Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): Implications for forecasting climate change impacts

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Abstract

For tsetse (Glossina spp.), the vectors of human and animal trypanosomiases, the physiological mechanisms linking variation in population dynamics with changing weather conditions have not been well established. Here, we investigate high- and low-temperature tolerance in terms of activity limits and survival in a natural population of adult Glossina pallidipes from eastern Zambia. Due to increased interest in chilling flies for handling and aerial dispersal in sterile insect technique control and eradication programmes, we also provide further detailed investigation of low-temperature responses. In wild-caught G. pallidipes, the probability of survival for 50% of the population at low-temperatures was at 3.7, 8.9 and 9.6 °C (95% CIs: ±1.5 °C) for 1, 2 and 3 h treatments, respectively. At high temperatures, it was estimated that treatments at 37.9, 36.2 and 35.6 °C (95% CIs: ±0.5 °C) would yield 50% population survival for 1, 2 and 3 h, respectively. Significant effects of time and temperature were detected at both temperature extremes (GLZ, p<0.05 in all cases) although a time–temperature interaction was only detected at high temperatures (p<0.0001). We synthesized data from four other Kenyan populations and found that upper critical thermal limits showed little variation among populations and laboratory treatments (range: 43.9–45.0 °C; 0.25 °C/min heating rate), although reduction to more ecologically relevant heating rates (0.06 °C/min) reduce these values significantly from ∼44.4 to 40.6 °C, thereby providing a causal explanation for why tsetse distribution may be high-temperature limited. By contrast, low-temperature limits showed substantial variation among populations and acclimation treatments (range: 4.5–13.8 °C; 0.25 °C/min), indicating high levels of inter-population variability. Ecologically relevant cooling rates (0.06 °C/min) suggest tsetses are likely to experience chill coma temperatures under natural conditions (∼20–21 °C). The results from acute hardening experiments in the Zambian population demonstrate limited ability to improve low-temperature tolerance over short (hourly) timescales after non-lethal pre-treatments. In flies which survived chilling, recovery times were non-linear with plateaus between 2–6 and 8–12 °C. Survival times ranged between 4 and 36 h and did not vary between flies which had undergone chill coma by comparison with flies which had not, even after factoring body condition into the analyses (p>0.5 in all cases). However, flies with low chill coma values had the highest body water and fat content, indicating that when energy reserves are depleted, low-temperature tolerance may be compromised. Overall, these results suggest that physiological mechanisms may provide insight into tsetse population dynamics, hence distribution and abundance, and support a general prediction for reduced geographic distribution under future climate warming scenarios.

Introduction

Recent demonstrations and predictions of the biological effects of anthropogenic climate change have revived interest in the factors determining the abundance and distribution of plants and animals (Walther et al., 2002; Thomas et al., 2004; Thuiller et al., 2005; Wilson et al., 2005; Kerr et al., 2007). Among the organisms in which range shifts have already been documented (Parmesan and Yohe, 2003) and are predicted to continue (Helmuth et al., 2002; Roura-Pascual et al., 2004; Kearney and Porter, 2004; Urban et al., 2007), disease vectors are of considerable significance given their roles in compromising human and veterinary health, and in consequence, regional economic development (Patz et al., 2000; Patz, 2002; Harvell et al., 2002; Rogers et al., 2002; Sutherst, 2004; Pascual et al., 2006). Much theoretical and empirical work has been undertaken on the likely effects of climate change on disease vectors (Martens et al., 1999; Githeko et al., 2000; Bourne et al., 2001; Kovats et al., 2001; Rogers and Randolph, 2006), demonstrating that substantial differences in climate change responses exist among vectors, and therefore the diseases they transmit (Hulme, 1996; Martens et al., 1999). For example, climate change has been strongly associated with increasing risk of transmission of blue-tongue virus (Kuhn et al., 2003; Purse et al., 2005) but not for that of malaria (Rogers and Randolph, 2000) or tick-borne encephalitis (Sumilo et al., 2007).

