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Habitat moisture availability and the local distribution of the Antarctic Collembola Cryptopygus antarcticus and Friesea grisea
Soil Biology & Biochemistry 36 (2004) 927–934 www.elsevier.com/locate/soilbio
Habitat moisture availability and the local distribution of the Antarctic Collembola Cryptopygus antarcticus and Friesea grisea Scott A.L. Haywarda,*, M. Roger Worlandb, Pete Conveyb, Jeff S. Balea b
a School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Received 24 March 2003; received in revised form 22 October 2003; accepted 1 February 2004
Abstract Population densities of the Collembola Cryptopygus antarcticus and Friesea grisea were compared in two maritime Antarctic habitats with different moisture availability. C. antarcticus was absent from the drier rock platform habitat, where F. grisea was the only collembolan collected. In contrast, the sand/pebble habitat on East Beach had greater moisture availability, and C. antarcticus dominated the arthropod community, with juveniles (individuals , 1 mm length) representing 58% of the population. The hygropreference characteristics of F. grisea were determined in relative humidity (RH) gradients (12 – 98% RH) at 10 and 20 8C. F. grisea demonstrated a stronger preference for 98% RH conditions than C. antarcticus, suggesting that the former species is less likely to vacate moist refuges when available. The movement of both species was also monitored at 10 and 15 8C under conditions of 33, 75 and 100% RH. C. antarcticus was more active than F. grisea at both temperatures, and its movement increased at a greater rate as a consequence of reduced RH. The limited desiccation tolerance of C. antarcticus, combined with the increased water loss that would result from its continued movement under declining RH conditions, suggests this species is not well suited to drought-prone environments. In contrast, the reduced movement and ‘risk averse’ behavioural strategy of F. grisea, i.e. taking advantage of moist refuges when available, facilitates water conservation between precipitation/habitat rehydration events. This study provides the first evidence that moisture availability and habitat structure are potential habitat segregation mechanisms between these two Antarctic Collembola. q 2004 Elsevier Ltd. All rights reserved. Keywords: Antarctic; Collembola; Moisture availability; Habitat segregation
1. Introduction Polar terrestrial environments have often been described as deserts, e.g. Llano (1956), where water availability is recognised as one of the most important limits on the distribution of terrestrial organisms (Kennedy, 1993). Collembola, in particular, are considered to be highly susceptible to desiccation because they rely on gas exchange across the cuticle for respiration in the absence of a tracheal system (Block and Harrisson, 1995). Dehydration tolerance differs between collembolan species (Joosse, 1971; Worland and Block, 1986; Hertzberg and Leinaas, 1998) often as a consequence of different cuticular permeability (Block et al., * Corresponding author. Address: Department of Entomology, The Ohio State University, 1735 Neil Avenue, 318 W. 12th Ave., Columbus OH, 43210, USA. Tel.: þ1-614-292-7287; fax: þ 1-614-292-2180. E-mail address: [email protected] (S.A.L. Hayward). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.02.007
1990). Such differences have been highlighted as a potential mechanism leading to habitat segregation in both temperate and Arctic environments (Joosse, 1981; Bauer and Christian, 1993; Hertzberg and Leinaas, 1998). The local distribution of Antarctic species also relates closely to their ability to resist desiccation (Worland and Block, 1986). Moisture availability can strongly influence insect activity, and Testerink (1982) indicated that some litterinhabiting Collembola stop locomotory activity as an immediate response to dry conditions. Other temperate species (e.g. Onychiurus armatus) also remain static, despite severe moisture stress, until they die (Bauer and Christian, 1993). Many species, however, actively move to track the moisture status of their habitat (Verhoef and van Selm, 1983; Hertzberg et al., 1994). Continued activity under desiccation stress may increase water loss through evapotranspiration, but it also increases the likelihood of locating moist refuges. In certain habitats therefore, it may
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be an advantageous behavioural strategy to actively seek moisture rather than wait for the environment to provide it. The amount of drought stress experienced often depends on habitat structure. Thick moss carpet on well-developed soil is likely to retain some moisture even after prolonged insolation. Dense vegetation also insulates from low temperatures, often reducing the likelihood of freezing at greater depths (Davey et al., 1992). However, unprotected and scattered vegetation on rocks, with poorly developed underlying soil is subject to extreme variations in moisture availability (Bauer and Christian, 1993) and temperature (Smith, 1988). The collembolan Cryptopygus antarcticus (Collembola, Isotomidae) is distributed throughout the maritime Antarctic (Tilbrook, 1967; Wallwork, 1973), and is the numerically dominant terrestrial microarthropod at many sites (Block, 1982a; Usher and Booth, 1984; Usher and Edwards, 1986), with populations reaching at least 1.5 £ 106 individuals m22 (Convey and Smith, 1997). This apparent dominance however, could be a consequence of the species’ favoured moss turf or carpet habitat being most amenable to arthropod extraction techniques (Convey and Smith, 1997). C. antarcticus is known to have limited desiccation tolerance (Block et al., 1990), but still occupies dry habitats (Block, 1982a). This species also possesses a furcula (jumping organ), which allows individuals to move rapidly and locate moist refuges if available. Friesea grisea (Collembola, Neanuridae) is also found throughout the maritime Antarctic (Lippert, 1971; Richard et al., 1994; Convey and Smith, 1997), though generally at lower densities, e.g. 2335 m22 (Block, 1982a). Its range extends into the continental Antarctic zone (Dallai et al., 1988), and it is believed to be the only true trans-Antarctic collembolan (Greenslade, 1995). No data exist on the desiccation tolerance of this species, while reports of preferred habitat portray conflicting views (Wise and Shoup, 1971; Lippert, 1971; Richard et al., 1994; Convey and Smith, 1997), with the most recent studies suggesting F. grisea is dominant in drier habitats. Current records suggest C. antarcticus and F. grisea often occur together, giving no indication of habitat segregation. While a number of studies have related differences in habitat use to drought resistance amongst Collembola (Joosse, 1981; Worland and Block, 1986; Bauer and Christian, 1993; Hertzberg et al., 1994; Hertzberg and Leinaas, 1998), much less is known about behavioural strategies underlying the ability of different species to occupy potentially stressful habitats (but see Hayward et al., 2000, 2001). We investigated the distribution of F. grisea and C. antarcticus within two contrasting terrestrial habitats in the maritime Antarctic. Patterns of dominance between these species were assessed with regard to differences in habitat moisture availability. Movement under desiccating conditions and hygropreference were also investigated to determine the role of moisture stress in habitat segregation.
2. Materials and methods 2.1. Study sites Rothera point (678340 S, 688080 W), in northern Marguerite Bay, is a low (maximum altitude 39 m) rock promontory at the southern extremity of the Wormald Ice Piedmont, with an ice-free area of ca. 1000 £ 250 m2 (Convey and Smith, 1997). On the east coast, there is a raised beach (Fig. 1) with patchily distributed vegetation of moss and algae (predominantly Prasiola crispa (Lightfoot) Meneghini), and an extensive snow bank providing meltwater channels for most of the summer. The west coast consists of rock platforms (Fig. 1) from which the snow clears early in the summer. There are isolated patches of P. crispa within less exposed sites, but these frequently dry out due to the lack of moisture in the substrate underneath. 2.2. Microclimate data and habitat patch desiccation A Campbell microclimate logger station incorporating miniature TRME-ES (IMKO, Ettlingen, Germany) Time Domain Reflectometry soil moisture sensors (3, 6 and 9 cm below surface) was set up on East Beach to record moisture availability (%water content m23) within the sand substrate (Fig. 2a), and precipitation (mm h21) (Fig. 2b), during
Fig. 1. Rothera point (678340 S. 688080 W) on the west coast of the Antarctic Peninsular (inset), indicating the main study sites: East Beach and the rock platform.
