Energetic cost of a meal in a frequent feeding lizard

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Abstract

Specific dynamic action (SDA) describes the rise in metabolism following feeding in animals and represents the energetic cost of digesting and assimilating a meal. The overall energetic cost of feeding may depend on whether or not an animal is post-absorptive at the time of feeding. The aim of this study was to compare the energetic cost of SDA due to feeding frequently compared with infrequently in the eastern water skink, Eulamprus quoyii. For similar quantities of food, repeated feeding incurred an energetic cost equal to 8.8% of the metabolizable energy of the meal (25 220 J), while single feeding incurred an energetic cost of 9.4% of the metabolizable energy of the meal (26 072 J). Experimental lizards maintained a rise in V̇O2 that was on average 1.8 times greater than the V̇O2 of the unfed controls over a 50-h interval as a result of feeding frequently. This prolonged rise in metabolism resulting from frequent feeding does not result in a higher energetic cost of SDA compared with that resulting from infrequent single feeding.

Introduction

Energy must be harvested by an organism from its environment to sustain life (Purves et al., 1992). Animals obtain energy by consuming food, but there are energetic costs associated with feeding; the energy spent in procuring a meal and specific dynamic action (SDA), which is the energetic cost associated with digestion and assimilation. SDA refers to the rise in metabolic rate that occurs in all animals as a result of the consumption of a meal (Kleiber, 1961). SDA incorporates the cost of digestion, absorption, and assimilation of food as well as prey handling and gastrointestinal growth (Cruz-Neto et al., 2001, Secor, 2001). SDA can be measured as the change in the rate of oxygen consumption (V̇O2) of an organism after feeding (Jobling, 1981, Wang et al., 2001). Typically V̇O2 reaches a peak soon after feeding, depending on size and composition of the meal, before gradually decreasing to prefeeding values (Jobling, 1981, Secor and Phillips, 1997). The duration of SDA and the peak V̇O2 achieved help to define the energetic cost of feeding and are, therefore, important ecological factors that can be quantified experimentally (Jobling, 1981).

The largest factorial changes in metabolism following feeding occur in large reptiles that feed infrequently (Wang et al., 2001). For example, SDA in the python (Python molurus) elicits an increase in V̇O2 that is greater than that resulting from muscular exercise (Secor and Diamond, 1997).

Comparative studies of SDA have used the response of fasted animals to a single meal to determine the energetic cost of digestion and assimilation (Jobling, 1981, Janes and Chappell, 1995, Sievert and Bailey, 2000). While this method may offer an accurate estimation of SDA for animals that feed infrequently, such as large sit-and-wait predators, it may be less accurate for animals that feed frequently. Most lizards, for example, typically never have completely empty guts when active (Halliday and Adler, 1987, Greer, 1989) and may therefore experience SDA for long periods. Hence, it was the aim of this study to compare the SDA in a lizard resulting from frequent feeding to that resulting from a single meal.

The concept of frequent and infrequent feeding can be problematic (Secor, 2001). While an animal that feeds weekly may be considered a frequent feeder when compared with an animal that feeds monthly, the same animal may be considered an infrequent feeder compared with an animal that feeds daily. In this study the term frequent feeding, as applied to the feeding habit of lizards, describes feeding while under the influence of an SDA elicited by a previous meal.

The omnivorous lizard Eulamprus quoyii (family: Scincidae) was used as an experimental model as it readily feeds in captivity (Weigel, 1988). We measured the V̇O2 in E. quoyii after they consumed mealworms (Tenebrio molitor), either as a single meal or as several small meals, to determine whether the rise in V̇O2 was sustained as a result of feeding behaviour, and to enable the calculation of the relative contribution of SDA to the resting metabolism of E. quoyii.

Section snippets

Animal maintenance and collection

Twenty-eight adult Eulamprus quoyii were captured by noosing (Simmons, 1987) in coastal bushland near Maroubra Beach, Sydney, (33°58′S, 151°16′E) in May, 2001. Lizards were housed individually in 450 mm×350 mm glass aquaria in a temperature regulated room at 20 °C. A 40 W light bulb, placed at one end of each aquarium, created a temperature gradient, with 41 °C at the warm end and 21 °C at the cool end. The heating lights were on from 09.00 h to 18.30 h. Room lights were set to a 12:12

Assimilation efficiency of energy (AE)

The average dry matter content of mealworms in this study was 41.0±1.1%. Gross energy content of mealworms was 27.7±0.4 kJ per gram of dry matter. The AE of E. quoyii fed six mealworms was 85.7±1.3%.

SDA in response to single feeding

The body mass of the experimental group (mean: 26.9 g) was not significantly different from that of the controls (mean: 27.0 g; F1,10=0.002, P=0.96) at the start of the experiment. V̇O2 changed significantly over time in both the experimental and control groups (experimental: F7,39=6.437, P<0.01;

Discussion

The lizard controls in both experimental treatments experienced significant variations in V̇O2 over time. These variations are the result of an endogenous circadian rhythm in the resting metabolic rate of E. quoyii which persists in the absence of an external light cue, but is dampened by constant light (Iglesias, 2001). All lizards showed similar variations in V̇O2 through time as a result of these circadian rhythms. However, V̇O2 was significantly greater in the digesting lizards compared

Acknowledgements

We thank K. Robert, J. Herbert, J. Sparrow, K. Rogers and C. Brown for all their help and advice. We also thank G. Packard for advice on statistics and S. Abubla without whom this study would never have taken place. This research had the approval of the NSW National Parks and Wildlife Service, and the University of Sydney Animal Care and Ethics Committee (LO4/5-2001/1/3380).

References (26)

  • S.M. Secor et al.

    Specific dynamic action of a large carnivorous lizard, Varanus albigularis

    Comp. Biochem. Physiol. A

    (1997)
  • R. Spencer et al.

    The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

    Comp. Biochem. Physiol. A

    (1998)
  • A.F. Bennett et al.

    Thermal relations of some Australian skinks (Sauria: Scincidae)

    Copeia

    (1986)
  • A.F. Bennett et al.

    Metabolism

  • A.P. Cruz-Neto et al.

    Energetic and physiological correlates of prey handling and ingestion in lizards and snakes

    Comp. Biochem. Physiol. A

    (2001)
  • A. Gorecki

    The adiabatic bomb calorimeter

  • A.E. Greer

    The Biology and Evolution of Australian Lizards

    (1989)
  • T. Halliday et al.

    The Encyclopedia of Reptiles and Amphibians

    (1987)
  • Iglesias, S., 2001. Specific dynamic action (SDA) in the lizard Eulamprus quoyii. Honours Thesis, University of Sydney,...
  • D.N. Janes et al.

    The effect of ration size and body size on specific dynamic action in Adele penguin chicks, Pygoscelis adeliae

    Physiol. Zool.

    (1995)
  • M. Jobling

    The influences of feeding on the metabolic rate of fishes: a short review

    J. Fish. Biol.

    (1981)
  • M. Kleiber

    The Fire of Life: An Introduction into Animal Energetics

    (1961)
  • J. Overgaard et al.

    The effects of fasting duration on the metabolic response to feeding in Python molurus: an evaluation of the energetic costs associated with gastrointestinal growth and upregulation

    Physiol. Biochem. Zool.

    (2002)
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