Environmental physiology of three species of Collembola at Cape Hallett, North Victoria Land, Antarctica
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
References (100)
Insect cold hardiness: freezing and supercooling—an ecophysiological perspective
Journal of Insect Physiology
(1987)- et al.
Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida
Journal of Insect Physiology
(2001) - et al.
Metabolic adaptations of Antarctic terrestrial microarthropods
Comparative Biochemistry and Physiology
(1978) - et al.
A comparative study of patterns of water loss from two antarctic springtails (Insecta, Collembola)
Journal of Insect Physiology
(1990) - et al.
Physiological variation in insects: large-scale patterns and their implications
Comparative Biochemistry and Physiology B
(2002) - et al.
Physiological variation in insects: large-scale patterns and their implications
Comparative Biochemistry and Physiology B—Biochemistry & Molecular Biology
(2002) - et al.
The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review
Pharmacology & Therapeutics
(1998) - et al.
The Collembola of northern Victoria Land (Antarctica): distribution and ecological remarks
Pedobiologia
(1997) - et al.
Habitat moisture availability and the local distribution of the Antarctic Collembola Cryptopygus antarcticus and Friesea grisea
Soil Biology & Biochemistry
(2004) - et al.
Flight muscle resting potential and species-specific differences in chill-coma
Journal of Insect Physiology
(2000)
Origin of the inland Acari of continental Antarctica, with particular reference to Dronning Maud Land
Zoological Journal of the Linnean Society
Terrestrial invertebrate abundance across a habitat transect in Keble Valley, Ross Island, Antarctica
Pedobiologia
Microhabitat selection and seasonality of alpine invertebrates
Pedobiologia
Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica
Journal of Insect Physiology
Insects at low temperatures: an ecological perspective
Trends in Ecology & Evolution
Seasonal changes in tolerance to cold and desiccation in Phauloppia sp. (Acari, Oribatida) from Finse, Norway
Journal of Insect Physiology
Factors that influence the supercooling point of the sub-Antarctic springtail Tullbergia antarctica
Journal of Insect Physiology
Ice nucleation and antinucleation in nature
Cryobiology
Water vapor absorption in arthropods by accumulation of myoinositol and glucose
Science
Oxygen consumption of the Antarctic springtail Parisotoma otooculata (Willem) (Isotomidae)
Revue d’Ecologie et de Biologie du Sol
Supercooling points of insects and mites on the Antarctic Peninsula
Ecological Entomology
Cold Resistance of two continental Antarctic micro-arthropods
Cryo-Letters
Terrestrial ecosystems: Antarctica
Polar Biology
Presence of thermal hysteresis producing antifreeze proteins in the Antarctic mite, Alaskozetes antarcticus
Journal of Experimental Zoology
Collembolan water relations and environmental change in the maritime Antarctic
Global Change Biology
Measurement of supercooling in small arthropods and water droplets
Cryo-Letters
Cold tolerance of microarthropods
Biological Reviews
Loss of supercooling ability in Cryptopygus antarcticus (Collembola: Isotomidae) associated with water uptake
Cryo-Letters
Insect Physiological Ecology. Mechanisms and Patterns
Terrestrial ecosystem responses to climate changes in the Antarctic
Refining the risk of freezing mortality for Antarctic terrestrial microarthropods
CryoLetters
Response of antarctic terrestrial microarthropods to long-term climate manipulations
Ecology
Soil arthropods as indicators of water stress in Antarctic terrestrial habitats?
