Elsevier

Journal of Insect Physiology

Volume 59, Issue 12, December 2013, Pages 1199-1211
Journal of Insect Physiology

Thermal biology, population fluctuations and implications of temperature extremes for the management of two globally significant insect pests

https://doi.org/10.1016/j.jinsphys.2013.09.004Get rights and content

Highlights

  • Upper and lower lethal temperatures are seldom encountered.

  • Critical minimum temperatures for activity and lower developmental thresholds are more frequently encountered.

  • Thermal limits were influenced by both seasonal and diurnal variation.

  • A trade-off was not detected between heat and cold shock survival.

Abstract

The link between environmental temperature, physiological processes and population fluctuations is a significant aspect of insect pest management. Here, we explore how thermal biology affects the population abundance of two globally significant pest fruit fly species, Ceratitis capitata (medfly) and C. rosa (Natal fruit fly), including irradiated individuals and those expressing a temperature sensitive lethal (tsl) mutation that are used in the sterile insect technique. Results show that upper and lower lethal temperatures are seldom encountered at the field sites, while critical minimum temperatures for activity and lower developmental thresholds are crossed more frequently. Estimates of abundance revealed that C. capitata are active year-round, but abundance declines markedly during winter. Temporal autocorrelation of average fortnightly trap captures and of development time, estimated from an integrated model to calculate available degree days, show similar seasonal lags suggesting that population increases in early spring occur after sufficient degree-days have accumulated. By contrast, population collapses coincide tightly with increasing frequency of low temperature events that fall below critical minimum temperatures for activity. Individuals of C. capitata expressing the tsl mutation show greater critical thermal maxima and greater longevity under field conditions than reference individuals. Taken together, this evidence suggests that low temperatures limit populations in the Western Cape, South Africa and likely do so elsewhere. Increasing temperature extremes and warming climates generally may extend the season over which these species are active, and could increase abundance. The sterile insect technique may prove profitable as climates change given that laboratory-reared tsl flies have an advantage under warmer conditions.

Introduction

Knowledge of thermal biology has proven especially useful for understanding insect demography, population fluctuations and in forecasting pest outbreaks (e.g. Kingsolver, 1989, Bale, 2010). Low temperatures associated with winter generally suppress insect population growth rates, through reductions in development, suppression of activity, indirect chilling injury, and/or direct chilling mortality (Chown and Nicolson, 2004, Bale, 2010). Insects may cope with winter conditions by either behavioural or physiological compensation, arrested development (e.g. diapause) or some combination thereof (Denlinger and Lee, 2010). Physiologically, insects can adjust thermal tolerance over either the short-term (hardening) or longer-term (acclimatization in the field and acclimation under controlled laboratory conditions). A common example of acclimatization is the suite of physiological changes occurring at the onset of winter, typically providing improved low temperature tolerance (Hoffmann et al., 2003). Knowledge of overwintering biology, including physiological responses, is therefore often critical for assessments of pest insect population dynamics (Bale, 2010). For many economically significant pest insects, seasonal variation in physiology or overwintering biology is poorly elucidated. Improving this situation is important not only for pest management over the short term, but is also significant in the context of rapidly changing climates globally (Bale and Hayward, 2010).

This is true for two of the most significant pests of commercially-grown fruit crops: the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) and the Natal fruit fly, C. rosa Karsch. Both are multivoltine, polyphagous tephritid flies that result in millions of dollars of losses annually (Malacrida et al., 2007, De Meyer et al., 2008). Demographic analyses of the two species suggest a very high net reproduction rate while young and a lack of diapause (Carey, 1984, Manrakhan and Addison, 2007). Ceratitis capitata probably originated from sub-Saharan East Africa and has become widely distributed in most continents with tropical and temperate climates (Malacrida et al., 2007). By contrast, C. rosa has a restricted African distribution (De Meyer et al., 2008, De Villiers et al., 2012), but is considered a significant biosecurity threat. In consequence, both species represent a burden to agriculture and act as barriers to economic transformation of rural communities through direct crop losses, the costs of control practices, and reduced market access. Comparatively little is known however about the relationships between their demography, abundance and thermal biology, and this is not a typical consideration in their management.