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placed in separate (10 l) containers. Two patches were placed directly on rock substrate, and the others inside containers half filled with sand (these patches were placed on tissue paper to prevent sand adhering to the vegetation). All four containers were then covered with a UV transparent perspex screen (40 cm above the container rim) to protect them from precipitation. Patches were weighed daily, at the same time, for 12 d, and their change in mass recorded. Each patch was then dried to constant mass at 45 8C and their dry mass and initial water content calculated. The moisture content of the sand substrate was determined gravimetrically at both the start and end of the 12 d period, and the mean moisture content calculated. 2.3. Sample collection, identification and storage Sample collections at both sites were made on 23 February 2000, after a period of rain. This ensured that recent climatic experiences were similar between sites, and that differences in arthropod content could not be attributed simply to differences in habitat moisture content at the time of collection. Ten similar sized (0.06 – 0.09 m2) P. crispa patches were selected at each site, using a quadrat, to limit differences between patches in moisture content/retention and the likelihood of being colonised by arthropods. Three vegetation cores (ca. 1 cm depth) were taken from each habitat patch on the rock platform (dia. 4 cm), and East Beach (dia. 2.5 cm), totalling 30 cores from each site. C. antarcticus (Willem) and F. grisea (Scha¨ffer) were the only two Collembola identified from all samples. Due to high densities of C. antarcticus on East Beach, smaller cores were used to limit the time taken to count and measure individuals. Samples were returned to the laboratory and Collembola extracted using two methods. (i)
Fig. 2. (a) Soil moisture (% m23) at three different depths on East Beach. (b) Precipitation levels (mm h21) for Rothera point from 6 to 26 February 2000. (c) P. crispa patch moisture content (calculated as percentage of initial water content) on either rock or sand substrate (n ¼ 2 for each substrate type), recorded daily for 12 d. Mean and standard errors are presented for each daily recording during a 12 d period.
February 2000. It was not possible to record moisture availability within the rock platform, which is assumed to be zero, though water films may persist on the rock surface under patches of vegetation. Thus, to aid site comparisons, the rate of P. crispa habitat patch desiccation was monitored on both rock and sand substrates. Four P. crispa patches (50 cm2), devoid of invertebrates, were weighed and each
Flotation method. P. crispa cores were placed in a beaker of water and agitated. Most Collembola floated to the surface and were collected for identification, measurement and counting under a binocular microscope (ii) Hand sorting. Sections of P. crispa were removed from the beaker and teased out into a single transparent sheet, under a binocular microscope, until all remaining individuals had been recorded. Collembola were identified with reference to Greenslade (1995), and mean population densities (individuals m22) calculated. C. antarcticus populations were split into two demographic groups (adults . 1 mm, juveniles , 1 mm) roughly according to size classes outlined by Tilbrook and Block (1972). Both C. antarcticus and F. grisea were maintained on moist P. crispa at 5 8C under constant illumination. As the hydration state of individuals can influence the results of both hygropreference (Madge, 1964) and activity
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experiments, two groups of 10 animals from each species were selected to determine mean water contents. Field fresh samples were weighed (Mettler UMT2 electronic microbalance, Beaumont Leys, Leicester, sensitivity ^ 0.25 mg) and then dried to constant mass at 45 8C. The dry mass was recorded and the mean initial water content calculated for each species. 2.4. Hygropreference Relative humidity (RH) gradients were generated using different saturated salt solutions: LiCl , 12% RH; MgCl2 , 33% RH; NaCl , 75% RH and K2SO4 , 98% RH. These were selected because they provided similar RH conditions across the range of temperatures investigated (Winston and Bates, 1960). The gradients were established in a grid chamber arrangement (Hayward et al., 2001), then placed inside a thermal containment system through which antifreeze solution was passed, and its temperature regulated using a thermal circulating bath (Lauda RCS6, Lauda Ko¨nigshofen, Germany). The temperature inside each chamber was monitored using an electronic thermometer (Comark, Stevenage, UK) with a miniature thermocouple attached, and once stable, eight animals (adults) were uniformly distributed across the gradient. Experiments were conducted in constant light at 10 and 20 8C and the position of each individual recorded every 10 min for 2 h. Four replicates were carried out for each regime. Small numbers of individuals were used to limit the influence of aggregative behaviour, and grid chambers employed to limit thigmotaxis (Hayward et al., 2000, 2001). The distribution was recorded by counting individuals within each humidity zone. When on the boundary of two zones, the position of the head was considered indicative of preference. The hygropreference of F. grisea was compared with that previously obtained for C. antarcticus (Hayward et al., 2001). 2.5. Movement under desiccation stress Using the same apparatus, the movement of both species was monitored at 10 and 15 8C under humidity conditions of 33, 75 and 100% RH. Single individuals (adults) were placed within square humidity chambers (4 £ 4 cm2) which had 64 grid squares marked on them. Animals were left for 2 min before recording their movement continuously for 5 min. Activity was measured as the number of grid lines crossed per unit time. Five replicates were carried out for each regime. 2.6. Statistical methods Chi-squared tests were employed to determine if the distribution of F. grisea within the RH gradient differed significantly from uniformity at the end of the observation period. Because the number of individuals in each
experiment was small, the sum of the final frequencies in each regime was used to calculate the test statistic. Twoway ANOVA’s were used to determine the significance of any difference in the amount of movement between the two species at each temperature for all humidities, and the degree of interaction between humidity and species factors. Differences in the rate of movement increase, as a consequence of changing RH, were determined using t-tests carried out on the linear regression coefficients of each species at each temperature.
3. Results 3.1. Site comparisons and habitat desiccation There was a clear difference in the distribution of F. grisea and C. antarcticus between the two sites. C. antarcticus was absent from P. crispa patches on the rock platform, while F. grisea was present in all 10 patches and was the only Collembola collected (mean density 750 ^ 212 individuals m22). On East Beach, C. antarcticus was dominant (mean density 99,668 ^ 24,734 individuals m22), and found in nine of the 10 patches sampled. Juveniles (, 1 mm in length) constituted 58% of the C. antarcticus population sampled. F. grisea occurred in only one of the 10 patches investigated (mean density 16.7 þ 16.7 individuals m22), which also included C. antarcticus. Patterns of water availability at 3 cm on East Beach (Fig. 2a) closely followed patterns of precipitation (Fig. 2b). At greater depths, moisture contents were higher and more stable. After 48 h without precipitation, P. crispa patches on the rock substrate lost almost 90% of their initial moisture content (Fig. 2c). It took 5 d before the moisture content of P. crispa patches on the sand substrate (mean moisture content 10.9 ^ 2.8%) dropped to this value (Fig. 2c). The moisture content of P. crispa patches on both substrate types remained similar after 6 d without precipitation. 3.2. Hygropreference and movement under desiccation stress Field fresh F. grisea and C. antarcticus had mean water contents of 66.4 ^ 3.7 and 68.9 ^ 4.9% (of fresh weight), respectively. F. grisea demonstrated a clear preference for the highest humidity (98% RH) at both 20 and 10 8C (Fig. 3) (x2 ¼ 80:74 and 25.76 at 20 and 10 8C, respectively, P , 0:01; 3 d.f.). C. antarcticus was significantly more mobile than F. grisea irrespective of RH at 10 8C (two-way ANOVA F1;24 ¼ 6:54; P , 0:05). For both species, there were highly significant differences in activity between humidities (twoway ANOVA F2;24 ¼ 13:71; P , 0:001) (Fig. 4a). At 15 8C (Fig. 4b), the difference in activity between species was not
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Table 1 Relationship between F. grisea and C. antarcticus mobility (activity assessed as grid lines crossed min21) and relative humidity at 10 and 158C, linear regression of data in Fig. 4 Species
Temperature (8C)
r2
F1;13
P
Regression coefficient
F. grisea
10 15 10 15
0.51 0.11 0.68 0.30
13.76 1.59 27.62 5.54
,0.01 0.23 ,0.001 ,0.05
20.0442 20.0166 20.0925 20.0413
C. antarcticus
Fig. 3. Distribution of F. grisea within RH gradients at 20 and 10 8C. Mean and standard errors are presented for 12 observations (four replicates for each temperature) n ¼ 8:
significant (F1;24 ¼ 2:91; P ¼ 0:101), but for both species, there was a significant difference in activity between humidities (F2;24 ¼ 5:61; P , 0:05). The interaction between species and RH factors was not significant at both temperatures (F2;24 ¼ 2:28; P ¼ 0:124 and F2;24 ¼ 0:68; P ¼ 0:515 for 10 and 15 8C, respectively).
