Philippe Vernon

Insects at low temperatures: an ecological perspective

Abstract Modern climate change has precipitated widespread interest in the responses of organisms to the thermal environment. In insects, it is not only changes in mean environmental temperature and growing season length that are important, but also their responses to environmental extremes. Much is now known about the ways in which insects cope with the ice–water threshold, and with the low temperatures that precede it. Recent work has demonstrated a diversity of physiological responses to cooling and freezing in insects, with extremes of temperature, rates of temperature change, the numbers of freeze–thaw transitions, climatic unpredictability and the state of the surrounding microhabitat being important factors determining the cold tolerance strategy adopted by an insect. Insect low temperature biology now integrates techniques ranging from laboratory-based functional genomics to climatology, making it not only intrinsically fascinating, but also of considerable relevance to investigations of the biological implications of climate change.

The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera: Tenebrionidae) during exposure to low temperature

Abstract.  In this study, the impact of acclimation (1 month at 15 °C vs. breeding at 30 °C) and fluctuating thermal regimes (daily transfers from low temperatures to various higher temperatures for 2 h) on the cold tolerance of the tropical beetle, Alphitobius diaperinus Panzer (Coleoptera: Tenebrionidae) was examined. Acclimation increased significantly the duration of survival (Lt50) at a constant 5 °C (7.7 ± 0.3 days to 9.7 ± 0.5 days). Survival of acclimated and nonacclimated beetles increased slightly at alternating temperatures of 5 °C/10 °C or 5 °C/15 °C. When daily transfer to 20 °C was applied, survival (Lt50) was improved markedly (nonacclimated: 15.5 ± 0.7 days, acclimated: 19.6 ± 0.6 days). The higher temperatures may allow progressive repair of injuries, and the effects of chilling may be repaired completely at 25 and 30 °C, a phenomenon recorded here for the first time. It is estimated that the theoretical upper threshold of chill injury (Th) of nonacclimated beetles is 15.1 °C whereas it is shifted down to 11.2 °C in acclimated beetles, which might enable this temperature to allow effective repair of injury.

Cold hardiness in molluscs

Molluscs inhabit all types of environments: seawater, intertidal zone, freshwater and land, and of course may have to deal with subzero temperatures. Ectotherm animals survive cold conditions by avoiding it by extensive supercooling (freezing avoidant species) or by bearing the freezing of their extracellular body fluids (freezing tolerant species). Although some studies on cold hardiness are available for intertidal molluscs, they are scarce for freshwater and terrestrial ones. Molluscs often exhibit intermediary levels of cold hardiness, with a moderate or low ability to supercool and a limited survival to the freezing of their tissues. Several factors could be involved: their dependence on water, their ability to enter dormancy, the probability of inoculative freezing in their environment, etc. Size is an important parameter in the development of cold hardiness abilities: it influences supercooling ability in land snails, which are rather freezing avoidant and survival to ice formation in intertidal organisms, which generally tolerate freezing.

The significance of the sub-Antarctic Kerguelen Islands for the assessment of the vulnerability of native communities to climate change, alien insect invasions and plant viruses

The suite of environments and anthropogenic modifications of sub-Antarctic islands provide key opportunities to improve our understanding of the potential consequences of climate change and biological species invasions on terrestrial ecosystems. The profound impact of human introduced invasive species on indigenous biota, and the facilitation of establishment as a result of changing thermal conditions, has been well documented on the French sub-Antarctic Kerguelen Islands (South Indian Ocean). The present study provides an overview of the vulnerability of sub-Antarctic terrestrial communities with respect to two interacting factors, namely climate change and alien insects. We present datasets assimilated by our teams on the Kerguelen Islands since 1974, coupled with a review of the literature, to evaluate the mechanism and impact of biological invasions in this region. First, we consider recent climatic trends of the Antarctic region, and its potential influence on the establishment, distribution and abundance of alien insects, using as examples one fly and one beetle species. Second, we consider to what extent limited gene pools may restrict alien species’ colonisations. Finally, we consider the vulnerability of native communities to aliens using the examples of one beetle, one fly, and five aphid species taking into consideration their additional impact as plant virus vectors. We conclude that the evidence assimilated from the sub-Antarctic islands can be applied to more complex temperate continental systems as well as further developing international guidelines to minimise the impact of alien species.

Water Relations, Fat Reserves, Survival, and Longevity of a Cold-exposed Parasitic Wasp Aphidius colemani (Hymenoptera: Aphidiinae)

Abstract Parasitoids exposed to low temperatures may suffer from extreme physiological conditions inducing direct or indirect chill injuries. Under long cold exposure (which also includes starvation), individuals face a great challenge in maintaining both water balance and energy reserves. Key parameters associated with individual fitness and physiological parameters related to cold-hardiness were analyzed. One-day-old mummies of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiinae) were exposed to cold (2 and 4°C) for various periods (1–3 wk) under a high relative humidity (75 ± 5% RH) and darkness. High mortality and shortened adult longevity occurred with increasing duration of exposure at low temperatures. Individual parasitoid mass loss increased with cold storage duration and was associated to a marked decrease in dry mass caused by lipid reserve depletion. Water content (water mass/dry mass) slightly increased with cold exposure duration because of starvation. Similar patterns were observed for both temperatures tested. This study emphasizes (1) how energetic reserves may be critical to survive at low temperatures and (2) that the survival and longevity are related, at least in part, to the depletion of energy reserves during starvation.

