J Comp Physiol B (2017) 187:29–50 DOI 10.1007/s00360-016-1035-8 REVIEW Physiological constraints and energetic costs of diving behaviour in marine mammals: a review of studies using trained Steller sea lions diving in the open ocean David A. S. Rosen1 · Allyson G. Hindle1 · Carling D. Gerlinsky1 · Elizabeth Goundie1 · Gordon D. Hastie1 · Beth L. Volpov1 · Andrew W. Trites1 Received: 17 February 2016 / Revised: 26 August 2016 / Accepted: 13 September 2016 / Published online: 29 September 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract Marine mammals are characterized as having basis of diving behaviour further our understanding of the physiological specializations that maximize the use of oxy- potential scope for behavioural responses of marine mam- gen stores to prolong time spent under water. However, it mals to environmental changes, the energetic significance has been difficult to undertake the requisite controlled stud- of these adjustments, and the consequences of approaching ies to determine the physiological limitations and trade-offs physiological limits. that marine mammals face while diving in the wild under varying environmental and nutritional conditions. For the Keywords Diving physiology · Steller sea lions · past decade, Steller sea lions (Eumetopias jubatus) trained Metabolism · Foraging to swim and dive in the open ocean away from the physi- cal confines of pools participated in studies that investi- gated the interactions between diving behaviour, energetic The need to study diving metabolism costs, physiological constraints, and prey availability. Many of these studies measured the cost of diving to understand Marine mammals are well known for being able to remain how it varies with behaviour and environmental and physi- submerged for extended durations. The early studies of ological conditions. Collectively, these studies show that marine mammals (mainly phocid or “true” seals) inves- the type of diving (dive bouts or single dives), the level of tigated the anatomical features by which they managed underwater activity, the depth and duration of dives, and to do so. These include adaptations for withstanding the the nutritional status and physical condition of the animal intense pressures experienced at depth and greater relative affect the cost of diving and foraging. They show that dive on-board oxygen stores than their terrestrial counterparts, depth, dive and surface duration, and the type of dive result which allows them to remain active during submergence in physiological adjustments (heart rate, gas exchange) breath-holding. For example, elevated oxygen storage is that may be independent of energy expenditure. They also present in both circulating haemoglobin and the myoglobin demonstrate that changes in prey abundance and nutritional of their locomotor muscle tissues (Kooyman 1985). status cause sea lions to alter the balance between time Marine mammals also possess a series of physiologi- spent at the surface acquiring oxygen (and offloading CO2 cal specializations that allow them to maximize the use and other metabolic by-products) and time spent at depth of these oxygen stores and prolong their time submerged acquiring prey. These new insights into the physiological (Davis and Williams 2012; Andersen 1966; Butler and Jones 1997). These are traditionally grouped into a set of physiological adjustments known as the “dive response”, Communicated by I. D. Hume. comprising apnea, peripheral vasoconstriction, and brady- * David A. S. Rosen cardia. In the face of low blood oxygen pressure (PO2), [email protected] apnea maximizes the use of oxygen stores by delaying the impulse to return to the surface to breathe. The reduction of 1 Marine Mammal Research Unit, Institute for the Oceans and Fisheries, University of British Columbia, 2202 Main blood flow to “non-essential” tissues limits their local rates Mall, Vancouver, BC V6T 1Z4, Canada of oxygen consumption (and may also assist in myoglobin 1 3 30 J Comp Physiol B (2017) 187:29–50 store utilization within constricted muscle groups; Davis However, actual measurements of diving metabolism et al. 2004). Bradycardia is required to maintain central are sparse. This is partly because it is highly challenging blood pressure in light of these adjustments to peripheral to measure in wild animals—a notable exception being blood flow. These physiological and anatomical adaptations Weddell seals (Leptonychotes weddellii) that reliably are widespread among marine mammals—although not surface in ice holes (Kooyman et al. 1980). It is equally always to the same degree (Mottishaw et al. 1999; Davis logistically difficult to obtain these measures from trained 2014). animals in aquariums and similar facilities, given that The common response of