Global Change Biology
Winter habitats and ecological adaptations for winter survival
Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island
Antarctic Science
Antarctic climate cooling and terrestrial ecosystem response
Nature
Antifreeze and ice nucleator proteins in terrestrial arthropods
Annual Review of Physiology
How small ectotherms thrive in the cold without really trying
Cryo-Letters
Notes on the occurrence and distribution of antarctic land arthropods (springtails and mites: Collembola and Acarina)
Entomological News
Temperature and three species of Antarctic arthropods
Pacific Insects Monographs
Water acquisition and partitioning in Drosophila melanogaster: effects of selection for desiccation-resistance
Journal of Experimental Biology
The Cryptoendolithic microbial environment in the Ross Desert of Antarctica: Satellite-Transmitted continuous nanoclimate data, 1984 to 1986
Polar Biology
Escaping the Bonferroni iron claw in ecological studies
Oikos
Site Description & Literature Review of Cape Hallett & Surrounding Areas
A respiratory hemocyanin from an insect
Proceedings of the National Academy of Sciences of the United States of America
Chill injury at alternating temperatures in Orchesella cincta (Collembola: Entomobryidae) and Pyrrhochoris apterus (Heteroptera: Pyrrhocoridae)
European Journal of Entomology
Topography and geology of the Cape Hallett district
Temperature preferences of the mite, Alaskozetes antarcticus, and the collembolan, Cryptopygus antarcticus from the maritime Antarctic
Physiological Entomology
Drought stress as a mortality factor in two pairs of sympatric species of Collembola at Spitsbergen, Svalbard
Polar Biology
Cited by (72)
Tolerance of high temperature and associated effects on reproduction in euedaphic Collembola
2023, Journal of Thermal BiologyThe Resilience of Polar Collembola (Springtails) in a Changing Climate
2022, Current Research in Insect ScienceCitation Excerpt :In summer, bare ground and (in some places) dark rocks in polar regions can capture a surprising amount of heat from the sun. Heat tolerances have been less-commonly measured, but reported high-temperature thresholds for polar Collembola range from 34 to 40 °C (Hodkinson et al., 1996; Sinclair et al., 2006b; Everatt et al., 2013; Everatt et al. 2014). This suggests that many Collembola may have thermal tolerances similar to their non-polar counterparts: upper functional thermal limits of Australian and South African Collembola range from 30-45 °C (Janion-Scheepers et al., 2018; Liu et al., 2020).
Time course of acclimation of critical thermal limits in two springtail species (Collembola)
2021, Journal of Insect PhysiologyCitation Excerpt :Strikingly, we observed a significant (albeit small) change only under 30℃ acclimation conditions in CTmax of Cryptopygus sp. 4, but in addition to the relatively small statistical effect size also present in our results the difference between the initial and final CTmax values in ℃ was relatively small. By contrast, Sinclair et al. (2006) showed that CTmax differed seasonally for Cryptopygus cisantarcticus, another isotomid species from the Antarctic, most probably the result of seasonal acclimatization. Interestingly, it was also reported that 1 month of acclimation from 4℃ to −2℃ resulted in a significantly reduced CTmax in C. antarcticus while a 4℃ to 9℃ acclimation did not result with any significant change in CTmax (Everatt et al., 2013b), so the difference between initial and acclimation temperature might be effective in addition to the length of acclimation.
Testing the climatic variability hypothesis in edaphic and subterranean Collembola (Hexapoda)
2018, Journal of Thermal BiologyPlasticity in reproductive output and development in response to thermal variation in ladybird beetle, Menochilus sexmaculatus
2018, Journal of Thermal BiologyCitation Excerpt :In real time, like the other climatic factors, temperature shows diurnal variation commonly overlapped by uneven fluctuations over 24 h and 365 days (Maharaj, 2003; Carrington et al., 2013). Amplitudes of daily thermal fluctuations can be more than 30 °C (Sinclair et al., 2006) and differ by season and habitat (Ragland and Kingsolver, 2008). The effect of fluctuating temperature variation has been identified in many diverse fields like biocontrol (Butler and Trumble, 2010; Colinet and Hance, 2010), insect assisted pollination (Rinehart et al., 2011; Yocum et al., 2012), forensic entomology (Catts and Goff, 1992; Higley et al., 2001), thermal tolerance physiology (Bozinovic et al., 2011; Marshall and Sinclair, 2012), and vector biology (Paaijmans et al., 2013; Lambrechts et al., 2011).
- 1
Present Address: School of Life Sciences, Arizona State University, Tempe, AZ, USA.