Fig. 4. Mobility (activity assessed as grid lines crossed min21) of F. grisea and C. antarcticus over 5 min period at (a) 10 8C and (b) 15 8C. Mean and standard errors are presented, five replicates for each regime.
The regression coefficients of activity vs. RH (Table 1) were significantly different between species at 10 8C (t ¼ 2:272; P , 0:05; 26 d.f.), indicating C. antarcticus increased movement at a faster rate as a consequence of decreasing RH. The difference between the regression coefficients of each species at 15 8C was not significant (t ¼ 0:7316; 26 d.f.). C. antarcticus did not demonstrate a jumping response during any of the investigations.
4. Discussion 4.1. Site comparisons and habitat desiccation C. antarcticus is the dominant arthropod in most terrestrial habitats in north Maguerite Bay (Convey and Smith, 1997). This species is dispersed by both wind and meltwater, and is usually the first collembolan to colonise ‘new’ P. crispa habitats on Rothera point (S. Hayward, pers. obs.). Also, population densities on East Beach reached 256,000 individuals m22, indicating that this species is well established on Rothera Point. Thus, its absence from the rock platform site is somewhat of an anomaly for this area, and is unlikely to be the consequence of limited dispersal. F. grisea dominated the rock platform habitat, but its lower abundance on East Beach is somewhat surprising. This species is often found at low densities (Convey and Smith, 1997; Convey and Quintana, 1997), and maximum densities on the rock platform (3,571 individuals m22) equate to only 10 individuals per core. Different coring methods can produce inconsistent distribution patterns (Usher and Booth, 1986), and the smaller core used on East Beach may have resulted in F. grisea being under represented at this site. Also, the greater moisture availability at the East Beach site may mean that the distribution of F. grisea is less aggregated. Habitat moisture status can be a critical factor influencing species dominance patterns in terrestrial arthropod communities (Lindberg et al., 2002), and may explain the distinct switch in dominance from C. antarcticus to F. grisea between the East Beach and rock platform habitats. In contrast to East Beach, the rock platform has limited moisture availability outside P. crispa patches (Fig. 2a), and habitat patches desiccate more rapidly on the rock vs.
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sand substratum (Fig. 2c). P. crispa patches on rock lost almost 90% of their moisture content after 2 d without precipitation (Fig. 2c), and 2 d intervals between rainfall events were not uncommon at this location (Fig. 2b). If the vegetation layer on the rock platform dries out, the substrate underneath provides limited refuge from desiccation stress for terrestrial arthropods. In this environment, therefore, it may be an advantageous behavioural strategy to conserve water by limiting movement, and staying within moist refuges in the vegetation for as long as they remain available. In contrast, it took 5 d without rain for P. crispa patches on sand to lose 90% of their initial moisture content (Fig. 2c), and this interval between precipitation events was not recorded during our study (Fig. 2b). Meltwater streams also increased the moisture input of P. crispa patches on East Beach, relative to those on the rock platform. Furthermore, even when desiccating conditions existed on the surface of East Beach, water remained available deeper in the soil profile (Fig. 2a). Thus, terrestrial arthropods could retreat into the sand to avoid desiccation stress. 4.2. Hygropreference and movement under desiccation stress The mean initial water content of C. antarcticus samples (68.9 ^ 4.9%) corresponds with previous values for field fresh individuals (Block and Harrisson, 1995; Hayward et al., 2001), and accurately reflects their moisture status within maritime Antarctic habitats. F. grisea samples had similar mean water contents (66.4 ^ 3.7%), suggesting that the observed response of both species to desiccation stress is realistic to field conditions. At 20 8C, both F. grisea (Fig. 3) and C. antarcticus (Hayward et al., 2001) selected high RH conditions, indicating that neither species vacate moist refuges at this temperature. At 10 8C, F.grisea again preferred 98% RH conditions (Fig. 3), whereas C. antarcticus demonstrated no RH preference (Hayward et al., 2001). C. antarcticus was also consistently more active than F. grisea at low relative humidities (Fig. 4 and Table 1). This behaviour suggests that C. antarcticus is not restricted to moist environments, and can actively disperse across unfavourable interpatch zones. In environments where access to water is limited, however, it may be advantageous to employ a ‘risk averse’ strategy and remain in favourable microhabitats, as the probability of locating more favourable conditions is small. Collembola sensitive to dehydration often demonstrate intense reactions to reduced humidity to increase the probability of locating moisture (Joosse, 1971). Thus, F. grisea may be more tolerant of desiccation than C. antarcticus, as its response to locate moisture under low RH conditions appears less intense. Further studies comparing the desiccation tolerance of these species are required, however. The limited movement of F. grisea under desiccating conditions (Fig. 4), combined with a preference for moist habitats (Fig. 3), may limit active
dispersal between patches, but is likely to increase the survival time of individuals in habitats prone to drought. F. grisea also has a vestigial furcula, which reduces its ability to rapidly locate moisture when under desiccation stress. This further supports the benefits of a ‘risk averse’ behavioural strategy. Other polar Collembola with reduced/ absent furcula also demonstrate a response to remain at the ‘wet’ end of RH gradients (e.g. Onychiurus arcticus, Hayward et al., 2000). When a habitat patch desiccates individuals have the option to either vacate in search of moisture, or remain and wait for the environment to improve. It would be reasonable to hypothesise that species with a high dispersal tendency will emigrate to escape the deteriorating habitat, whereas species with low dispersal abilities remain (Harada, 1998), sometimes even to the point of death (see Bauer and Christian, 1993). Activity of C. antarcticus is strongly influenced by temperature (Schenker and Block, 1986; Burn and Lister, 1988), and although this species can tolerate periods of low humidity, emigration increases in response to habitat desiccation (S. Hayward, pers. obs.). Rapid patch desiccation on the rock platform, combined with high emigration and a lack of moist refuges, suggest extensive mortality. This provides further evidence as to why C. antarcticus may be excluded from this habitat. 4.3. Other factors influencing distribution patterns A number of other factors, in combination with habitat moisture availability, may contribute to the different species composition between sites. Mortality caused by desiccation is often selective with respect to size, with smaller individuals being more vulnerable due to their larger surface area-to-volume ratio (Leinaas and Fjellberg, 1985). Interestingly, F. grisea is stockier than C. antarcticus, and therefore, has a smaller surface area-to-volume ratio. Small size is not always a disadvantage, however, as small animals may be better able to penetrate into protected microhabitats if available (Ring et al., 1990). Block (1982a) found that small C. antarcticus (750 –1060 mm) dominated dry moss turf habitats on Signy Island, and wetter moss carpets were dominated (in terms of biomass) by larger individuals (1370 –1680 mm). Small individuals (, 1 mm) also dominated C. antarcticus populations on East Beach. The rock platform is more exposed than East Beach and, with a lower moisture content, has a reduced heat capacity. This means the site is more susceptible to freeze-thaw events, as well as lower summer and winter minimum temperatures. Data concerning the cold tolerance of F. grisea are limited, but Block (1982b) found that this species had lower supercooling points than C. antarcticus. Different Q10 responses to temperature, or different tolerances to high temperatures (irrespective of RH), may also influence species distribution patterns. The greater
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wind exposure experienced on the west coast rock platform habitat is also likely to further promote habitat desiccation, as well as increase salt water splash, which may be unfavourable to certain terrestrial arthropod species. Differences in diet quality and type between sites could also affect species composition. C. antarcticus is known to eat P. crispa (Worland and Lukesˇova´, 2000), but dried vegetation often has diminished palatability to insects as a result of low water content (Scriber, 1977). C. antarcticus also selects filamentous fungi as part of its diet (Broady, 1979), but the availability of fungi is often lower in dry habitats (Holding et al., 1974). Members of the genus Friesea, however, are typically predatory on nematodes, tardigrades and diatoms (P. Convey, pers. comm.). As certain Antarctic nematodes are known to enter a state of anhydrobiosis (Pickup and Rothery, 1991), the diet of F. grisea may be less restricted in environments prone to drought.