In the case of tsetse-born trypanosomiasis, declared recently an under-investigated vector-borne disease (Cattand et al., 2006), few predictions have been made concerning likely climate change effects. Rogers and Packer (1993) suggested that in East Africa, climate change would result in an increase in available habitat and thus a possible expansion of the overall range of tsetse, particularly into high-altitude areas that may currently exclude the species owing to low temperatures (see also Rogers and Randolph, 1993). By contrast, other reports have suggested a net decline in the distributional range of the tsetse species considered. For example, under various future climate change scenarios Glossina morsitans is expected to experience a reduction in suitable habitat and hence a contraction of its geographic range (Hulme, 1996). Further confounding the issue is the related question of whether autonomous control will effectively render tsetse-borne trypanosomiasis an increasingly unimportant problem (Bourne et al., 2001; see also Rogers and Randolph, 2002). Nonetheless, it might be predicted that changes in temperature and moisture regimes would have a substantial influence on the abundances and distributions of tsetse owing to the strong relationships between these population-level characteristics and the environmental variables.

Many studies have demonstrated strong relationships between temperature and moisture availability, and the abundance and/or distribution of Glossina spp. at both coarse and fine scales. For example, spatial distribution data collected for regions such as south-central Africa show strong relationships with these environmental variables (e.g., Robinson et al., 1997a, Robinson et al., 1997b; Rogers and Robinson, 2004), as does distribution and abundance data recorded across the continent (Rogers and Williams, 1994; Rogers, 2000; Rogers and Robinson, 2004). In the case of G. morsitans, suitable habitat, as indicated by fly presence or absence, is marked by a temperature difference of only 0.5 °C for the sub-species in south-central Africa (Robinson et al., 1997a, Robinson et al., 1997b). Likewise, at both short and long time scales, fly abundance is positively related to temperature and humidity (Kitron et al., 1996; Mohamed-Ahmed and Wynholds, 1997; see also Huyton and Brady, 1975; Van Etten, 1982; Rogers and Randolph, 1991; Esterhuizen et al., 2005). Indeed, tsetse demographics are strongly influenced in all life stages by temperature, and by moisture availability (Bursell, 1959; Langley, 1977; Rogers, 1990; Hargrove, 2001, Hargrove, 2004), although the functions describing these relationships can differ markedly within and between various life stages. For example, increasing mean monthly maximum temperature in the range of 25–36 °C is correlated with a linear reduction in weekly survival probability, especially in Glossina morsitans morsitans (Hargrove, 2001), and declining water availability may have a similar influence (Rogers and Randolph, 1986; Hargrove, 2004).

Despite these obvious links between environmental variables, demographic change, and estimates of field abundance and distribution, it is not yet clear what the mechanistic basis is thereof. For example, the negative relationship between increasing temperature and survival probability might reflect direct physiological temperature sensitivity, an indirect physiological effect mediated through increasing metabolic rates requiring more frequent feeding and therefore higher foraging risk (Torr and Hargrove, 1999; Hargrove, 2004; Terblanche and Chown, 2007), or simply an increase in predation owing to greater activities of other species (see Leak, 1999). Each of these mechanisms has very different implications for models of the impacts of climate change on tsetse abundance and distribution. The first suggests that reasonably straightforward climatic envelope models (see Hijmans and Graham, 2006) might be extrapolated to future conditions, whilst the latter two mechanisms indicate that matters may be substantially more complicated. In consequence, mechanistic understanding of the likely links between the abiotic environment and the dynamics of a population is required to develop realistic climate envelope models, particularly those which use physiological information to define limits or critical thresholds to animal function and performance (Helmuth et al., 2005). Indeed, such a mechanistic approach can provide major insights into the likely effects of climate change on species distributions and abundance (see Kearney and Porter, 2004; Pörtner and Knust, 2007), because it presents an alternative to the more correlative climate-matching approaches typically used to make such forecasts (e.g., Rogers et al. (2002), Rogers and Robinson (2004), Sumilo et al. (2007); for recent reviews of climate modelling methods, see Graham and Hijmans, 2006; Rogers, 2006). Thus, in the first part of this study we examine the direct responses of an important south-east African vector of trypanosomiasis, Glossina pallidipes, to high and low temperature, to determine whether these responses might constitute an important link between temperature, population dynamics and geographic distributions (see Gaston (2003) for general review of this field).

