Life stage-related differences in hardening and acclimation of thermal tolerance traits in the kelp fly, Paractora dreuxi (Diptera, Helcomyzidae)

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Abstract

It is widely appreciated that physiological tolerances differ between life stages. However, few studies have examined stage-related differences in acclimation and hardening. In addition, the behavioural responses involved in determining the form and extent of the short-term phenotypic response are rarely considered. Here, we investigate life stage differences in the acclimation and hardening responses of the survival of a standard heat shock (SHS) and standard low temperature (or cold) shock (SCS), and the crystallization temperature (or supercooling point, SCP) of adults and larvae of the sub-Antarctic kelp fly, Paractora dreuxi. These stages live in the same habitat, but differ substantially in their mobility and thus environmental temperatures experienced. Results showed that neither acclimation nor hardening affected the lower lethal limits in larvae or adults. Adults showed an increase in survival of upper lethal limits after low temperature acclimation, whilst larvae showed a consistent lack of response. The acclimation × hardening interaction significantly affected the SCP in adults, but no response to either acclimation or hardening was found in the larvae. This study further demonstrates the complexities of thermal tolerance responses in P. dreuxi.

Introduction

Acclimation and hardening responses in insects have recently become subjects of increasing interest in the literature. An ability to acclimate and/or to harden have not only been shown to increase survival (Rako and Hoffmann, 2006, Jensen et al., 2007), but also to improve reproductive potential (Shreve et al., 2004), locomotion (Deere and Chown, 2006) and shock recovery (David et al., 1998, Rako and Hoffmann, 2006). Enhanced survival or performance following acclimation and/or hardening (Chown and Nicolson, 2004) is underpinned by a wide array of biochemical mechanisms (Storey and Storey, 2005), although mostly at some metabolic cost (Hoffmann, 1995).

The extent of the response to hardening (short exposures (hours) to moderately high or low temperatures) and to acclimation (exposure over several days) can differ markedly within a species depending on the traits involved (Deere et al., 2006, Slabber et al., 2007; see Hoffmann et al., 2003 for hardening and acclimation definitions). Generally, acclimation responses in cold tolerance traits are more pronounced than those in heat tolerance traits (Kingsolver and Huey, 1998, Klok and Chown, 2003, Slabber and Chown, 2005, Terblanche and Chown, 2006), although exceptions to this trend have been found in several species, including moths and flies (Klok and Chown, 1998, Hoffmann et al., 2003, Sinclair and Chown, 2003). Nonetheless, it is clear that considerable variation in the responses to acclimation of different thermal tolerance traits exists, which likely also reflects genetically based differences in these traits (Rako et al., 2007).

It is also widely appreciated that physiological tolerances differ depending on life stage. For example, several studies have demonstrated pronounced differences in response to low and to high temperatures among non-diapausing life stages (e.g. Levins, 1969, Czajka and Lee, 1990, Vernon and Vannier, 1996, Feder et al., 1997a, Klok and Chown, 2001, Lee et al., 2006, Rinehart et al., 2006, Cho et al., 2007, but see also Klok and Chown, 2000). However, fewer studies have examined stage-related differences in acclimation and hardening. Where such work has been done (e.g. Loeschcke and Krebs, 1996, Slabber and Chown, 2005, Lee et al., 2006, Powell and Bale, 2006, Jensen et al., 2007) variation in responses among life stages is the norm, although the form and extent of the life stage-related differences in response varies among species. For example, pronounced differences in hardening among adults and larvae were found in the Antarctic midge Belgica antarctica (Lee et al., 2006) and among adults and nymphs of the grain aphid Sitobion avenae (Powell and Bale, 2006), whilst almost no differences in acclimation response were found among adults and larvae of the rove beetle, Halmaeusa atriceps (Slabber and Chown, 2005). Clearly, differences in acclimation and/or hardening might be expected for diapause vs. non-diapause individuals, or among stages that differ in the extent to which they overwinter (see e.g. Leather et al., 1993, Flannagan et al., 1998, Rinehart and Denlinger, 2000, Hayward et al., 2005).

By contrast, it is not known whether consistent, life stage-related differences in hardening or acclimation among species might exist where neither diapause nor quiescence are involved, nor what factors might underlie such differences. Obviously some trade-off between habitat use (or habitat selection by females for their offspring) and behavioural responses (including mobility) must be involved in determining the form and extent of the short-term phenotypic response (see e.g. Huey, 1991, Feder et al., 1997b, Huey et al., 2003), and it could only be similarities in this trade-off that might effect consistent stage-related differences in phenotypic plasticity among species. For example, leaf-mining or fruit-dwelling insect larvae might be expected to show a considerably greater basal tolerance than their free-living adults owing to regular exposures to extreme temperatures. Alternatively, behavioural flexibility on the part of the adults might preclude the necessity for well-developed phenotypic plasticity. Such differences will likely also vary among the traits investigated, since recovery from coma or critical limits to activity might be more significant for adult fitness, whilst absolute lethal limits might be more significant for fitness in less mobile larvae (Chown and Nicolson, 2004), and indeed these may be considered different traits (see below). However, determining whether this is the case requires explicit documentation not only of hardening and acclimation responses among life stages and traits (e.g. Deere et al., 2006, Jensen et al., 2007), but also careful consideration of differences in behavioural responses and environmental conditions faced by the different life stages (e.g. Lee et al., 2006). Only once such information is available for a reasonably wide range of species, traits and environments could any generality be sought, and in consequence tests be undertaken of hypotheses concerning the conditions under which different forms of plasticity are most likely to evolve (see Chown and Terblanche, 2007, Ghalambor et al., 2007 for review).

