Low-temperature tolerance of false codling moth Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) in South Africa

https://doi.org/10.1016/j.jtherbio.2009.05.002Get rights and content

Abstract

  • (1)

    The low-temperature tolerance of false codling moth (FCM) Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae) is a significant aspect of this pest's population dynamics and has implications for post-harvest control and sterile insect technique programs.

  • (2)

    Here, we report results of experiments examining the effects of time, temperature and their interactions on low-temperature tolerance in adult FCM. In addition, using a variety of thermal pre-treatments, we examine the potential for hardening responses over several hours to improve low-temperature tolerance in FCM.

  • (3)

    Lower lethal temperature assays showed significant effects of time, temperature and significant interactions between time and temperature on survival (p<0.0001 in all cases). The temperature at which the probability of survival of 50% of the FCM population after 2 h of exposure was −4.5 °C, which varied significantly to −0.5 °C in 10 h. Gender and early adult age did not affect low-temperature tolerance of FCM.

  • (4)

    Using a range of non-lethal, low- and high-temperature pre-treatments, FCM survival could not be increased (p>0.84) and thus limited evidence for rapid cold hardening was found. These results are discussed with respect to microclimate temperatures in typical FCM environments and have implications for understanding population dynamics in this species and the diversity of low-temperature responses of insects.

Introduction

Temperature is a critical abiotic factor affecting insect population dynamics. At sub-lethal temperatures, it determines the rate of acquisition and consumption of resources, thereby influencing growth, development and reproduction. Most importantly, temperature determines the likelihood of mortality and hence, population declines, especially at extremes (reviewed in Hoffmann et al., 2003; Chown and Terblanche, 2007). However, the temperature tolerance of an insect is not a fixed characteristic. By contrast, lethal temperatures are determined by a host of factors that can vary over different timescales both within and among species. For example, an insect's thermal tolerance may be influenced by its thermal history, within either its lifetime (e.g., season, diurnal temperature cycles) or its parental lifetime (e.g., Crill et al., 1996; reviewed in Hoffmann et al., 2003; Chown and Nicolson, 2004). In addition, a population's thermal tolerance may vary with development (life stage) and gender, among other factors (reviewed in Bowler and Terblanche, 2008). Temperature tolerance may also differ among species depending on the ecological and evolutionary history of a species (e.g., temperate vs. tropical environment) (Addo-Bediako et al., 2000; Kimura, 2004; Chown and Terblanche, 2007). Ultimately, it is these factors, combined with complex interactions between duration and severity of exposure (e.g., Rako and Hoffmann, 2006; Marais et al., 2009) (longer or more severe exposures typically result in lower survival), that determine an insect's thermal tolerance.

Insects are able to survive extreme temperature variation using a host of physiological and biochemical mechanisms (reviewed in Cossins and Bowler, 1987; Lee and Denlinger, 1991; Chown and Nicolson, 2004). One such mechanism is rapid cold hardening (Lee et al., 1987), and can be defined as a rapid improvement in survival at a lethal temperature after brief pre-treatment (1–2 h) to a sub-lethal temperature shock (reviewed in Clark and Worland, 2008). In some species as much as 80–100% improvement in survival has been reported (e.g., Drosophila melanogaster; Jensen et al., 2007). Similarly, at warm temperatures, brief exposure to high sub-lethal temperatures result in greater survival at a lethal high temperature after a few hours. For example, this has been demonstrated in the wasp Trichogramma carverae (Scott et al., 1997). Such mechanisms are likely employed by insects to quickly alter their physiological tolerances over the course of a day (Kelty and Lee, 2001; Overgaard and Sørensen, 2008) to increase mating and feeding time (Shreve et al., 2004) and can be critical to the survival of sudden, unpredictable cold snaps in the wild (Chown and Nicolson, 2004). However, not all species examined to date have inducible thermal tolerance, especially over short timescales. For example, little evidence for rapid cold hardening has been observed in the tsetse fly Glossina pallidipes (Terblanche et al., 2008) and a host of other insects do not show rapid adjustments to temperature stress (reviewed in Sinclair et al., 2003; Chown and Nicolson, 2004). Thus, it is unreasonable to assume that all insect species will show rapidly adjustable thermal tolerance (i.e., limited acute phenotypic plasticity). Furthermore, of the terrestrial arthropod species that do show hardening responses, considerable variation in the magnitude of the protection afforded exists both within (Jensen et al., 2007; Terblanche et al., 2007; but see also Marais et al., 2009) and among species (e.g., Bahrndorff et al., 2009; reviewed in Chown and Nicolson, 2004). As a consequence, understanding the variation in thermal tolerance of insects, in terms of basal tolerance, magnitude of plasticity and potential phylogenetic or environmental constraints, has implications for the evolution of insect thermal tolerance.