5. Conclusions In conclusion, a number of factors may exclude C. antarcticus from the rock platform habitat, but regular drying of P. crispa patches and the lack of moist refuges are likely to be of key importance. F. grisea appears to employ a more ‘risk averse’ behavioural strategy to desiccation stress, which may explain its ability to persist in drier habitats. Further studies of this species’ desiccation tolerance are required, however. Knowledge of the detailed small-scale distribution of Antarctic terrestrial arthropods is limited, and it is important that the often extremely dense aggregations of species such as C. antarcticus do not conceal other patterns of distribution and dominance (Convey and Smith, 1997). Also, by understanding the response of different species to changing habitat conditions, we can more accurately predict patterns of development in terrestrial communities as a consequence of climate change.
Acknowledgements S.A.L. Hayward was funded by a NERC CASE studentship at Birmingham University, in collaboration with British Antarctic Survey (BAS).
References Bauer, R., Christian, E., 1993. Adaptations of three springtail species to granite boulder habitats (Collembola). Pedobiologia 37, 280 –290. Block, W., 1982a. The Signy Island terrestrial reference sites: XIV. Population studies on the Collembola. British Antarctic Survey Bulletin 55, 33 –49. Block, W., 1982b. Supercooling points of insects and mites on the Antarctic Peninsula. Ecological Entomology 7, 1–8.
933
Block, W., Harrisson, P.M., 1995. Collembola water relations and environmental change in the maritime Antarctic. Global Change Biology 1, 347 –359. Block, W., Harrisson, P.M., Vannier, G., 1990. A comparative study of patterns of water loss from two Antarctic Springtails (Insecta, Collembola). Journal of Insect Physiology 36, 181–187. Broady, P.A., 1979. Feeding studies on the collembolan Cryptopygus antarcticus Willem at Signy Island, South Orkney Islands. British Antarctic Survey Bulletin 48, 37–46. Burn, A.J., Lister, A., 1988. Activity patterns in an Antarctic arthropod community. British Antarctic Survey Bulletin 78, 43–48. Convey, P., Quintana, R.D., 1997. The terrestrial arthropod fauna of Cierva Point SSSI, Danco Coast, northern Antarctic Peninsular. European Journal of Soil Biology 33, 19 –29. Convey, P., Smith, R.I.L., 1997. The terrestrial arthropod fauna and its habitats in northern Maguerite Bay and Alexander Island, maritime Antarctic. Antarctic Science 9, 12–26. Dallai, R., Malatesta, E., Focardi, S., 1988. On two Antarctic Collembola Gressittacantha terranova and Friesea grisea. Revue d’Ecologie et de Biologie du Sol 25, 365–372. Davey, M.C., Pickup, J., Block, W., 1992. Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island. Antarctic Science 4, 383– 388. Greenslade, P., 1995. Collembola from the Scotia Arc and Antarctic Peninsula including descriptions of two new species and notes on biogeography. Polskie Pismo Entomologiczne 64, 305 –319. Harada, T., 1998. To fly or not to fly: response of water striders to drying out of habitat. Ecological Entomology 23, 370– 376. Hayward, S.A.L., Worland, M.R., Bale, J.S., Convey, P., 2000. Temperature and the hygropreference of the Arctic Collembolan Onychiurus arcticus and mite Lauroppia translamellata. Physiological Entomology 25, 266–272. Hayward, S.A.L., Bale, J.S., Worland, M.R., Convey, P., 2001. Influence of temperature on the hygropreference of the Collembolan, Cryptopygus antarcticus, and the mite, Alaskozetes antarcticus from the maritime Antarctic. Journal of Insect Physiology 47, 11 –18. Hertzberg, K., Leinaas, H.P., 1998. Drought stress as a mortality factor in two pairs of sympatric species of Collembola at Spitzbergen, Svalbard. Polar Biology 19, 302–306. Hertzberg, K., Leinaas, H.P., Ims, R.A., 1994. Patterns of abundance and demography: Collembola in a habitat patch gradient. Ecography 17, 349– 359. Holding, A.J., Collins, V.G., French, D.D., D’Sylva, T., Baker, J.H., 1974. Relationship between viable bacterial counts and site characteristics in tundra. In: Holding, A.J., Heal, O.W., Maclean, S.F., Flanagan, P.W. (Eds.), Soil Organisms and Decomposition in Tundra, Swedish IBP Committee, Stockholm, pp. 49 –64. Joosse, E.N.G., 1971. Ecological aspects of aggregation in Collembola. Revue d’Ecologie et de Biologie du Sol 8, 91–97. Joosse, E.N.G., 1981. Ecological strategies and population regulation of Collembola in heterogeneous environments. Pedobiologia 21, 346– 356. Kennedy, A.D., 1993. Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arctic and Alpine Research 25, 308–315. Leinaas, H.P., Fjellberg, A., 1985. Habitat structure and life history strategies of two, partly sympatric and closely related, lichen feeding Collembola species. Oikos 44, 448–458. Lindberg, N., Engtsson, J.B., Persson, T., 2002. Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. Journal of Applied Ecology 39, 924 –936. Lippert, G., 1971. Occurrence of arthropods in mosses at Anvers Island, Antarctic Peninsula. Pacific Insects Monograph 25, 137 –144. Llano, G.A., 1956. Botanical research essential to a knowledge of Antarctica. In: Crary, A.P., Gould, L.M., Hulbert, E.O., Odishaw, H., Smith, W.E. (Eds.), Antarctica in the Geophysical Year
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(Geophysical Monograph No. 1), American Geophysical Union, Washington, DC, pp. 124– 133. Madge, D.S., 1964. The humidity reactions of Oribatid mites. Acarologia 6, 566– 591. Pickup, J., Rothery, P., 1991. Water-loss and anhydrobiotic survival in nematodes of Antarctic fellfields. Oikos 61, 379–388. Richard, K.J., Convey, P., Block, W., 1994. The terrestrial arthropod fauna of the Byers Peninsular, Livingston Island, South Shetland Islands. Polar Biology 14, 371–379. Ring, R.A., Block, W., Sømme, L., Worland, M.R., 1990. Body water content and desiccation resistance in some arthropods from Subantarctic South Georgia. Polar Biology 10, 581–588. Schenker, R., Block, W., 1986. Micro-arthropod activity in three contrasting terrestrial habitats on Signy Island, maritime Antarctic. British Antarctic Survey Bulletin 71, 31 –43. Scriber, J.M., 1977. Limiting effects of low leaf-water content on the nitrogen utilisation, energy budget and growth of Hyalophora cercropia (Lepidoptera: Saturniidae). Oecologia 28, 269–287. Smith, R.I.L., 1988. Recording bryophyte microclimate in remote and severe environments. In: Glime, J.M., (Ed.), Methods in Bryology, Hattori Botanical Laboratory, Nichinan, pp. 275–284. Testerink, G.J., 1982. Metabolic adaptations to seasonal changes in humidity and temperature in litter-inhabiting springtails. Oikos 40, 234– 340. Tilbrook, P.J., 1967. The terrestrial invertebrate fauna of the maritime Antarctic. Philosophical Transactions of the Royal Society of London B 252, 261–278.
