Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica

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Abstract

The environmental physiology of three speciesof Collembola: Cryptopygus cisantarcticus, Isotoma klovstadi (Isotomidae) and Friesea grisea (Neanuridae) was investigated from November 2002 to February 2003 at Cape Hallett, North Victoria Land, Antarctica. All three species were freeze avoiding, and while supercooling points were variable on seasonal and daily scales in I. klovstadi and C. cisantarcticus, they remained largely static in F. grisea. LT50 (temperature where 50% of animals are killed by cold) was −13.6, −19.1 and −19.8 °C for C. cisantarcticus, I. klovstadi and F. grisea, respectively. Upper lethal temperature was 34, 34 and 38 °C for C. cisantarcticus, I. klovstadi and F. grisea. Critical thermal minimum onset (the temperature where individuals entered chill coma) was ca. −7, −12 and −8 °C for C. cisantarcticus, I. klovstadi and F. grisea, and 25% of I. klovstadi individuals froze without entering chill coma. Critical thermal maximum (the onset of spasms at high temperature) was 30, 33 and 34 °C for C. cisantarcticus, I. klovstadi and F. grisea. Haemolymph osmolality was approximately 720 mOsm for C. cisantarcticus and 680 mOsm for I. klovstadi, and both species showed a moderate degree of thermal hysteresis, which persisted through the season. Desiccation resistance was measured as survival above silica gel, and the species survived in the rank order of C. cisantarcticus<<I. klovstadi=F. grisea. Desiccation resulted in an increase in haemolymph osmolality in I. klovstadi, and water was quickly regained by desiccation-stressed individuals that had access to liquid water, but not by individuals placed in high humidity, indicating that this species is unable to absorb atmospheric water vapour. SDS-PAGE did not suggest any strong patterns in protein synthesis either seasonally or in response to temperature or desiccation stress. Microclimate temperatures were measured at sites representative of collection sites for the three species. Microclimate temperatures were highly variable on a diurnal and weekly scale (the latter relating to weather patterns), but showed little overall variation across the summer season. Potentially lethal high and low temperatures were recorded at several sites, and it is suggested that these temperature extremes account for the observed restriction of the less-tolerant C. cisantarcticus at Cape Hallett. Together, these data significantly increase the current knowledge of the environmental physiology of Antarctic Collembola.

Introduction

The organisms that live in terrestrial Antarctic habitats must tolerate the temperature extremes, aridity, short growing season and long months of complete darkness that characterise Antarctica (Block, 1994). Given current climate change (IPCC, 2001; Doran et al., 2002; Parmesan and Yohe, 2003), understanding the physiological tolerances of Antarctic species, and the extent to which these tolerances may influence community dynamics and determine distribution, is an important aspect of managing and conserving Antarctic biodiversity (Convey et al., 2003, Convey et al., 2002; Peck, 2002; Walther et al., 2002; Peck et al., 2004). In terms of species diversity, distribution and abundance, Collembola (springtails) are one of the dominant members of the terrestrial Antarctic fauna. Endemism in the Antarctic springtail fauna is high, and the group is found in habitats extending almost as far south as ice-free land permits (Wise and Gressitt, 1965; Block, 1994). In consequence, research on the ecology and physiology of Antarctic Collembola has a long history (e.g. Ewing, 1922; Gressitt, 1967; Janetschek, 1967; Tillbrook, 1977; Cannon and Block, 1988; Sinclair and Sjursen, 2001a; Worland and Convey, 2001).

