Intrinsic and extrinsic influences on standard metabolic rates of three species of Australian otariid
Volume 5 • 2017
10.1093/conphys/cow074
Research article
Intrinsic and extrinsic influences on
standard metabolic rates of three species
of Australian otariid
Monique A. Ladds1,*, David J. Slip1,2 and Robert G. Harcourt1
1
2
Marine Predator Research Group, Department of Biological Sciences, Macquarie University, North Ryde, NSW 2113, Australia
Taronga Conservation Society Australia, Bradley’s Head Road, Mosman, NSW 2088, Australia
*Corresponding author: Marine Predator Research Group, Department of Biological Sciences, Macquarie University, North Ryde, NSW 2113,
Australia. Tel: +61 298507980. Email:
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The study of marine mammal energetics can shed light on how these animals might adapt to changing environments.
Their physiological potential to adapt will be influenced by extrinsic factors, such as temperature, and by intrinsic factors,
such as sex and reproduction. We measured the standard metabolic rate (SMR) of males and females of three Australian
otariid species (two Australian fur seals, three New Zealand fur seals and seven Australian sea lions). Mean SMR ranged
from 0.47 to 1.05 l O2 min−1, which when adjusted for mass was from 5.33 to 7.44 ml O2 min−1 kg−1. We found that
Australian sea lion mass-specific SMR (sSMR; in millilitres of oxygen per minute per kilogram) varied little in response to
time of year or moult, but was significantly influenced by sex and water temperature. Likewise, sSMR of Australian and
New Zealand fur seals was also influenced by sex and water temperature, but also by time of year (pre-moult, moult or
post-moult). During the moult, fur seals had significantly higher sSMR than at other times of the year, whereas there was
no discernible effect of moult for sea lions. For both groups, females had higher sSMR than males, but sea lions and fur
seals showed different responses to changes in water temperature. The sSMR of fur seals increased with increasing water
temperature, whereas sSMR of sea lions decreased with increasing water temperature. There were no species differences
when comparing animals of the same sex. Our study suggests that fur seals have more flexibility in their physiology than
sea lions, perhaps implying that they will be more resilient in a changing environment.
Key words: Metabolic rate, otariid, sex, water temperature
Editor: Steven Cooke
Received 30 June 2016; Revised 15 December 2016; Editorial Decision 18 December 2016; accepted 9 January 2017
Cite as: Ladds MA, Slip DJ, Harcourt RG (2017) Intrinsic and extrinsic influences on standard metabolic rates of three species of Australian
otariid. Conserv Physiol 5(1): cow074; doi:10.1093/conphys/cow074.
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Introduction
Predicted global climate change is already altering the marine
environment and will subsequently affect the animals that
live and hunt within its bounds (Simmonds and Isaac, 2007).
Some of the changes expected include increasing ocean temperatures and changes to seasonal oceanic processes that will
be likely to affect the distribution of fish assemblages within
the marine environment (Learmonth et al., 2006; Schumann
et al., 2013). Pinnipeds may be particularly susceptible to
these changes if their prey distribution alters such that they
have to travel further or dive deeper to obtain food
(Staniland et al., 2007) or if the marine environment warms
to such an extent that they cannot thermoregulate effectively
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© The Author 2017. Published by Oxford University Press and the Society for Experimental Biology.
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Research article
Conservation Physiology • Volume 5 2017
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(Boyles et al., 2011). Thus, in order to predict how changes
in environmental conditions might impact on pinnipeds it is
important to understand how different groups use their
energy stores over a range of environmental conditions
(Canale and Henry, 2010). Understanding how much flexibility pinnipeds have in order to adapt to the changing conditions can be, in part, met through studying their energetics
(Geiser and Turbill, 2009; Canale and Henry, 2010).
The study of energetics provides information about the
needs of pinnipeds and the cost of satisfying those needs
(Williams and Yeates, 2004). Survival requires the maintenance of an overall positive energy balance, satisfied by
obtaining more energy than is expended. Energy expenditure
is most accurately estimated by determining metabolic rates,
and these can vary over seasons and years, with body mass
accounting for most of this variation for mammals (Kleiber,
1947; McNab, 2008). Pinniped energy expenditure is also
influenced by intrinsic factors, such as activity, reproduction
(preparation for and recovery from the energetic demands of
the breeding season), moult and sex, and extrinsic factors,
such as temperature and photoperiod, can also contribute to
some of this variation. These factors have been investigated
in a wide range of phocid (e.g. Rosen and Renouf, 1995;
Boily and Lavigne, 1997; Ochoa-Acuña et al., 1998;
Sparling et al., 2006) and otariid seals (e.g. Costa and Gales,
2003; Williams et al., 2007; Ladds et al., 2016) but have not
shown any consistent relationships among species.
Harbour seals (Phoca vitulina) demonstrate sex and age
variation, with metabolic rates declining with age, females
faster than males, and they experience metabolic depression
during pre- and post-moult stages (Rosen and Renouf,
1995). In contrast, grey seals (Halichoerus grypus) have their
highest metabolic rate during winter and they increase,
rather than depress, their metabolic rate during the moult
(Boily and Lavigne, 1997). Within otariids there appear to
be clear seasonal patterns in metabolic rate of fur seals
(Dalton et al., 2015), although no effect of reproduction or
season has been found for sea lions (Williams et al., 2007).
The processes that underlie these variations in response to
changing environmental conditions are not well understood,
and it is clear that the responses vary greatly betw (...truncated)