Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Predicting rate of oxygen consumption from heart rate while little penguins work, rest and play☆
Introduction
Recent studies have shown that heart rate (fH) can successfully be used as a proxy for the measurement of rate of oxygen consumption (V˙O2) and/or metabolic rate in free-ranging animals (Butler et al., 2004). Application of this method requires a calibration between fH and V˙O2 under controlled conditions. This is often obtained by subjecting an animal to a variable workload through exercise such as walking (Bevan et al., 1994), swimming (Butler et al., 1992) or flying (Ward et al., 2002). However, exercise is not the only method which has been used. The aim of these ‘calibration studies’ is not to examine the effects of exercise per se, but to elevate levels of fH and V˙O2 to those likely to be found under natural conditions in free-ranging animals and to describe a relationship between the two. For example, other studies have examined the relationships between fH and V˙O2 by varying ambient temperature (Froget, 2002, Morhardt and Morhardt, 1971), digestive state (McPhee et al., 2003) or both (Clark et al., 2005a).
A key finding of these studies is that the fH/V˙O2 relationship can vary under differing conditions, which underlines the importance of tailoring calibration procedures to the likely range of activities undertaken and conditions experienced by free-ranging animals. A series of examples illustrate this point. The fH/V˙O2 relationship has been found to vary if measured on different dates within a season in American kestrels (Falco sparverius, Gessaman, 1980). Relationships varied between seasons of the year in white tailed deer (Odocoileus virginianus, Holter et al., 1976), perhaps due to a reduction in heart mass and hence stroke volume during periods when the animals were less active. However, there was no significant difference in the relationship in macaroni penguins when inactive/fasting, active/breeding and inactive/moulting (Green et al., 2001, Green et al., 2005b). Some apparent seasonal changes may be due in part to changes in body mass and/or body composition and more recent models have emphasised the importance of correcting for body mass in studies of this type (Fahlman et al., 2004, Green et al., 2005a). Other studies which have detected differences between individuals and modes of locomotion may have drawn incorrect conclusions through the inappropriate incorporation of these body mass effects (Packard and Boardman, 1999).
Humans show different relationships between leg and arm exercise (Vokac et al., 1975) and during static or dynamic exercise (Maas et al., 1989). Juvenile steller sea lions (Eumetopias jubatus) appear to have different relationships while swimming and while digesting food (McPhee et al., 2003). There was no difference in the relationship while barnacle geese walked or swam (Nolet et al., 1992), but Ward et al. (2002) found differences between walking and flying in the same species. Conversely, both Bevan et al. (1995) and Green et al. (2005b) found no difference in the relationships when gentoo (Pygoscelis papua) and macaroni (Eudyptes chrysolophus) penguins walked or swam using their flippers (wings). In king penguins (Aptenodytes patagonicus), the relationship determined for penguins exposed to cold temperatures was different from that determined while the birds exercised (Froget et al., 2002). In addition to this, the nutritional state and body composition in king penguins has a profound and complex effect on these relationships (Fahlman et al., 2005, Fahlman et al., 2004, Froget et al., 2001). In lower vertebrates it is essential to include the effects of varying temperature in predictive models (Butler et al., 2002, Clark et al., 2006, Clark et al., 2005b).
In the present study we investigate the relationship between fH and V˙O2 in the little penguin (Eudyptula minor). With their large and varied geographical range (Williams, 1995) little penguins must adapt to challenging environments ranging from discontinuous bouts of foraging in cold water, fasting, walking long distances to nest sites, and incubating and brooding in nests and burrows at temperatures up to 43 °C (Ropert-Coudert et al., 2004). Our aim was to determine how the relationship between fH and V˙O2 in little penguins varies in response to changing levels of exercise, temperature and digestive status, with the ultimate objective of utilising this relationship to predict the V˙O2 of free-ranging animals.
Section snippets
Animals
All experiments were carried out with La Trobe University Ethics Committee approval (AEC 04/37(L)) and relevant wildlife permits. Twelve little penguins in six breeding pairs were obtained from Phillip Island Nature Park, Victoria, Australia. Penguins were transported by car to La Trobe University, Melbourne, Australia, where all experiments took place. The experiments were performed between September 9 and 21, 2004, which was during the pre-breeding/courtship phase in this year (Peter Dann,
Minimum and maximum rates
The little penguins remained calm while in the respirometer, whether resting, exercising or digesting meals. During exercise periods the birds adopted the same gait and body position observed in free-ranging birds walking from the sea to their nest sites (J.A. Green, personal observation). Minimum and maximum values for fH and V˙O2 are shown in Table 1. Preliminary analyses suggested that during feeding trials, fH and V˙O2 may have had insufficient time to return to minimum or resting levels so
Minimum rates, maximum rates and thermoneutrality
Rates of oxygen consumption have been measured several times in the little penguin (including the subspecies the white-flippered penguin, E. minor albosignata) and a range of results has been reported (Table 1). Maximum V˙O2 determined in the present study was less than that recorded by Pinshow et al. (1976), but their penguins were trained and walked at a maximum speed approximately 50% greater than that recorded in the present study. Walking aerobic scope (maximum V˙O2/minimum V˙O2) was
Acknowledgments
This article is dedicated to Russ Baudinette, who was not only a great and inspirational scientist but a great human being. He also introduced two of us (PBF and PJB) to little penguins. The authors would like to thank all those who assisted in feeding the penguins and the staff of Phillip Island Nature Park, who provided the penguins for this study, especially Marg Healy and Peter Dann.
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Presented as part of the Russell V. Baudinette Memorial Symposium held in Adelaide, Australia, 1–2 October 2005.
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Current address: School of Earth and Environmental Sciences, University of Adelaide, South Australia, 5005, Australia.