reduced heart rate and pool depths cannot accommodate natural diving behav- restricted blood flow observed in early studies of div- iour. While some novel tests have been undertaken meas- ing physiology suggested that energy expenditure (i.e., uring the metabolism of harbour seals (Phoca vitulina) metabolism) while diving was low—certainly lower than swimming for extended linear distances in a pool, it is for active terrestrial mammals. The diving metabolic rate questionable whether this invokes the same physiological (DMR) has been directly measured in a few pinniped spe- responses as diving to depth (Gallon et al. 2007; Sparling cies, but rarely under conditions that approach natural div- et al. 2007b). In particular, the effect that pressure has on ing in the wild, and often under conditions that are euphe- the respiratory system may significantly alter physiol- mistically characterized as “forced diving” (e.g., Irving ogy, including how gases are managed (Scholander 1940; et al. 1935; Scholander et al. 1942). Although forced div- McDonald and Ponganis 2013; Fahlman et al. 2009). ing experiments provided novel and useful insight into Furthermore (as discussed later), once these operational marine mammal diving physiology, they likely repre- impediments have been solved, the actual calculation of sented an extreme example of the dive response that does metabolic rate while diving from gas exchange data is not not occur frequently in nature (in fact, some have referred as straightforward as it would first appear, and there are to these experiments as demonstrations of the “fear still varying opinions on how to experimentally estimate response”). We now appreciate that the dive response is the actual energy cost. not an automatic reflex, but rather a graded adjustment that To attempt to address this paucity of data, we undertook is under some degree of voluntary control (Butler 1988; a risky venture: we decided to study the diving metabo- Butler and Jones 1997). lism of trained Steller sea lions (Eumetopias jubatus) away Quantifying the metabolism of marine mammals while from the confines—and security—of a traditional labora- diving is important beyond the realm of comparative tory or aquarium setting. Sea lions (otariids) had, of course, physiology. The rate at which oxygen stores are depleted, been trained to operate freely in the open ocean before. together with the extent of these stores, allows an animal’s However, these were California sea lions (Zalophus cali- aerobic dive limit (ADL) to be calculated. The ADL is the fornianus), and most endeavours had been undertaken by maximum time that an animal can remain submerged rely- military organizations for security rather than research pur- ing solely on aerobic metabolism (Kooyman et al. 1983). poses (although a group at Moss Landing started a research Although the transition between aerobic and anaerobic program in 2005). In 2004, we began relocating trained metabolism during diving is likely not a distinct switch, the female Steller sea lions from the Vancouver Aquarium ADL is a critical comparative parameter for investigating (where they had been raised since pups) to the University the ecological physiology and behaviour of marine mam- of British Columbia’s Open Water Research Station, based mals. It not only defines the physiological constraints and at a marina in Port Moody, British Columbia. The concept costs of different foraging patterns, but it is also integral was to bridge the gap between the types of largely uncon- to formulating optimal foraging strategies (Carbone and trolled studies that could be conducted with wild animals in Houston 1996; Houston and Carbone 1992; Thompson and their natural environment and controlled experiments con- Fedak 2001). ducted with trained animals in an artificial (and physically In theory, determining the diving metabolism of a restricted) environment. marine mammal is relatively straightforward; it can be The Open Water Station is unique in that research- V˙ estimated from the rate of oxygen consumption ( O2) and ers can measure physiological, behavioural, and eco- V˙ carbon dioxide production ( CO2) over a dive event using logical variables during controlled experiments using sea the standard techniques of flow-through respirometry. This lions diving unrestrained in the open ocean environment. entails having the animal breathe into a semi-enclosed con- Although under trainer control, the sea lions perform tainer with a constant flow-through airstream upon return- dives to depths and for durations similar to wild animals ing to the surface after completing a dive. Consequently, (Merrick and Loughlin 1997), and can make foraging and V˙ V˙ the O2 and CO2 during the dive are inferred from data oxygen management decisions