All Antarctic Collembola that have been studied are freeze avoiding, surviving sub-zero temperatures by maintaining their body fluids in a liquid state, and are killed upon freezing at a temperature referred to as the supercooling point (SCP) (Cannon and Block, 1988; Sinclair et al., 2003b). Consequently SCP frequency distributions are a valid and useful way to assess the population distribution of cold tolerance in these species (Cannon and Block, 1988; Worland and Convey, 2001). Bimodal SCP distributions have been commonly described, and seem to be a consequence of ice nucleators from food in the gut (Cannon and Block, 1988). The higher (less cold-hardy) mode of the distribution is thought to be made up largely of active, foraging individuals, while the low (more cold-hardy) group are thought to be non-feeding or moulting individuals (Worland, 2005), with a general shift to the low group also observed in preparation for winter (Cannon and Block, 1988). Recently, rapid shifts between these groups in response to diurnal temperature cycles have been demonstrated in species from the maritime (Worland and Convey, 2001) and continental (Sinclair et al., 2003b) Antarctic. However, bimodal SCP distributions are absent in Friesea grisea (Neanuridae) at Cape Hallett (Sinclair et al., 2003b) and possibly also in Gomphiocephalus hodgsoni (Hypogastruridae) at Cape Bird (Sinclair and Sjursen, 2001a), suggesting that bimodality may not be the rule in non-isotomid species. Thermal hysteresis proteins, which stabilise the body fluids of supercooled insects against homogeneous ice nucleation and prevent inoculative freezing (Zachariassen and Husby, 1982; Zachariassen and Kristiansen, 2000) are present in several alpine Collembola (Zettel, 1984) and have been detected in G. hodgsoni (Sinclair and Sjursen, 2001a), but are not present in Cryptopygus antarcticus (Isotomidae) from the maritime Antarctic (Block and Duman, 1989).

Apart from cold tolerance, other aspects of the thermal biology of Antarctic Collembola have received less attention. As may be expected, Antarctic Collembola are able to maintain activity at low temperatures, with reported chill coma temperatures (≈critical thermal minimum) ranging from near zero in G. hodgsoni (Janetschek, 1967) to −10 °C in C. antarcticus (Sømme and Block, 1982). Thermal preferenda are often surprisingly high: in the region of 10 °C for G. hodgsoni (Fitzsimons, 1971) and 9–13 °C for warm-acclimated C. antarcticus (Hayward et al., 2003). Upper thermal limits have rarely been measured, although Fitzsimons (1971) reported an upper lethal temperature of +29.5 °C for G. hodgsoni. With the exceptions of an investigation of the potential of Hsp70 as an ecotoxicological biomarker (Staempfli et al., 2002) and the demonstration of the induction of Hsp70 in response to desiccation (Bayley et al., 2001), molecular responses to thermal or other environmental stresses (see Chown and Nicolson, 2004, for review) have not been investigated in Collembola.

Low precipitation, sub-zero temperatures, and high water vapour deficit mean that desiccation is a major stress for terrestrial Antarctic organisms (Kennedy, 1993). Cutaneous respiration, permeable cuticles and a large surface area:volume ratio conspire to make Collembola susceptible to desiccation (Hopkin, 1997), and significant interspecific variation in behaviour, cuticle structure and consequently rate of water loss mean that there is significant among-species variation in desiccation tolerance (Hopkin, 1997; Hertzberg and Leinaas, 1998). Hayward et al. (2004) suggested that the fine-scale distributions of Friesea grisea and C. antarcticus at Rothera on the Antarctic Peninsula may be a consequence of their different rates of or tolerances to water loss. Collembola are generally poor osmoregulators (Hopkin, 1997). Haemolymph osmolalities of most Collembola under normal conditions fall between 200 and 400 mOsm kg−1 (Hopkin, 1997; Sinclair and Chown, 2002). Early spring haemolymph osmolalities of up to 1755 mOsm kg−1, decreasing to ca. 500 mOsm kg−1 in summer, were reported in G. hodgsoni (Sinclair and Sjursen, 2001a). Block and Harrisson (1995) report much lower osmolalities of ca. 284 mOsm kg−1 for C. antarcticus.

