods

Results

Conclusion