Tilbrook, P.J., Block, W., 1972. Oxygen uptake in an Antarctic collembole, Cryptopygus antarcticus. Oikos 23, 313–317. Usher, M.B., Booth, R.G., 1984. Arthropod communities in a maritime Antarctic moss-turf habitat: three dimensional distribution of mites and Collembola. Journal of Animal Ecology 53, 427–441. Usher, M.B., Booth, R.G., 1986. Arthropod communities in a maritime Antarctic moss-turf habitat: multiple scales of pattern in the mites and collembola. Journal of Animal Ecology 55, 155–170. Usher, M.B., Edwards, M., 1986. The selection of conservation areas in Antarctica: an example using the arthropod fauna of Antarctic islands. Environmental Conservation 13, 115–122. Verhoef, H.A., van Selm, A.J., 1983. Distribution and population dynamics of Collembola in relation to soil moisture. Holarctic Ecology 6, 387 –394. Wallwork, J.A., 1973. Zoogeography of some terrestrial micro-Arthropoda in Antarctica. Biological Reviews 48, 233 –259. Winston, P.W., Bates, D.H., 1960. Saturated solutions for the control of humidity in biological research. Ecology 41, 232 –237. Wise, K.A.J., Shoup, J., 1971. Entomological investigations in Antarctica, 1964–65 season. Pacific Insects Monograph 25, 27–56. Worland, M.R., Block, W., 1986. Survival and water loss in some Antarctic arthropods. Journal of Insect Physiology 32, 579–584. Worland, M.R., Lukesˇova´, A., 2000. The effect of feeding on specific soil algae on the cold-hardiness of two Antarctic micro-arthropods (Alaskozetes antarcticus and Cryptopygus antarcticus). Polar Biology 23, 766–777.
Habitat moisture availability and the local distribution of the Antarctic Collembola Cryptopygus antarcticus and Friesea grisea Scott A.L. Haywarda,*, M. Roger Worlandb, Pete Conveyb, Jeff S. Balea b
a School of Biosciences, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK
Received 24 March 2003; received in revised form 22 October 2003; accepted 1 February 2004
Abstract Population densities of the Collembola Cryptopygus antarcticus and Friesea grisea were compared in two maritime Antarctic habitats with different moisture availability. C. antarcticus was absent from the drier rock platform habitat, where F. grisea was the only collembolan collected. In contrast, the sand/pebble habitat on East Beach had greater moisture availability, and C. antarcticus dominated the arthropod community, with juveniles (individuals , 1 mm length) representing 58% of the population. The hygropreference characteristics of F. grisea were determined in relative humidity (RH) gradients (12 – 98% RH) at 10 and 20 8C. F. grisea demonstrated a stronger preference for 98% RH conditions than C. antarcticus, suggesting that the former species is less likely to vacate moist refuges when available. The movement of both species was also monitored at 10 and 15 8C under conditions of 33, 75 and 100% RH. C. antarcticus was more active than F. grisea at both temperatures, and its movement increased at a greater rate as a consequence of reduced RH. The limited desiccation tolerance of C. antarcticus, combined with the increased water loss that would result from its continued movement under declining RH conditions, suggests this species is not well suited to drought-prone environments. In contrast, the reduced movement and ‘risk averse’ behavioural strategy of F. grisea, i.e. taking advantage of moist refuges when available, facilitates water conservation between precipitation/habitat rehydration events. This study provides the first evidence that moisture availability and habitat structure are potential habitat segregation mechanisms between these two Antarctic Collembola. q 2004 Elsevier Ltd. All rights reserved. Keywords: Antarctic; Collembola; Moisture availability; Habitat segregation
1. Introduction Polar terrestrial environments have often been described as deserts, e.g. Llano (1956), where water availability is recognised as one of the most important limits on the distribution of terrestrial organisms (Kennedy, 1993). Collembola, in particular, are considered to be highly susceptible to desiccation because they rely on gas exchange across the cuticle for respiration in the absence of a tracheal system (Block and Harrisson, 1995). Dehydration tolerance differs between collembolan species (Joosse, 1971; Worland and Block, 1986; Hertzberg and Leinaas, 1998) often as a consequence of different cuticular permeability (Block et al., * Corresponding author. Address: Department of Entomology, The Ohio State University, 1735 Neil Avenue, 318 W. 12th Ave., Columbus OH, 43210, USA. Tel.: þ1-614-292-7287; fax: þ 1-614-292-2180. E-mail address: [email protected] (S.A.L. Hayward). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.02.007
1990). Such differences have been highlighted as a potential mechanism leading to habitat segregation in both temperate and Arctic environments (Joosse, 1981; Bauer and Christian, 1993; Hertzberg and Leinaas, 1998). The local distribution of Antarctic species also relates closely to their ability to resist desiccation (Worland and Block, 1986). Moisture availability can strongly influence insect activity, and Testerink (1982) indicated that some litterinhabiting Collembola stop locomotory activity as an immediate response to dry conditions. Other temperate species (e.g. Onychiurus armatus) also remain static, despite severe moisture stress, until they die (Bauer and Christian, 1993). Many species, however, actively move to track the moisture status of their habitat (Verhoef and van Selm, 1983; Hertzberg et al., 1994). Continued activity under desiccation stress may increase water loss through evapotranspiration, but it also increases the likelihood of locating moist refuges. In certain habitats therefore, it may
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be an advantageous behavioural strategy to actively seek moisture rather than wait for the environment to provide it. The amount of drought stress experienced often depends on habitat structure. Thick moss carpet on well-developed soil is likely to retain some moisture even after prolonged insolation. Dense vegetation also insulates from low temperatures, often reducing the likelihood of freezing at greater depths (Davey et al., 1992). However, unprotected and scattered vegetation on rocks, with poorly developed underlying soil is subject to extreme variations in moisture availability (Bauer and Christian, 1993) and temperature (Smith, 1988). The collembolan Cryptopygus antarcticus (Collembola, Isotomidae) is distributed throughout the maritime Antarctic (Tilbrook, 1967; Wallwork, 1973), and is the numerically dominant terrestrial microarthropod at many sites (Block, 1982a; Usher and Booth, 1984; Usher and Edwards, 1986), with populations reaching at least 1.5 £ 106 individuals m22 (Convey and Smith, 1997). This apparent dominance however, could be a consequence of the species’ favoured moss turf or carpet habitat being most amenable to arthropod extraction techniques (Convey and Smith, 1997). C. antarcticus is known to have limited desiccation tolerance (Block et al., 1990), but still occupies dry habitats (Block, 1982a). This species also possesses a furcula (jumping organ), which allows individuals to move rapidly and locate moist refuges if available. Friesea grisea (Collembola, Neanuridae) is also found throughout the maritime Antarctic (Lippert, 1971; Richard et al., 1994; Convey and Smith, 1997), though generally at lower densities, e.g. 2335 m22 (Block, 1982a). Its range extends into the continental Antarctic zone (Dallai et al., 1988), and it is believed to be the only true trans-Antarctic collembolan (Greenslade, 1995). No data exist on the desiccation tolerance of this species, while reports of preferred habitat portray conflicting views (Wise and Shoup, 1971; Lippert, 1971; Richard et al., 1994; Convey and Smith, 1997), with the most recent studies suggesting F. grisea is dominant in drier habitats. Current records suggest C. antarcticus and F. grisea often occur together, giving no indication of habitat segregation. While a number of studies have related differences in habitat use to drought resistance amongst Collembola (Joosse, 1981; Worland and Block, 1986; Bauer and Christian, 1993; Hertzberg et al., 1994; Hertzberg and Leinaas, 1998), much less is known about behavioural strategies underlying the ability of different species to occupy potentially stressful habitats (but see Hayward et al., 2000, 2001). We investigated the distribution of F. grisea and C. antarcticus within two contrasting terrestrial habitats in the maritime Antarctic. Patterns of dominance between these species were assessed with regard to differences in habitat moisture availability. Movement under desiccating conditions and hygropreference were also investigated to determine the role of moisture stress in habitat segregation.