Diet of the house mouse (Mus musculus) on Guillou island, Kerguelen archipelago, Subantarctic

Abstract. The diet of the house mouse (Mus musculus domesticus), introduced to the Kerguelen archipelago in the 1800s, was studied at monthly intervals from August 1997 to July 1998 in the closed communities of Acaena magellanica, the main habitat of mice on Guillou Island. The analysis of 291 stomach contents showed that this opportunistic rodent included a variety of items in its diet: earthworms (Dendrodrilus rubidus tenuis, Microscolex kerguelensis), caterpillars of a flightless moth (Pringleophaga kerguelensis), weevil adults and larvae (Ectemnorrhinus spp.), seeds of Acaena magellanica, and floral parts of dandelion (Taraxacum officinale). The animal prey were dominant in its diet all year round, except in summer. Based on the presence of chaetae in the stomach contents, our results show that earthworms are an important prey for the house mouse at Kerguelen. The consequences of these food habits for the invertebrate communities of the subantarctic islands are discussed.

A comparative approach to the entomological diversity of polar regions

The Arctic and Antarctic are both cold deserts but show contrasting geographic and climatic features. Marked differences are noticeable in the richness of insect communities at these high latitudes. In the north, a continuous terrestrial gradient links sub-Arctic and Arctic regions, while in the south, the Southern Ocean is an efficient barrier between the sub-Antarctic and the Antarctic. In spite of stressful environmental conditions, insects are present but species richness is poor. Functional diversity is subordinate to these constrained features. However, ecological and physiological adaptations are varied and generally show no taxonomic pattern. On sub-Antarctic islands, the recent increase in human activities has precipitated a dramatic increase in entomological diversity. In the Arctic, the spectacular underrepresentation of the Exopterygota cannot be explained only by biogeographic criteria. An ecophysiological interpretation is suggested and leads to an evolutionary hypothesis of entomological biodiversity in polar regions.

Consequences of acclimation on survival and reproductive capacities of cold-stored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae).

Abstract The cold storage of parasitoid mummies is a crucial point during mass production of parasitoids for aphid control in wheat, Triticum spp. In this study, the effect of acclimation to cold before storage of mummies containing Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae) was evaluated on survival, sterility, and fecundity of parasitoids. Groups of 1-d-old and 3-d-old mummies were stored at −5°C for 10 d without acclimation or after one of five different acclimation treatments. One-day-old and 3-d-old mummies contain prepupa and postmetamorphosis but not yet sclerotinized adult parasitoids, respectively. The offspring and sex ratio of stored parasitoids were compared with a control that was left at rearing temperatures (20°C). Without acclimation, two-thirds of the parasitoids died during storage, for both ages of mummies tested. For stored 1-d-old mummies, subsequent survival increased under progressive exposure to low temperatures and reached 67.3% after 480 min of acclimation. In the same way, percentage of male sterility decreased with acclimation duration, whereas female fecundity increased. For stored 3-d-old mummies, subsequent survival improved with the duration of the acclimation treatment, but not male sterility and female fecundity.

Metabolic responses to cold in subterranean crustaceans

SUMMARY Changes in polyol, sugar and free amino acid (FAA) body contents were investigated in the aquatic, subterranean (i.e. hypogean) crustaceans Niphargus rhenorhodanensis and Niphargus virei and in a morphologically close aquatic, surface-dwelling (i.e. epigean) crustacean Gammarus fossarum acclimated to 12°C, 3°C and –2°C. With decreasing temperature, G. fossarum significantly increased its alanine and glutamine levels, while trehalose body content was found to increase above control levels only at –2°C. N. virei showed moderate increases of alanine and glycine, and no change in trehalose level was observed in this species. By contrast, N. rhenorhodanensis was the only species showing a significant rise in its total FAA pool, mainly explained by alanine, glycine, arginine and glutamine accumulations. This species also gradually increased its trehalose body content with decreasing temperature. Several cold-hardy ectotherms show metabolic responses to cold that are identical to those observed in N. rhenorhodanensis. A previous comparative study showed that the hypogean N. rhenorhodanensis exhibited a survival time (Lt50) at– 2°C that was 26.3 times and 2.6 times higher than the hypogean N. virei and the epigean G. fossarum, respectively. Thus, crustacean levels of FAA and trehalose were correlated with their respective cold tolerances. Such differences in metabolic responses to cold in both hypogean organisms were unexpected since they both live in thermally buffered biotopes. Considering the current distribution areas of the two subterranean crustaceans studied, we assume that the cold hardiness found in the hypogean N. rhenorhodanensis could be correlated with its biogeography history during the quaternary glaciations.

Evolution of freezing susceptibility and freezing tolerance in terrestrial arthropods

Arthropods have evolved various adaptations to survive adverse seasons and it has long been discussed why some arthropods are freezing-susceptible and some are freezing-tolerant. However, which mode of frost resistance came first during the course of evolution? A commonly held opinion is that no choice of strategy has been offered in evolution, because each species of arthropod may have its own evolutionary and natural history, leading to cold-hardiness. Freezing tolerance is more frequent in holometabolous insect orders and partially used by certain vertebrates, like some terrestrially hibernating amphibians and reptiles. Supported by phylogenetic, ontogenetic and ecological arguments, we suggest here that freezing tolerance is more recent than freezing susceptibility in the course of arthropods evolution. In addition, we observe that three basic modes of freezing resistance in insect species exist in the field: (i) permanent or year-round freezing-susceptible species, (ii) alternative or seasonal freezing-susceptible/freezing-tolerant species, (iii) permanent or year-round freezing tolerant species.