Temperature-dependence of metabolic rate in Glossina morsitans morsitans (Diptera, Glossinidae) does not vary with gender, age, feeding, pregnancy or acclimation

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Abstract

While variation in metabolic rate at a single temperature can occur for a variety of reasons and the effect of temperature is well established in insects, within-generation variation of metabolic rate-temperature relationships has been relatively poorly explored. In this study, we investigate the effects of gender, age, feeding and pregnancy, as well as three acclimation temperatures (19, 24, 29 °C), on standard metabolic rate and its temperature-dependence within post-developmental (i.e. non-teneral) adult G. morsitans morsitans. Although most of the independent variables influenced metabolic rate at a single test temperature (P<0.001 in most cases), and cold-acclimation resulted in significant up-regulation of metabolic rate at all test temperatures relative to 24 and 29 °C acclimation (P<0.0001), mass-independent metabolic rate-temperature relationships were surprisingly invariant over all experimental groups (P>0.05 in all cases). Slopes of log10 metabolic rate (ml CO2 h−1) against temperature (°C) ranged from a minimum of 0.03035 (±S.E.=0.003) in young fasted females to a maximum of 0.03834 (±0.004) in mature fasted males. These findings have implications for predicting the metabolic responses of tsetse flies to short-term temperature variation and may also have applications for modelling tsetse population dynamics as a function of temperature.

Introduction

Metabolic rate may be defined as the summation of sub-cellular, cellular, and organism-level processes which require ATP (Hochachka et al., 2003). As such, metabolic rate represents the costs of living in a specific environment and may in turn provide insight into the evolution of life histories across a range of environments (Chown and Gaston, 1999). For this reason and because metabolic rate estimates can be readily obtained, there has been considerable attention paid to metabolic rate and its variation for many years (reviewed in McNab, 2002; Chown and Nicolson, 2004). Much of this work has been concerned with allometry (scaling) and the effects of temperature on metabolic rate. The recent development of a ‘metabolic theory of ecology’ (Brown et al., 2004), which is a general theory apparently explaining the scaling of metabolic rate across all taxa, much of the variation in life histories of organisms, and global-scale variation in diversity, has stimulated renewed interest in metabolic rate and its variation.

In insects, metabolic rate may vary for several reasons, of which the most commonly accepted are size (Lighton and Fielden, 1995), activity (Bartholomew and Lighton, 1985; Reinhold, 1999), and ambient temperature (Keister and Buck, 1964). However, metabolic rate can vary for other reasons too. For example, age and ontogeny, diapause, gender, feeding status, reproductive status, time of day and season can all exercise a considerable influence on metabolic rate (Chown and Nicolson, 2004). Over larger scales, metabolic rate can also vary adaptively, principally in two possible ways. First, a reduction in metabolic rate is often found as a response to xeric conditions, and is thought to function as a water conservation mechanism through a reduction in respiratory water loss (Edney, 1977; Chown, 2002). Second, cold climate (usually high latitude or altitude) populations may show elevated metabolic rates relative to warm climate populations when tested at similar temperatures, which is widely known as temperature compensation (Hazel and Prosser, 1974) or metabolic cold adaptation (MCA, Chown and Gaston, 1999). Although controversial (e.g. Clarke, 2003) MCA may be beneficial to insects by enabling them to complete growth, development and reproduction at relatively cooler temperatures (Chown and Gaston, 1999).

Metabolic rate and its temperature-dependence (or rate-temperature (RT) relationships) are also responsive to environmental variation, and the metabolic response to temperature can differ between populations and between species (Scholander et al., 1953; Sømme and Block, 1991; Addo-Bediako et al., 2002). In general, however, the patterns in and processes underlying variation in RT relationships have not been systematically explored for insects, although variation of metabolic rate with temperature has been widely documented (Keister and Buck, 1964; Chown and Nicolson, 2004). Nonetheless, there have been some comparative studies. At the intraspecific level, Berrigan and Partridge (1997) found no relationship between the slope of the RT relationship and latitude in Drosophila melanogaster. By contrast, Chown et al. (1997) documented systematic changes in the RT relationship among populations of weevils on sub-Antarctic Marion Island such that the higher elevation populations tended to have reduced slopes than those at lower elevations. At the interspecific level, Addo-Bediako et al. (2002) found an increase in the slope of the RT relationship with increasing latitude in northern (but not southern) hemisphere species. They suggested that hemispheric variation in the extent of latitudinal change of the RT relationship might be a consequence of more variable environments in the northern than in the southern hemispheres.