2. Materials and methods 2.1. Study sites Rothera point (678340 S, 688080 W), in northern Marguerite Bay, is a low (maximum altitude 39 m) rock promontory at the southern extremity of the Wormald Ice Piedmont, with an ice-free area of ca. 1000 £ 250 m2 (Convey and Smith, 1997). On the east coast, there is a raised beach (Fig. 1) with patchily distributed vegetation of moss and algae (predominantly Prasiola crispa (Lightfoot) Meneghini), and an extensive snow bank providing meltwater channels for most of the summer. The west coast consists of rock platforms (Fig. 1) from which the snow clears early in the summer. There are isolated patches of P. crispa within less exposed sites, but these frequently dry out due to the lack of moisture in the substrate underneath. 2.2. Microclimate data and habitat patch desiccation A Campbell microclimate logger station incorporating miniature TRME-ES (IMKO, Ettlingen, Germany) Time Domain Reflectometry soil moisture sensors (3, 6 and 9 cm below surface) was set up on East Beach to record moisture availability (%water content m23) within the sand substrate (Fig. 2a), and precipitation (mm h21) (Fig. 2b), during
Fig. 1. Rothera point (678340 S. 688080 W) on the west coast of the Antarctic Peninsular (inset), indicating the main study sites: East Beach and the rock platform.
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placed in separate (10 l) containers. Two patches were placed directly on rock substrate, and the others inside containers half filled with sand (these patches were placed on tissue paper to prevent sand adhering to the vegetation). All four containers were then covered with a UV transparent perspex screen (40 cm above the container rim) to protect them from precipitation. Patches were weighed daily, at the same time, for 12 d, and their change in mass recorded. Each patch was then dried to constant mass at 45 8C and their dry mass and initial water content calculated. The moisture content of the sand substrate was determined gravimetrically at both the start and end of the 12 d period, and the mean moisture content calculated. 2.3. Sample collection, identification and storage Sample collections at both sites were made on 23 February 2000, after a period of rain. This ensured that recent climatic experiences were similar between sites, and that differences in arthropod content could not be attributed simply to differences in habitat moisture content at the time of collection. Ten similar sized (0.06 – 0.09 m2) P. crispa patches were selected at each site, using a quadrat, to limit differences between patches in moisture content/retention and the likelihood of being colonised by arthropods. Three vegetation cores (ca. 1 cm depth) were taken from each habitat patch on the rock platform (dia. 4 cm), and East Beach (dia. 2.5 cm), totalling 30 cores from each site. C. antarcticus (Willem) and F. grisea (Scha¨ffer) were the only two Collembola identified from all samples. Due to high densities of C. antarcticus on East Beach, smaller cores were used to limit the time taken to count and measure individuals. Samples were returned to the laboratory and Collembola extracted using two methods. (i)
Fig. 2. (a) Soil moisture (% m23) at three different depths on East Beach. (b) Precipitation levels (mm h21) for Rothera point from 6 to 26 February 2000. (c) P. crispa patch moisture content (calculated as percentage of initial water content) on either rock or sand substrate (n ¼ 2 for each substrate type), recorded daily for 12 d. Mean and standard errors are presented for each daily recording during a 12 d period.
February 2000. It was not possible to record moisture availability within the rock platform, which is assumed to be zero, though water films may persist on the rock surface under patches of vegetation. Thus, to aid site comparisons, the rate of P. crispa habitat patch desiccation was monitored on both rock and sand substrates. Four P. crispa patches (50 cm2), devoid of invertebrates, were weighed and each
Flotation method. P. crispa cores were placed in a beaker of water and agitated. Most Collembola floated to the surface and were collected for identification, measurement and counting under a binocular microscope (ii) Hand sorting. Sections of P. crispa were removed from the beaker and teased out into a single transparent sheet, under a binocular microscope, until all remaining individuals had been recorded. Collembola were identified with reference to Greenslade (1995), and mean population densities (individuals m22) calculated. C. antarcticus populations were split into two demographic groups (adults . 1 mm, juveniles , 1 mm) roughly according to size classes outlined by Tilbrook and Block (1972). Both C. antarcticus and F. grisea were maintained on moist P. crispa at 5 8C under constant illumination. As the hydration state of individuals can influence the results of both hygropreference (Madge, 1964) and activity
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experiments, two groups of 10 animals from each species were selected to determine mean water contents. Field fresh samples were weighed (Mettler UMT2 electronic microbalance, Beaumont Leys, Leicester, sensitivity ^ 0.25 mg) and then dried to constant mass at 45 8C. The dry mass was recorded and the mean initial water content calculated for each species. 2.4. Hygropreference Relative humidity (RH) gradients were generated using different saturated salt solutions: LiCl , 12% RH; MgCl2 , 33% RH; NaCl , 75% RH and K2SO4 , 98% RH. These were selected because they provided similar RH conditions across the range of temperatures investigated (Winston and Bates, 1960). The gradients were established in a grid chamber arrangement (Hayward et al., 2001), then placed inside a thermal containment system through which antifreeze solution was passed, and its temperature regulated using a thermal circulating bath (Lauda RCS6, Lauda Ko¨nigshofen, Germany). The temperature inside each chamber was monitored using an electronic thermometer (Comark, Stevenage, UK) with a miniature thermocouple attached, and once stable, eight animals (adults) were uniformly distributed across the gradient. Experiments were conducted in constant light at 10 and 20 8C and the position of each individual recorded every 10 min for 2 h. Four replicates were carried out for each regime. Small numbers of individuals were used to limit the influence of aggregative behaviour, and grid chambers employed to limit thigmotaxis (Hayward et al., 2000, 2001). The distribution was recorded by counting individuals within each humidity zone. When on the boundary of two zones, the position of the head was considered indicative of preference. The hygropreference of F. grisea was compared with that previously obtained for C. antarcticus (Hayward et al., 2001). 2.5. Movement under desiccation stress Using the same apparatus, the movement of both species was monitored at 10 and 15 8C under humidity conditions of 33, 75 and 100% RH. Single individuals (adults) were placed within square humidity chambers (4 £ 4 cm2) which had 64 grid squares marked on them. Animals were left for 2 min before recording their movement continuously for 5 min. Activity was measured as the number of grid lines crossed per unit time. Five replicates were carried out for each regime. 2.6. Statistical methods Chi-squared tests were employed to determine if the distribution of F. grisea within the RH gradient differed significantly from uniformity at the end of the observation period. Because the number of individuals in each
experiment was small, the sum of the final frequencies in each regime was used to calculate the test statistic. Twoway ANOVA’s were used to determine the significance of any difference in the amount of movement between the two species at each temperature for all humidities, and the degree of interaction between humidity and species factors. Differences in the rate of movement increase, as a consequence of changing RH, were determined using t-tests carried out on the linear regression coefficients of each species at each temperature.