The ability of pest insects to undergo such dramatic and rapid changes in temperature tolerance also deserves thorough investigation for several reasons, of which three are perhaps most significant. First, since the thermal tolerance of a species forms an integral component of bioclimatic modelling (e.g., Manrique et al., 2008), without knowledge of a species’ temperature tolerance any prediction of an insect's geographic distribution and abundance under future climate change scenarios is severely limited. Second, the ability of a pest species to undergo rapid thermal hardening could severely affect post-harvest control techniques, especially if insects or fruits are temperature treated at some point prior to entering storage and distribution (Burks and Hagstrum, 1999; Sharp and Hallman, 1994). It is therefore clear that knowing how an insect's thermal history contributes to its thermal tolerance is of fundamental importance to post-harvest control practices (reviewed in Neven, 2000). Third, in order to implement the sterile insect technique (SIT) in the field, laboratory-reared insects are typically chilled for handling and sorting prior to release in the field (Carpenter et al., 2007; M. Addison, pers. comm.). Yet the effect of such rapid chilling on subsequent extreme temperatures experienced by these laboratory-reared insects is poorly understood and may compromise field performance, and thus the SIT program (Terblanche et al., 2008). This could be particularly problematic if the insects acquire resistance to such treatments during laboratory culture.

Here, we investigate the low-temperature tolerance of a major economic pest in South Africa, the false codling moth (FCM) T. leucotreta. False codling moth feeds on a wide range of cultivated crops including deciduous, subtropical and tropical fruit, including citrus. The sterile insect technique for control of FCM is also presently under way in the Citrusdal (Western Cape) citrus-growing region in order to complement current control practices in South Africa (Carpenter et al., 2007). Specifically, we aimed to determine the low-temperature mortality of adult FCM under varying temperatures and durations of exposure to better comprehend the type of low-temperature stress that might be lethal in wild populations. In addition, we assessed whether factors such as gender and early adult age influence thermal tolerance. Finally, we investigated whether FCM shows short-term phenotypic plasticity in the form of rapid cold hardening after a variety of pre-treatments. We discuss these findings in the context of FCM pest management and insect thermal biology.

Section snippets

Insect culture

A laboratory colony of T. leucotreta was employed for these experiments. The FCM culture was initiated from wild moths collected in Citrusdal, South Africa, under standard culture conditions (reviewed in Carpenter et al., 2007). The colony is reared under optimal temperature conditions (25 °C: 50% relative humidity), has been in culture for <5 years and is occasionally supplemented with wild individuals to avoid inbreeding depression or genetic divergence from wild populations. At present,

Effects of time and temperature

No effects of early adult age and gender on low-temperature tolerance of FCM were detected at −3 °C for 4 h (p>0.53 in all cases). The effects of time and temperature on survival of FCM were highly significant (Table 1). A positive relationship was found between temperature and proportion of survival in FCM, indicating that more severe low temperatures were increasingly lethal (Table 1; Fig. 1). A negative relationship between survival and duration of exposure was found, showing that increasing

Effects of low-temperature exposure and duration on survival

The effects of time and temperature on FCM survival have, to our knowledge, not been previously reported. Most research on FCM to date have focused on taxonomy (e.g., Timm et al., 2008), chemical resistance (Hofmeyr and Pringle, 1998), biocontrol (Carpenter et al., 2004) or pheromone disruption (e.g., Hofmeyr and Burger, 1995; Carpenter et al., 2007). By contrast, relatively little is known about FCM thermal biology. FCM is nocturnal and present all year round in South African citrus orchards (

Acknowledgements

This project was financially supported by Citrus Research International and Sub-Committee B (Stellenbosch University). The manuscript was improved by discussion with Frank Chidawanyika, Casper Nyamukondiwa, Matthew Addison and climate data supported by Elsje Kleynhans.

References (45)

  • B.J. Sinclair et al.

    Rapid responses to high temperature and desiccation but not to low temperature in the freeze tolerant sub-Antarctic caterpillar Pringloephaga marioni (Lepidoptera, Tineidae)

    Journal of Insect Physiology

    (2003)
  • J.S. Terblanche et al.

    Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis

    Journal of Insect Physiology

    (2007)
  • J.S. Terblanche et al.

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

    Journal of Insect Physiology

    (2008)
  • A.A. Addo-Bediako et al.

    Thermal tolerance, climatic variability and latitude

    Proceedings of the Royal Society of London B

    (2000)
  • S. Bahrndorff et al.

    The rapid cold hardening response of Collembola is influenced by thermal variability of the habitat

    Functional Ecology

    (2009)
  • G.J. Begemann et al.

    The phenology of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae), Tortrix capensana (Walker) and Cryptophlebia leucotreta (Meyrick) (Lepidoptera: Tortricidae) on citrus at Zebediela, South Africa

    African Entomology

    (1999)
  • S. Bloem et al.

    Radiation biology and inherited sterility in false codling moth (Lepidoptera: Tortricidae)

    Journal of Economic Entomology

    (2003)
  • K. Bowler et al.

    Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?

    Biological Reviews

    (2008)
  • J. Carpenter et al.

    Area-wide control tactics for the false codling moth Thaumatotibia leucotreta in South Africa: a potential invasive species

  • S.L. Chown et al.

    Insect Physiological Ecology. Mechanisms and Patterns

    (2004)
  • S.L. Chown et al.

    Physiological diversity in insects: ecological and evolutionary contexts

    Advances in Insect Physiology

    (2007)
  • M.S. Clark et al.

    How insects survive the cold: molecular mechanisms—a review

    Journal of Comparative Physiology B

    (2008)
  • Cited by (0)

    View full text