Thus, it is clear that comprehension of the nature and extent of variation in RT relationships can provide considerable insight into the responses of organisms to their environments and how these responses influence variation in diversity at a variety of hierarchical levels. Nowhere has this become more clear than in the recent debate regarding the underlying causes of temperature-dependence of metabolic rate and their consequences for the metabolic theory of ecology (Gillooly et al., 2001; Clarke, 2004; Clarke and Fraser, 2004). Because variation in the temperature-dependence of metabolic rate must, at least to some extent, be a function of natural selection (Hochachka and Somero, 2002; Clarke, 2004), understanding this variation at a population level is of considerable importance in the context of the way in which the environment influences RT relationships. Indeed, Bennett (1987) pointed out that, despite its importance for understanding the evolution of physiological responses, inter-individual variation is surprisingly poorly investigated.

In this paper we therefore explore the effects of gender, feeding status, pregnancy and age on metabolic rate and its temperature-dependence in the tsetse fly Glossina morsitans morsitans (Diptera, Glossinidae). In addition, using three acclimation temperatures, we investigate the influence of temperature on metabolic rate and RT relationships. Our aim is not simply to determine the extent of metabolic rate variation with these factors, but more importantly to determine whether they influence the R-T relationship. In choosing a tsetse fly as a model organism, we recognize that it is one of a group of vectors of trypanosomes that can infect both humans and animals, which are therefore of considerable medical and socio-economic importance (Leak, 1999). Although metabolic rate in tsetse has received considerable attention, both in the laboratory (Rajagopal and Bursell, 1966; Taylor, 1977a, Taylor, 1977b, Taylor, 1978a, Taylor, 1978b; Terblanche et al., 2004) and in the field (Taylor, 1978b; Hargrove and Coates, 1990), variation in the temperature-dependence of tsetse metabolic rate is relatively poorly understood. Recent models of tsetse population dynamics typically include the effects of temperature on various life-history parameters (Hargrove, 2004), many of which (at least those associated with production—see Kozłowksi and Gawelczyk, 2002) are influenced by metabolic rate. These models necessarily simplify temperature effects across various physiological stages and cohorts, although the extent to which such assumptions are valid is not known. Thus an additional goal of this work is to determine whether these simplifying assumptions are realistic.

Section snippets

Study animals and laboratory conditions

Pupae of Glossina morsitans morsitans Westwood (Diptera, Glossinidae) were obtained from the laboratory colony maintained at the Entomology Unit, FAO/IAEA Agriculture and Biotechnology Laboratory, Seibersdorf, International Atomic Energy Agency, Vienna, Austria. Gene diversities over four mitochondrial loci in these laboratory flies are within the range of six field populations (Wohlford et al., 1999). Similarly, microsatellite diversities are homogeneous among two laboratory strains and six

Gender and feeding status effects in young flies

Body mass and test temperature both had a significant positive influence on metabolic rate (Table 1, Table 2; Fig. 2). Furthermore, metabolic rate (throughout we use this term to mean metabolic rate corrected for mass in the GLM) was significantly affected by gender in G. m. morsitans at all test temperatures when flies were in the fasted state, although in the fed state males had lower metabolic rates than females only at 24 and 28 °C. Thus, there were significant interactions between gender

Discussion

Several previous studies have investigated metabolic rate in adult Glossina species (Rajagopal and Bursell, 1966; Taylor, 1977b, Taylor, 1978a; Hargrove and Coates, 1990; Terblanche et al., 2004). In G. m. morsitans and G. pallidipes, feeding, pregnancy and maturation elicit increases in resting metabolic rate (Rajagopal and Bursell, 1966; Taylor, 1977b; Terblanche et al., 2004). Fasted teneral male G. m. orientalis (mean individual mass of approximately 16.6 mg, estimated from Rajagopal and

Acknowledgments

We thank Larissa Heyns for laboratory assistance. This work was funded by an NIH Grant AI- 52456 to E.S. Krafsur. Elliot Krafsur, Jacques Deere, Susana Clusella Trullas, Saskia Goldberg, Jeanne Gouws and two anonymous reviewers provided useful comments on an earlier version of this manuscript.

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    Present address: School of Life Sciences, Box 874501, Arizona State University, Tempe, AZ 85287-4501, USA.

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