An essential element of environmental physiology is determination of the conditions that organisms actually encounter (Bale, 1987; Kingsolver, 1989; Danks, 1991; Sinclair et al., 2003c). In terrestrial Antarctic habitats, microclimatic temperatures have long been collected as part of ecological and physiological studies (e.g. Pryor, 1962; Janetschek, 1963, Janetschek, 1967; Rudolph, 1963), and this practice has been significantly advanced by the development and availability of automatic dataloggers (e.g. Block, 1985; Sømme, 1986; Friedmann et al., 1987; Davey et al., 1992; Sinclair and Sjursen, 2001a). Although most records are limited to temperature data, these are of value in assessing the magnitude and frequency of thermal stresses in the field. Indeed, recent assessments of daily temperature variation prompted greater temporal resolution of cold hardiness studies, revealing diurnal changes in the SCPs of arthropods in response to this variation (Worland and Convey, 2001; Sinclair et al., 2003b). Integrating microclimate temperature recordings and physiological information is therefore essential for understanding the likelihood that organisms experience physiologically stressful conditions in the field, the variability of these stresses at small and large spatial scales, and their importance in influencing population dynamics and consequently the abundance and distribution of the species concerned. The extent to which organisms are operating at the edge of their physiological tolerances is of great significance for understanding the changes that are likely to be induced by rapid climatic change (Holt et al., 1997; Kingsolver and Huey, 1998; Sinclair, 2001a).

Although apparently extensive, as the brief review above suggests, physiological and ecological investigations of Antarctic Collembola have been dominated by research on C. antarcticus in the Maritime Antarctic, and this work has contributed substantially to modern understanding of springtail biology in the Antarctic. However, comprehensive investigations of the biology of one species in a single region is inadequate for understanding the environmental physiology of a higher taxon, and its likely responses to climate change (Chown et al., 2002a). This is especially true for the wide range of species found across Antarctica: a continent whose regions’ climates vary dramatically, both currently and in predicted responses to global climate change (Convey, 2001; Doran et al., 2002; Walther et al., 2002). Here, we therefore extend previous studies of the environmental physiology of the Antarctic springtail fauna by investigating the thermal biology and water relations of three species of Collembola at Cape Hallett, North Victoria Land; an area for which little information is currently available. Furthermore, we investigate protein expression in one of the species, and present high-resolution microclimate temperature data for a summer at Cape Hallett, placing the physiological measurements in an appropriate environmental context.

Section snippets

Study site and animals

This work was conducted at the 72 ha Cape Hallett ice-free area (72°19′S, 170°13′E; Antarctic Specially Protected Area No. 106, http://www.cep.aq/apa/) in North Victoria Land, Antarctica. The site consists of basalt screes, moraines and beach deposits (Harrington et al., 1967). Approximately half of the area is occupied by an Adelie Penguin (Pygoscelis adeliae) colony, and is consequently devoid of terrestrial arthropods (Sinclair, Scott, Klok, Terblanche, Marshall, Reyers and Chown, in

Supercooling points

SCPs were unimodal (but strongly skewed, skewness±SEM=1.56±0.16) in F. grisea, and bimodal in I. klovstadi and C. cisantarcticus (Fig. 1). SCPs of F. grisea did not change significantly across the season, nor between ‘day’ and ‘night’ (Table 1; see also Sinclair et al., 2003b). High- and low-group SCPs of C. cisantarcticus also did not change between night and day (Table 1). In one period (26 Nov–2 Dec 2002, which also had the lowest mean temperature), I. klovstadi low group mean was

Discussion

The extremely low winter temperatures experienced by Collembola during winter at Cape Hallett (see Pryor, 1962) are likely to be a primary stressor driving their physiological evolution. However, we show here that potentially lethal high and low temperatures do occur in the microhabitats during the summer. Thus, Collembola living at Cape Hallett must show resistance adaptations (sensu Precht, 1958) to survive in their environment, even during the summer. Although the period from November to

Acknowledgements

Thanks to Ian Hawes for providing access to AWS data, and Mhairi McFarlane and two anonymous reviewers for comments on an earlier draft of the manuscript. We are grateful to Antarctica New Zealand, the Italian National Antarctic Programme, Helicopters New Zealand, Quark Expeditions and the crew of the icebreaker Kapitan Khlebnikov for logistic support; the Department of Environmental Affairs and Tourism (South Africa), the New Zealand Foundation for Research, Science and Technology and the

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    Present Address: School of Life Sciences, Arizona State University, Tempe, AZ, USA.

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