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Critical Thermal Limits, Temperature Tolerance and Water Balance of a Sub-Antarctic Kelp Fly, Paractora Dreuxi

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Critical Thermal Limits, Temperature Tolerance and Water Balance of a Sub-Antarctic Kelp Fly, Paractora Dreuxi Journal of Insect Physiology 47 (2001) 95–109 www.elsevier.com/locate/jinsphys Critical thermal limits, temperature tolerance and water balance of a sub-Antarctic kelp fly, Paractora dreuxi (Diptera: Helcomyzidae) C. Jaco Klok *, Steven L. Chown Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa Received 11 April 2000 Abstract Paractora dreuxi displays distinct ontogenetic differences in thermal tolerance and water balance. Larvae are moderately freeze tolerant. Mean larval onset of chill coma was Ϫ5.1°C, and onset of heat stupor was 35.5°C. Larval supercooling point (SCP) was Ϫ3.3°C with 100% recovery, although mortality was high below Ϫ4°C. Starvation caused SCP depression in the larvae. Adults were significantly less tolerant, with critical thermal limits of Ϫ2.7 and 30.2°C, no survival below the SCP (Ϫ9.6°C), and no change in SCP with starvation. Moderate freeze tolerance in the larvae supports the contention that this strategy is common in insects from southern, oceanic islands. Fly larvae survived desiccation in dry air for 30 h, and are thus less desiccation tolerant than most other sub-Antarctic insect larvae. Water loss rates of the adults were significantly lower than those of the larvae. Lipid metabolism did not contribute significantly to water replacement in larvae, which replaced lost body water by drinking fresh water, but not sea water. Kelp fly larvae had excellent haemolymph osmoregulatory abilities. Current climate change has led to increased temperatures and decreased rainfall on Marion Island. These changes are likely to have significant effects on P. dreuxi, and pro- nounced physiological regulation in larvae suggests that they will be most susceptible to such change. 2000 Elsevier Science Ltd. All rights reserved. Keywords: Ontogenetic differences; CTMin;CTMax; Freeze tolerance; Osmoregulation; Marion Island; Climate change 1. Introduction contributors to ecosystem functioning (Tre´hen et al., 1985; Crafford and Scholtz, 1987; Ha¨nel and Chown, The majority of studies concerning temperature and 1998). In consequence, there is little information avail- water relations of arthropods in the sub- and maritime able on the way in which these ecologically important Antarctic regions has concerned strictly terrestrial spec- arthropods cope with their often variable environments, ies. With the exception of a few studies of semi-aquatic and how their physiological responses differ to those of flies, beetles and copepods (Chown and Van Drimmelen, arthropods from terrestrial environments in the region. 1992; Chown, 1993; Convey and Block, 1996; Daven- Such comparisons are of considerable interest from port and MacAlister, 1996; Davenport et al., 1997), little three perspectives. First, the ways in which terrestrial emphasis has been given to environmental tolerances of and aquatic species cope with their respective environ- arthropods living in shoreline or semi-aquatic habitats ments are usually quite different (e.g. Lee and Denlinger, (see Block, 1984; Klok and Chown 1997, 1998; Sinclair, 1991; Hadley, 1994), yet many insect species make the 1999). Nonetheless, these habitats, and particularly the transition from one environment to the other as they shore zones, are characterized by high arthropod diver- develop. Although marked ontogenetic differences in sity (Bellido, 1981; Trave´, 1981; Chown, 1990; Marshall physiology have been documented in some insect spec- et al., 1999), of which a variety of species are major ies (Morrissey and Baust, 1976; Tre´hen and Vernon, 1986; Vernon, 1986; Vernon and Vannier 1986, 1996), the subtleties of such differences remain to be thor- * Corresponding author. Tel.: +2712-420-3236; fax: +2712-342- oughly explored (see Spicer and Gaston, 1999 for 3136. discussion). Second, it has been mooted repeatedly that E-mail address: [email protected] (C.J. Klok). the cold hardiness strategy adopted by most mid-latitude 0022-1910/00/$ - see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S0022-1910(00)00087-1 96 C.J. Klok, S.L. Chown / Journal of Insect Physiology 47 (2001) 95–109 southern hemisphere insect species is one of freeze toler- group, and lies 2100 km south east of Cape Town, and ance (e.g. Klok and Chown, 1997; Van der Merwe et to the north of the Antarctic Polar Front. It has a highly al., 1997). This is thought to be a consequence of the oceanic climate with mean monthly temperatures rang- oceanic nature of the region, which leads to generally ing from a winter low of 2°C to a summer high of 7°C moist habitats and, as a result, a high risk of freezing with little annual variation (Schulze, 1971; Blake, 1996). due to external inoculation by ice crystals. Nonetheless, Precipitation is in excess of 2000 mm per yr and the data with which to test this idea are limited, and it has