3. Results 3.1. Site comparisons and habitat desiccation There was a clear difference in the distribution of F. grisea and C. antarcticus between the two sites. C. antarcticus was absent from P. crispa patches on the rock platform, while F. grisea was present in all 10 patches and was the only Collembola collected (mean density 750 ^ 212 individuals m22). On East Beach, C. antarcticus was dominant (mean density 99,668 ^ 24,734 individuals m22), and found in nine of the 10 patches sampled. Juveniles (, 1 mm in length) constituted 58% of the C. antarcticus population sampled. F. grisea occurred in only one of the 10 patches investigated (mean density 16.7 þ 16.7 individuals m22), which also included C. antarcticus. Patterns of water availability at 3 cm on East Beach (Fig. 2a) closely followed patterns of precipitation (Fig. 2b). At greater depths, moisture contents were higher and more stable. After 48 h without precipitation, P. crispa patches on the rock substrate lost almost 90% of their initial moisture content (Fig. 2c). It took 5 d before the moisture content of P. crispa patches on the sand substrate (mean moisture content 10.9 ^ 2.8%) dropped to this value (Fig. 2c). The moisture content of P. crispa patches on both substrate types remained similar after 6 d without precipitation. 3.2. Hygropreference and movement under desiccation stress Field fresh F. grisea and C. antarcticus had mean water contents of 66.4 ^ 3.7 and 68.9 ^ 4.9% (of fresh weight), respectively. F. grisea demonstrated a clear preference for the highest humidity (98% RH) at both 20 and 10 8C (Fig. 3) (x2 ¼ 80:74 and 25.76 at 20 and 10 8C, respectively, P , 0:01; 3 d.f.). C. antarcticus was significantly more mobile than F. grisea irrespective of RH at 10 8C (two-way ANOVA F1;24 ¼ 6:54; P , 0:05). For both species, there were highly significant differences in activity between humidities (twoway ANOVA F2;24 ¼ 13:71; P , 0:001) (Fig. 4a). At 15 8C (Fig. 4b), the difference in activity between species was not
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Table 1 Relationship between F. grisea and C. antarcticus mobility (activity assessed as grid lines crossed min21) and relative humidity at 10 and 158C, linear regression of data in Fig. 4 Species
Temperature (8C)
r2
F1;13
P
Regression coefficient
F. grisea
10 15 10 15
0.51 0.11 0.68 0.30
13.76 1.59 27.62 5.54
,0.01 0.23 ,0.001 ,0.05
20.0442 20.0166 20.0925 20.0413
C. antarcticus
Fig. 3. Distribution of F. grisea within RH gradients at 20 and 10 8C. Mean and standard errors are presented for 12 observations (four replicates for each temperature) n ¼ 8:
significant (F1;24 ¼ 2:91; P ¼ 0:101), but for both species, there was a significant difference in activity between humidities (F2;24 ¼ 5:61; P , 0:05). The interaction between species and RH factors was not significant at both temperatures (F2;24 ¼ 2:28; P ¼ 0:124 and F2;24 ¼ 0:68; P ¼ 0:515 for 10 and 15 8C, respectively).
Fig. 4. Mobility (activity assessed as grid lines crossed min21) of F. grisea and C. antarcticus over 5 min period at (a) 10 8C and (b) 15 8C. Mean and standard errors are presented, five replicates for each regime.
The regression coefficients of activity vs. RH (Table 1) were significantly different between species at 10 8C (t ¼ 2:272; P , 0:05; 26 d.f.), indicating C. antarcticus increased movement at a faster rate as a consequence of decreasing RH. The difference between the regression coefficients of each species at 15 8C was not significant (t ¼ 0:7316; 26 d.f.). C. antarcticus did not demonstrate a jumping response during any of the investigations.
4. Discussion 4.1. Site comparisons and habitat desiccation C. antarcticus is the dominant arthropod in most terrestrial habitats in north Maguerite Bay (Convey and Smith, 1997). This species is dispersed by both wind and meltwater, and is usually the first collembolan to colonise ‘new’ P. crispa habitats on Rothera point (S. Hayward, pers. obs.). Also, population densities on East Beach reached 256,000 individuals m22, indicating that this species is well established on Rothera Point. Thus, its absence from the rock platform site is somewhat of an anomaly for this area, and is unlikely to be the consequence of limited dispersal. F. grisea dominated the rock platform habitat, but its lower abundance on East Beach is somewhat surprising. This species is often found at low densities (Convey and Smith, 1997; Convey and Quintana, 1997), and maximum densities on the rock platform (3,571 individuals m22) equate to only 10 individuals per core. Different coring methods can produce inconsistent distribution patterns (Usher and Booth, 1986), and the smaller core used on East Beach may have resulted in F. grisea being under represented at this site. Also, the greater moisture availability at the East Beach site may mean that the distribution of F. grisea is less aggregated. Habitat moisture status can be a critical factor influencing species dominance patterns in terrestrial arthropod communities (Lindberg et al., 2002), and may explain the distinct switch in dominance from C. antarcticus to F. grisea between the East Beach and rock platform habitats. In contrast to East Beach, the rock platform has limited moisture availability outside P. crispa patches (Fig. 2a), and habitat patches desiccate more rapidly on the rock vs.
