The effects of acclimation on thermal tolerance, desiccation resistance and metabolic rate in Chirodica chalcoptera (Coleoptera: Chrysomelidae)

Abstract

Despite much focus on species responses to environmental variation through space and time, many higher taxa and geographic areas remain poorly studied. We report the effects of temperature acclimation on thermal tolerance, desiccation rate and metabolic rate for adult Chirodica chalcoptera (Coleoptera: Chrysomelidae) collected from Protea nerifolia inflorescences in the Fynbos Biome in South Africa. After 7 days of acclimation at 12, 19 and 25 °C, critical thermal maxima (mean±s.e.: 41.8±0.2 °C in field-fresh beetles) showed less response (<1 °C change) to temperature acclimation than did the onset of the critical thermal minima (0.1±0.2, 1.0±0.2 and 2.3±0.2 °C, respectively). Freezing was lethal in C. chalcoptera (field-fresh SCP −14.6 °C) and these beetles also showed pre-freeze mortality. Survival of 2 h at −10.1 °C increased from 20% to 76% after a 2 h pre-exposure to −2 °C, indicating rapid cold hardening. Metabolic rate, measured at 25 °C and adjusted by ANCOVA for mass variation, did not differ between males and females (2.772±0.471 and 2.517±0.560 ml CO₂ h⁻¹_, respectively), but was higher in 25 °C-acclimated beetles relative to the field-fresh and 12 °C-acclimated beetles. Body water content and desiccation rate did not differ between males and females and did not respond significantly to acclimation. We place these data in the context of measured inflorescence and ambient temperatures, and predict that climate change for the region could have effects on this species, in turn possibly affecting local ecosystem functioning.

Introduction

The ways in which physiological responses vary through space and the extent to which phenotypic plasticity might effect a change in these responses over time are enjoying renewed interest, most notably because of concerns about climate change effects on biota, and an increase in the sophistication of molecular and genomic tools to investigate these questions (Feder and Mitchell-Olds, 2003; Hoffmann et al., 2003; Chown and Nicolson, 2004). In insects, spatially explicit work has revealed several significant patterns. First, responses to high and low temperature are decoupled, lower lethal temperature limits typically respond more strongly to acclimation and to natural selection than upper lethal limits, and it appears that phenotypic plasticity can account for much of the response shown by insects (reviewed in Chown and Nicolson, 2004; see also Ayrinhac et al., 2004; Hoffmann et al., 2005). Second, metabolic rate does not seem to vary with environmental temperature (Addo-Bediako et al., 2002), nor does it always scale as mass^0.75 (Lighton and Fielden, 1995). Third, desiccation resistance generally varies in a direction that is consistent with adaptive responses to environmental water availability (Edney, 1977; Gibbs et al., 1997; Addo-Bediako et al., 2001), and responds predictably to acclimation at given humidity conditions (Hoffmann, 1990; Sjursen et al., 2001).

These patterns are all controversial for different reasons. In the first case, several studies have shown that decoupling of upper and lower lethal limits is not typical of all species (Hoffmann et al., 2002; Sgrò and Blows, 2004), and most investigations are undertaken using model species, leaving several groups and geographic regions under-represented (Chown et al., 2002; Klok and Chown, 2003). As far as metabolic rate variation is concerned, the metabolic theory of ecology predicts that metabolic rate should covary with environmental temperature and should scale as mass^0.75 (Gillooly et al., 2001; Brown et al., 2004). In insects, this does not seem to be the case, although the data are equivocal (Lighton and Fielden, 1995; Chown and Gaston, 1999; Addo-Bediako et al., 2002), largely because several groups and areas are again under-represented amongst the information that is available (e.g. Duncan et al., 2002). In the last instance, the controversy concerns not so much the fact that desiccation resistance should vary with water availability, but rather which routes of water loss are likely to vary the most and how strong a temperature acclimation response is likely to be, if it is at all extant (Chown, 2002; Gibbs et al., 1998). Indeed, thermal acclimation effects on desiccation resistance have been investigated in only a few instances (Hoffmann, 1990; Hoffmann and Watson, 1993; Hoffmann et al., 2005).

A theme common to the debate in each of these fields is that whilst useful data on model organisms continue to accumulate apace, broader scale studies, which can usefully complement these investigations (see Kingsolver and Huey, 1998) are compromised by an absence of information from many areas and taxa, and by an absence of information on a variety of traits for the same species (Chown et al., 2002). Indeed, information on the full range of ecophysiological traits is available for only a handful of species (Chown and Nicolson, 2004). There are several ways in which these problems might be addressed (see e.g. Zachariassen et al., 1987), of which the accumulation of information on a variety of traits for poorly represented taxa from little studied environments is a significant one. This is particularly true for environments that are not considered “stressful”, and so have had little attention paid to their constituent species because “clear-cut”, significant responses are unexpected (for additional discussion see Feder et al., 1987).

In this paper, we therefore provide data on the responses of critical thermal limits, metabolic rate and desiccation resistance to temperature acclimation from a species that is a member of a diverse higher taxon, the Chrysomelidae, which is poorly represented in the physiological literature. This species also occurs in a geographic area that is not considered particularly climatically stressful–the Fynbos Biome of South Africa. Specifically, we determine: (i) whether the strength of the acclimation response is the same for both critical thermal minima and maxima; (ii) what, if any, is the extent of the response of desiccation resistance to treatment temperature; (iii) whether there is conservation of metabolic rate with given different treatment temperatures, and how the metabolic rate of this species compares with other similar-sized beetles. Rapid cold hardening in insects from environments that may not be thermally ‘extreme’ has not been widely investigated (Chown and Nicolson, 2004). Therefore, we include investigations of both cold hardiness and rapid cold hardening. Information on the microclimate of this species is provided because comprehension of the survival strategies of insects cannot be achieved without it (Baust and Rojas, 1985; Bale, 1991).