island experiences a high degree of cloudiness (climate not been well-explored in species where adult and larval data from Schulze, 1971; Smith and Steenkamp, 1990). habitats might differ (see Addo-Bediako et al., 2000; Sea surface temperatures vary between 2°C in winter to Convey and Block, 1996 for exceptions). Third, differ- 8°C in summer with an annual mean of 5°C (De Villi- ences in the physiological tolerances of terrestrial and ers, 1976). aquatic species are not only likely to influence the range On boulder beaches, P. dreuxi larvae and adults occur of habitats they can occupy, and hence, ultimately differ- from just above the high water mark to the lower limit ences in their geographic ranges (Chown and Gaston, of closed vascular vegetation, feeding predominantly on 1999), but they may also influence the extent to which decaying kelp deposits, but also, facultatively, on seal changes in the abiotic environment will differentially and penguin carcasses and other carrion (Crafford, 1984; influence these species. The latter is of particular con- Tre´hen et al., 1985). Larval duration is approximately cern in Antarctic and sub-Antarctic environments where two months, of which instar III lasts for 40–50 days and climates are changing rapidly (Smith et al., 1996; Berg- is responsible for most kelp consumption. Mature instar strom and Chown, 1999). III larvae pupariate below the beach surface to a depth In this study we examine thermal tolerances and water of 50 cm. The pupal stage lasts for 30–60 days and the balance in adults and larvae of Paractora dreuxi Se´guy adults can live for 14–21 days (Crafford, 1984), feeding (Diptera: Helcomyzidae), a brachypterous kelp fly that on the slime that covers decaying kelp fronds (personal frequents kelp deposits in the littoral habitats on the observation). The largest biomass of third instar larvae coastlines of the Prince Edward and Crozet islands in is found in the supralittoral zone, 7–9 m from the shore- the sub-Antarctic (Crafford, 1984; Tre´hen et al., 1985; line. Both adults and larvae avoid the intertidal zone but Crafford and Scholtz, 1987). The associations of P. do occur in low densities in the splash zone (the upper dreuxi with kelp deposits differ markedly between the part of the eulittoral zone) situated 3–7 m from the larvae and the adults. The larvae are less mobile than shoreline (Crafford and Scholtz, 1987). Nonetheless, this adults and are mostly confined to kelp, or the substrate species may come into contact with seawater, either as below the kelp, where they either burrow into the fronds, saltspray blown ashore by high winds, or during storms feed between the fronds, or, in the later instars, feed on when large swells, which override the small (71 cm) the underlying detritus (Crafford, 1984; Crafford and tidal range, inundate the boulder beaches well into the Scholtz, 1987). Here they are subject to substantial fluc- supralittoral zone (De Villiers, 1976; Smith, 1977; Craf- tuations in temperature and water availability. In con- ford and Scholtz, 1987). trast, the shorter-lived adults, though brachypterous, are Large wrack beds are known to have stable internal highly mobile as a consequence of their search for ovi- temperatures compared to ambient temperatures position and feeding sites (Crafford, 1984; Tre´hen et al., (Crafford and Scholtz, 1987; Chown, 1996). However, 1985). However, they often take refuge, at least on sunshine, varying wind conditions, rainfall and sporadic Marion Island (Prince Edward group), between the boul- snowfalls do cause wide fluctuations in the microclimate ders below the kelp-substrate interface either when pred- of smaller kelp deposits, especially the smaller strings ators are present, or when weather conditions are that are also utilized by P. dreuxi (Crafford, 1984). Rela- unfavourable to them. Using flies collected at Marion tive to the stable ambient temperatures, temperatures in Island, we test the hypothesis that stage-related differ- kelp deposits on Marion Island can fluctuate widely, ences in association of P. dreuxi with stranded kelp will from below zero (mean of Ϫ2.3±0.5°C, range Ϫ1.3 to result in differences in their environmental tolerances. Ϫ3.0, n=10 observation days with single temperatures We also examine the idea that these differences will recorded during the early morning) in winter, to 29– affect the likely impact of climate change (especially 37°C during sunny days in early spring (Crafford, 1984, declining rainfall) on the stages. C.J. Klok, unpublished data). Furthermore, kelp deposits often desiccate completely despite the high rainfall at Marion Island (Crafford and Scholtz, 1987), although 2. Material and methods they rehydrate after rain, the main source of fresh water 2.1. Study site and animals on boulder beaches. This study was undertaken from May to October Sub-Antarctic Marion Island (46°54ЈS37°45ЈE) is the 1998, a period when low temperatures are common. larger of two islands forming the Prince Edward Islands Blake (1996) has demonstrated that in lowland areas of C.J.
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