In addition to chemical control (pesticides including malathion), the Sterile Insect Technique (SIT) is one of the main methods used to control C. capitata (Klassen and Curtis, 2005). SIT involves releasing many males that have been rendered reproductively sterile by radiation, with the intent that they will mate with wild females and reduce the number of viable offspring (Knipling, 1959). Strains of C. capitata currently used in SIT campaigns possess a ‘temperature sensitive lethal’ (tsl) mutation that makes females homozygous for the tsl gene more susceptible to high temperature mortality (Franz, 2005). Application of a heat stress to eggs kills female embryos and permits large-scale, male-only releases. The release of a male-only strain improves the efficacy of SIT because only wild females will be present in the target area (Caceres, 2002). Females homozygous for the tsl gene remain sensitive to high temperatures throughout their lifetime such that sustained temperatures of over 28 °C lead to significant adult mortality within only a few days (Franz, 2005). It remains unknown however, whether the tsl mutation or irradiation affects the thermal tolerance of released male tsl C. capitata under field conditions. Such data have direct implications for ongoing SIT control programmes in South Africa and other parts of the world where C. capitata is considered a major pest. By contrast, control of C. rosa does not yet involve the release of sterile males, but the future of large-scale SIT campaigns could benefit from knowledge of radiation effects on the thermal tolerance of this species.

The overall aim of this work is therefore to determine aspects of the thermal environment that influence the population fluctuations of these two key horticultural pests to inform management and control practice. Specifically, to understand the influence of tsl and climate on demography or population fluctuations more generally, especially given expectations of future warming climates around the globe (Archer and Rahmstorf, 2010), we examined the extent to which thermal physiology accounts for population variability in both species. We determined the key thermobiological traits, including plastic responses in the field, across both species and in irradiated/unirradiated and untreated vs. tsl strains of C. capitata, and complemented these investigations with assessments of longevity of adults in the field. These data were then used in conjunction with microclimate information to estimate which physiological parameters, including developmental rates and limits, estimated from other studies, might be most significant in affecting population fluctuations, how SIT treatments might affect them, and what a warmer future might mean for the management of these species.

Section snippets

Materials and methods

We focused on traits likely to modify the impact of temperature on population growth. Our primary focus here was to understand factors influencing the field population abundances of wild flies and for this reason these traits were scored on untreated flies which were assumed to be representative of wild flies. These included upper and lower lethal temperature (ULT, LLT), supercooling point (SCP), functional activity limits (or critical thermal limits) recorded as critical thermal minima (CTmin)

Supercooling points and lower lethal temperatures

Supercooling point was similar across both species, but differed among life stages (Fig. 1A; Fig. S1). Further differentiation of animals into those removed just prior to and those removed several degrees after the SCP showed no evidence of freeze tolerance (ESM). Cooling rate had no significant effect on SCPs (χ2 = 0.19, df = 3, P > 0.97) (Table S1).

LLT varies among stages and species (Table 1) but it is clear that pre-freeze mortality is significant with complete mortality by −3 to −7 °C (Fig. 1B

Discussion

Insect populations fluctuate as a consequence of intrinsic and extrinsic factors such as changing abiotic and biotic conditions (Price, 1997). In the case of this study system, resources are abundant nearly year round given the timing of fruit production and the practise of leaving unharvested and fallen fruit in the orchards (Manrakhan and Addison, 2007). The agroecosystem setting implies low predation rates and the use of SIT has little significant impact on parasitoid populations (Wong et

Acknowledgements

Citrus Research International, SIT Africa and P. J. Pieterse provided valuable support during this research. Weather SA and ARC-Institute for Soil, Climate and Water assisted with weather data. We are grateful to several anonymous referees for constructive and insightful comments on an earlier version of this manuscript. This research was supported by Fruitgro Science, Citrus Research International, NRF THRIP and Stellenbosch University.

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  • Cited by (0)

    1

    Present address: Department of Earth and Environmental Sciences, Botswana International University of Science and Technology (BIUST), Private Bag BO 041 Bontleng, Gaborone, Botswana.

    2

    Present address: Department of Plant Sciences, University of Pretoria, Private Bag X20, Hatfield 0083, South Africa.

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