Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): Implications for forecasting climate change impacts
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
References (101)
- et al.
Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster
Journal of Insect Physiology
(1999) - et al.
Dissecting chill coma recovery as a measure of cold resistance: evidence for a biphasic response in Drosophila melanogaster
Journal of Insect Physiology
(2004) - et al.
Climate change and future populations at risk of malaria
Global Environmental Change
(1999) - et al.
Cold tolerance and proline metabolic gene expression in Drosophila melanogaster
Journal of Insect Physiology
(2001) - et al.
The effects of carbon dioxide anesthesia and anoxia on rapid cold-hardening and chill coma recovery in Drosophila melanogaster
Journal of Insect Physiology
(2006) - et al.
Effects of environmental change on emerging parasitic diseases
International Journal for Parasitology
(2000) - et al.
Complexity of the cold acclimation response in Drosophila melanogaster
Journal of Insect Physiology
(2006) Satellites, space, time and the African trypanosomiases
Advances in Parasitology
(2000)- et al.
Vector-borne diseases, models, and global change
The Lancet
(1993) - et al.
Distribution of tsetse and ticks in Africa: past, present and future
Parasitology Today
(1993)
A response to the aim of eradicating tsetse from Africa
Trends in Parasitology
Rapid responses to high temperature and desiccation but not to low temperature in the freeze-tolerant sub-Antarctic caterpillar Pringleophaga marioni (Lepidoptera, Tineidae)
Journal of Insect Physiology
Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica
Journal of Insect Physiology
Temperature-dependence of metabolic rate in Glossina morsitans morsitans (Diptera, Glossinidae) does not vary with gender, age, feeding, pregnancy or acclimation
Journal of Insect Physiology
Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis
Journal of Insect Physiology
Controlling the false discovery rate: a practical and powerful approach to multiple testing
Journal of the Royal Statistical Society B
Environmental Change and the Autonomous Control of Tsetse and Trypanosomiasis in Sub-Saharan Africa
Learning influences host choice in tsetse
Biology Letters
The relation between age and cold resistance in tsetse flies and the value of chilling when transporting tsetse for experiments
Proceedings of the Royal Entomological Society of London A
The water balance of tsetse flies
Transactions of the Royal Entomological Society of London
The effect of temperature on the consumption of fat during pupal development in Glossina
Bulletin of Entomological Research
Environmental aspects: temperature
An energy budget for Glossina (Diptera: Glossinidae)
Bulletin of Entomological Research
Climate and tsetse flies: laboratory studies upon Glossina submorsitans and tachinoides
Philosophical Transactions of the Royal Society of London B
Tropical diseases lacking adequate control measures: dengue, leishmaniasis, and African trypanosomiasis
Insect Physiological Ecology. Mechanisms and Patterns
Physiological diversity in insects: ecological and evolutionary contexts
Advances in Insect Physiology
Water relations, fat reserves, survival, and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae)
Environmental Entomology
Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster
Journal of Thermal Biology
The fly that came in from the cold: geographic variation in recovery time from low-temperature exposure in Drosophila subobscura
Functional Ecology
Abundance and distribution of the tsetse flies, Glossina austeni and G. brevipalpis, in different habitats in South Africa
Medical and Veterinary Entomology
The Structure and Dynamics of Geographic Ranges
Chill-coma tolerance, a major climatic adaptation among Drosophila species
Evolution
Climate change and vector-borne diseases: a regional analysis
Bulletin of the World Health Organisation
A comparison of methods for mapping species ranges and species richness
Global Ecology and Biogeography
The effect of temperature and saturation deficit on mortality in populations of male Glossina m. morsitans (Diptera: Glossinidae) in Zimbabwe and Tanzania
Bulletin of Entomological Research
Tsetse population dynamics
Activity rhythms of tsetse flies (Glossina spp.) (Diptera: Glossinidae) at low and high temperatures in nature
Bulletin of Entomological Research
Optimized simulation as an aid to modelling, with an application to the study of a population of tsetse flies, Glossina morsitans morsitans Westwood (Diptera: Glossinidae)
Bulletin of Entomological Research
Climate warning and disease risks for terrestrial and marine biota
Science
Habitat temperature and the temporal scaling of cold hardening in the high Arctic collembolan, Hypogastrura tullbergi (Schäffer)
Ecological Entomology
Climate change and latitudinal patterns of intertidal thermal stress
Science
Biophysics, physiological ecology, and climate change: does mechanism matter?
Annual Review of Physiology
A systematic approach to area-wide tsetse distribution and abundance maps
Bulletin of Entomological Research
The ability of climate envelope models to predict the effect of climate change on species distributions
Global Change Biology
Very high resolution interpolated climate surfaces for global land areas
International Journal of Climatology
Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster
Journal of Evolutionary Biology
Climate Change and Southern Africa. An Exploration of Some Potential Impacts and Implications in the SADC Region
Some effects of light and heat on feeding and resting behavior of tsetse flies, Glossina morsitans Westwood
Journal of Entomology A—Physiology and Behaviour
Cited by (130)
Does heat tolerance actually predict animals' geographic thermal limits?
2024, Science of the Total EnvironmentTick and Vector-borne Disease Expansion with Climate Change
2022, Fowler's Zoo and Wild Animal Medicine Current Therapy: Volume 10Validating measurements of acclimation for climate change adaptation
2020, Current Opinion in Insect ScienceLife-stage related responses to combined effects of acclimation temperature and humidity on the thermal tolerance of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae)
2019, Journal of Thermal BiologyCitation Excerpt :Conversely, high temperature and low RH (33 °C; 45%RH) impaired heat tolerance (HKDT) following larval and pupal acclimations, pointing to thermal fitness costs (HKDT) associated with interactive potentially irreversible effects of high temperature and low RH stress. Previous studies reported that high temperatures and low RH have a detrimental effect on insect survival (Terblanche et al., 2007b, 2008). Given that the rate of water loss in insects is dependent on temperature and RH (Gibbs et al., 2003), our results are therefore in agreement with Bubliy et al. (2012), who reported that D. melanogaster exposed to drier environments were knocked down faster than those exposed to humid environments.
Effect of starvation on the cold tolerance of adult Drosophila suzukii (Diptera: Drosophilidae)
2021, Bulletin of Entomological Research