In the second part of the study, we examine the short-term responses of this species to low temperatures. Early work suggested that low-temperature developmental constraints probably set the low-temperature limits to tsetse distribution (e.g., Bursell, 1960; Phelps and Burrows, 1969). In consequence, the low-temperature physiology of adult tsetse is typically not well studied (exceptions include early work by Mellanby (1936), Burnett (1957), Phelps and Burrows (1969); reviewed in Bursell (1964)). Also, thermal limits to activity have not been well explored in tsetse (but see, for example, Macfie, 1912; Mellanby, 1936), and lower lethal limit data are restricted to a few species only. Moreover, interest in the low-temperature physiology of tsetse is increasing because of the ongoing, though controversial (see Rogers and Randolph, 2002) proposals for the use of sterile insect technique (SIT) for their control and eradication. Indeed, flies reared for SIT are typically chilled for handling and sorting prior to and during aerial dispersal (Burnett, 1957; Leak, 1999), and chilling is regularly used for sorting flies in the laboratory. Much interest therefore exists in understanding how low-temperature treatments may influence fly performance (e.g. Mutika et al., 2001) and survival. For example, a rapid cold hardening response, as has been found in other fly taxa (Lee et al., 1987; Nilson et al., 2006), could result in flies recovering during handling and transport, which in turn could negatively affect the efficacy of laboratory work and SIT programmes. Moreover, broad divergence in physiology between laboratory colonies and field populations (Terblanche et al., 2006) raises issues of mating compatibility and the competitiveness of colony-bred flies released into wild populations.

Therefore we (i) investigate acute time×temperature effects on adult survival and limits to activity, (ii) synthesize available information and explore sources of intra-specific variation in thermal tolerances in G. pallidipes (e.g., geographic variation, acclimation, experimental methodology), (iii) determine if this species has the capacity to rapidly cold harden (reviewed in Chown and Nicolson (2004), Terblanche et al. (2007)) after pre-exposure to sub-lethal temperatures, (iv) explore the effects of temperature on chill coma recovery time and (v) examine short-term costs associated with chill coma and assess the possibility that energy metabolism plays a role in cold tolerance.

Section snippets

Study sites and collection

The work focuses on adult flies because they are the life stage most susceptible to high-temperature effects in the wild (Hargrove, 2004), and because adult flies are those that will be released in SIT operations (Leak, 1999). Field-collected G. pallidipes (Diptera: Glossinidae) were trapped in the South Luangwa National Park, Zambia (Mfuwe, Table 1). For each of the field experiments, flies were collected from 10 odour-baited Ngu traps (key attractive components: 4-methyl-phenol, 3-n-propynol,

High-temperature responses

Time and temperature had a significant effect on survival at high temperatures and the interaction between time and temperature was also significant (Table 2; Fig. 2A). Here, longer exposure time or more severe temperatures resulted in a reduction in high-temperature survival, but the form of the relationship between temperature and survival differed depending on exposure time. The temperature at which 50% of the population survived (Upper Lethal Temperature, ULT50) for the 1, 2 and 3 h

Thermal limits, mortality, and geographic range

Temperature tolerance has long been a topic of interest to biologists investigating tsetse, given indications that high temperatures have negative effects on populations of these species (summarized in Bursell, 1964; Leak, 1999; Hargrove, 2004; see also Hargrove, 2001; Table 4). Typically, physiological estimates of high-temperature tolerance are substantially higher than the estimates of survival probability derived from mark-recapture studies in tsetse. For example, experimental work in G.

Acknowledgements

We are grateful to Charlene Janion (Centre for Invasion Biology) and Patsy and Herman Miles of the Wildlife Camp, for excellent logistic support at several stages in the project. John Mashili and John Silutongwe aided with trapping, collection and fly identification and our Zambia Wildlife Authority scout, Wisdom Kakumbwe, provided watchful eyes and safety during several close encounters. The referees are thanked for their comments. This work was supported by the DST-NRF Centre of Excellence

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