Here, we contribute to this requirement by investigating life stage-related differences in the acclimation and hardening responses of the survival of a standard heat shock (SHS) and standard low temperature (or cold) shock (SCS), and the crystallization temperature (or supercooling point, SCP) of a sub-Antarctic kelp fly, Paractora dreuxi, in which adults and larvae live in the same habitat, but differ substantially in mobility (Crafford, 1984, Crafford and Scholtz, 1987, Marais and Chown, 2008). In doing so we broaden considerably the range of treatments over which this species was previously investigated (Terblanche et al., 2007), demonstrating that responses vary amongst traits, and are more consistent among life stages for some traits (SCS, SCP) than for others (SHS).

This work complements a recent study of life stage differences in the effects of acclimation on chill coma recovery in the same species (Marais and Chown, 2008), specifically by focussing on survival of standardized high and low temperatures. Much evidence now supports the contention that knockdown traits, such as knockdown temperature or chill coma recovery, might differ substantially from survival traits, such as survival of a given heat or cold shock. Not only have clear experimental differences in these traits and their responses to acclimation, hardening and selection been demonstrated, especially at the intraspecific level (see Hoffmann et al., 2003, Chown and Nicolson, 2004, Rako and Hoffmann, 2006), but evidence is also accumulating to demonstrate that the traits may be genetically independent (Rako et al., 2007). In consequence, whilst the set of trials reported here is superficially similar to those concerning chill coma recovery undertaken by Marais and Chown (2008), in our view they represent examination of a different set of physiological features. Such a view would be demonstrably incorrect if the responses of the two sets of traits (knockdown and survival) proved to be similar.

Section snippets

Study site and animal collection

Adults (mass c. 15–40 mg) and final instar larvae (mass c. 40 mg) of the endemic kelp-fly, P. dreuxi mirabilis Séguy (Diptera, Helcomyzidae), inhabit pebbled beaches on sub-Antarctic Marion Island (46°54S 37°45E), closely associated with decaying bull-kelp (Durvillaea antarctica) and decomposing organic matter (Crafford and Scholtz, 1987). The larval duration is approximately 2 months, the pupal stage lasts for 30–60 days, while the adult lifespan is 14–21 days (Crafford, 1984). Although

Results

Life stage had the largest effect on SCP, with larvae having a typically higher SCP than adults, irrespective of acclimation and hardening (Table 1, Fig. 1). The response to acclimation differed among life stages as evidenced by the significance of life stage and the marginally significant acclimation × life stage interaction (Table 1). Separate GLZs for larvae and adults revealed that the SCP in larvae is typically insensitive both to acclimation and to hardening, whilst in adults the response

Discussion

Life stage-related differences in thermal tolerance have been recorded previously for P. dreuxi. As was the case here, Klok and Chown (2001) found that the SCP of larvae was higher than that of the adults, and showed that this is related to moderate freeze tolerance in the larvae and freeze intolerance in the adults. These authors also found differences in the critical limits and lower and upper lethal temperatures that are more or less in keeping with what we have documented here. Life stage

Acknowledgements

Erika Nortje is thanked for assistance with the collection of flies and maintenance of the fly colony during the acclimation trials. Two referees provided helpful comments on a previous version of the manuscript. The South African National Antarctic Programme provided logistic support in the field.

References (58)

  • B.J. Sinclair et al.

    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

    (2003)
  • B.J. Sinclair et al.

    Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica

    Journal of Insect Physiology

    (2003)
  • S. Slabber et al.

    Acclimation effects on thermal tolerances of springtails from sub-Antarctic Marion Island: indigenous and invasive species

    Journal of Insect Physiology

    (2007)
  • 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)
  • M.J. Angilletta et al.

    Coadaptation: a unifying principle in evolutionary thermal biology

    Physiological and Biochemical Zoology

    (2006)
  • W. Block

    Cold tolerance of insects and other arthropods

    Philosophical Transactions of the Royal Society of London B

    (1990)
  • K. Bowler et al.

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

    Biological Reviews

    (2008)
  • J.R. Cho et al.

    Cold hardiness in the black rice bug Scotinophara lurida

    Physiological Entomology

    (2007)
  • 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)
  • J.E. Crafford

    Life cycle and kelp consumption of Paractora dreuxi mirabilis (Diptera: Helcomyzidae): a primary decomposer of stranded kelp on Marion Island

    South African Journal of Antarctic Research

    (1984)
  • J.E. Crafford et al.

    Phenology of stranded kelp degradation by the kelp fly Paractora dreuxi mirabilis (Helcomyzidae) at Marion Island

    Polar Biology

    (1987)
  • M.C. Czajka et al.

    A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster

    Journal of Experimental Biology

    (1990)
  • J.R. David et al.

    Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster

    Journal of Thermal Biology

    (1998)
  • J.A. Deere et al.

    Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance

    American Naturalist

    (2006)
  • M.E. Feder et al.

    Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology

    Annual Review of Physiology

    (1999)
  • M.E. Feder et al.

    Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae

    Functional Ecology

    (1997)
  • R.D. Flannagan et al.

    Diapause-specific gene expression in pupae of the flesh fly Sarcophaga crassipalpis

    Proceedings of the National Academy of Sciences

    (1998)
  • C.K. Ghalambor et al.

    Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments

    Functional Ecology

    (2007)
  • Cited by (0)

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    Present address: Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa.

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