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sand substratum (Fig. 2c). P. crispa patches on rock lost almost 90% of their moisture content after 2 d without precipitation (Fig. 2c), and 2 d intervals between rainfall events were not uncommon at this location (Fig. 2b). If the vegetation layer on the rock platform dries out, the substrate underneath provides limited refuge from desiccation stress for terrestrial arthropods. In this environment, therefore, it may be an advantageous behavioural strategy to conserve water by limiting movement, and staying within moist refuges in the vegetation for as long as they remain available. In contrast, it took 5 d without rain for P. crispa patches on sand to lose 90% of their initial moisture content (Fig. 2c), and this interval between precipitation events was not recorded during our study (Fig. 2b). Meltwater streams also increased the moisture input of P. crispa patches on East Beach, relative to those on the rock platform. Furthermore, even when desiccating conditions existed on the surface of East Beach, water remained available deeper in the soil profile (Fig. 2a). Thus, terrestrial arthropods could retreat into the sand to avoid desiccation stress. 4.2. Hygropreference and movement under desiccation stress The mean initial water content of C. antarcticus samples (68.9 ^ 4.9%) corresponds with previous values for field fresh individuals (Block and Harrisson, 1995; Hayward et al., 2001), and accurately reflects their moisture status within maritime Antarctic habitats. F. grisea samples had similar mean water contents (66.4 ^ 3.7%), suggesting that the observed response of both species to desiccation stress is realistic to field conditions. At 20 8C, both F. grisea (Fig. 3) and C. antarcticus (Hayward et al., 2001) selected high RH conditions, indicating that neither species vacate moist refuges at this temperature. At 10 8C, F.grisea again preferred 98% RH conditions (Fig. 3), whereas C. antarcticus demonstrated no RH preference (Hayward et al., 2001). C. antarcticus was also consistently more active than F. grisea at low relative humidities (Fig. 4 and Table 1). This behaviour suggests that C. antarcticus is not restricted to moist environments, and can actively disperse across unfavourable interpatch zones. In environments where access to water is limited, however, it may be advantageous to employ a ‘risk averse’ strategy and remain in favourable microhabitats, as the probability of locating more favourable conditions is small. Collembola sensitive to dehydration often demonstrate intense reactions to reduced humidity to increase the probability of locating moisture (Joosse, 1971). Thus, F. grisea may be more tolerant of desiccation than C. antarcticus, as its response to locate moisture under low RH conditions appears less intense. Further studies comparing the desiccation tolerance of these species are required, however. The limited movement of F. grisea under desiccating conditions (Fig. 4), combined with a preference for moist habitats (Fig. 3), may limit active
dispersal between patches, but is likely to increase the survival time of individuals in habitats prone to drought. F. grisea also has a vestigial furcula, which reduces its ability to rapidly locate moisture when under desiccation stress. This further supports the benefits of a ‘risk averse’ behavioural strategy. Other polar Collembola with reduced/ absent furcula also demonstrate a response to remain at the ‘wet’ end of RH gradients (e.g. Onychiurus arcticus, Hayward et al., 2000). When a habitat patch desiccates individuals have the option to either vacate in search of moisture, or remain and wait for the environment to improve. It would be reasonable to hypothesise that species with a high dispersal tendency will emigrate to escape the deteriorating habitat, whereas species with low dispersal abilities remain (Harada, 1998), sometimes even to the point of death (see Bauer and Christian, 1993). Activity of C. antarcticus is strongly influenced by temperature (Schenker and Block, 1986; Burn and Lister, 1988), and although this species can tolerate periods of low humidity, emigration increases in response to habitat desiccation (S. Hayward, pers. obs.). Rapid patch desiccation on the rock platform, combined with high emigration and a lack of moist refuges, suggest extensive mortality. This provides further evidence as to why C. antarcticus may be excluded from this habitat. 4.3. Other factors influencing distribution patterns A number of other factors, in combination with habitat moisture availability, may contribute to the different species composition between sites. Mortality caused by desiccation is often selective with respect to size, with smaller individuals being more vulnerable due to their larger surface area-to-volume ratio (Leinaas and Fjellberg, 1985). Interestingly, F. grisea is stockier than C. antarcticus, and therefore, has a smaller surface area-to-volume ratio. Small size is not always a disadvantage, however, as small animals may be better able to penetrate into protected microhabitats if available (Ring et al., 1990). Block (1982a) found that small C. antarcticus (750 –1060 mm) dominated dry moss turf habitats on Signy Island, and wetter moss carpets were dominated (in terms of biomass) by larger individuals (1370 –1680 mm). Small individuals (, 1 mm) also dominated C. antarcticus populations on East Beach. The rock platform is more exposed than East Beach and, with a lower moisture content, has a reduced heat capacity. This means the site is more susceptible to freeze-thaw events, as well as lower summer and winter minimum temperatures. Data concerning the cold tolerance of F. grisea are limited, but Block (1982b) found that this species had lower supercooling points than C. antarcticus. Different Q10 responses to temperature, or different tolerances to high temperatures (irrespective of RH), may also influence species distribution patterns. The greater
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wind exposure experienced on the west coast rock platform habitat is also likely to further promote habitat desiccation, as well as increase salt water splash, which may be unfavourable to certain terrestrial arthropod species. Differences in diet quality and type between sites could also affect species composition. C. antarcticus is known to eat P. crispa (Worland and Lukesˇova´, 2000), but dried vegetation often has diminished palatability to insects as a result of low water content (Scriber, 1977). C. antarcticus also selects filamentous fungi as part of its diet (Broady, 1979), but the availability of fungi is often lower in dry habitats (Holding et al., 1974). Members of the genus Friesea, however, are typically predatory on nematodes, tardigrades and diatoms (P. Convey, pers. comm.). As certain Antarctic nematodes are known to enter a state of anhydrobiosis (Pickup and Rothery, 1991), the diet of F. grisea may be less restricted in environments prone to drought.
5. Conclusions In conclusion, a number of factors may exclude C. antarcticus from the rock platform habitat, but regular drying of P. crispa patches and the lack of moist refuges are likely to be of key importance. F. grisea appears to employ a more ‘risk averse’ behavioural strategy to desiccation stress, which may explain its ability to persist in drier habitats. Further studies of this species’ desiccation tolerance are required, however. Knowledge of the detailed small-scale distribution of Antarctic terrestrial arthropods is limited, and it is important that the often extremely dense aggregations of species such as C. antarcticus do not conceal other patterns of distribution and dominance (Convey and Smith, 1997). Also, by understanding the response of different species to changing habitat conditions, we can more accurately predict patterns of development in terrestrial communities as a consequence of climate change.
Acknowledgements S.A.L. Hayward was funded by a NERC CASE studentship at Birmingham University, in collaboration with British Antarctic Survey (BAS).
References Bauer, R., Christian, E., 1993. Adaptations of three springtail species to granite boulder habitats (Collembola). Pedobiologia 37, 280 –290. Block, W., 1982a. The Signy Island terrestrial reference sites: XIV. Population studies on the Collembola. British Antarctic Survey Bulletin 55, 33 –49. Block, W., 1982b. Supercooling points of insects and mites on the Antarctic Peninsula. Ecological Entomology 7, 1–8.
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Block, W., Harrisson, P.M., 1995. Collembola water relations and environmental change in the maritime Antarctic. Global Change Biology 1, 347 –359. Block, W., Harrisson, P.M., Vannier, G., 1990. A comparative study of patterns of water loss from two Antarctic Springtails (Insecta, Collembola). Journal of Insect Physiology 36, 181–187. Broady, P.A., 1979. Feeding studies on the collembolan Cryptopygus antarcticus Willem at Signy Island, South Orkney Islands. British Antarctic Survey Bulletin 48, 37–46. Burn, A.J., Lister, A., 1988. Activity patterns in an Antarctic arthropod community. British Antarctic Survey Bulletin 78, 43–48. Convey, P., Quintana, R.D., 1997. The terrestrial arthropod fauna of Cierva Point SSSI, Danco Coast, northern Antarctic Peninsular. European Journal of Soil Biology 33, 19 –29. Convey, P., Smith, R.I.L., 1997. The terrestrial arthropod fauna and its habitats in northern Maguerite Bay and Alexander Island, maritime Antarctic. Antarctic Science 9, 12–26. Dallai, R., Malatesta, E., Focardi, S., 1988. On two Antarctic Collembola Gressittacantha terranova and Friesea grisea. Revue d’Ecologie et de Biologie du Sol 25, 365–372. Davey, M.C., Pickup, J., Block, W., 1992. Temperature variation and its biological significance in fellfield habitats on a maritime Antarctic island. Antarctic Science 4, 383– 388. Greenslade, P., 1995. Collembola from the Scotia Arc and Antarctic Peninsula including descriptions of two new species and notes on biogeography. Polskie Pismo Entomologiczne 64, 305 –319. Harada, T., 1998. To fly or not to fly: response of water striders to drying out of habitat. Ecological Entomology 23, 370– 376. Hayward, S.A.L., Worland, M.R., Bale, J.S., Convey, P., 2000. Temperature and the hygropreference of the Arctic Collembolan Onychiurus arcticus and mite Lauroppia translamellata. Physiological Entomology 25, 266–272. Hayward, S.A.L., Bale, J.S., Worland, M.R., Convey, P., 2001. Influence of temperature on the hygropreference of the Collembolan, Cryptopygus antarcticus, and the mite, Alaskozetes antarcticus from the maritime Antarctic. Journal of Insect Physiology 47, 11 –18. Hertzberg, K., Leinaas, H.P., 1998. Drought stress as a mortality factor in two pairs of sympatric species of Collembola at Spitzbergen, Svalbard. Polar Biology 19, 302–306. Hertzberg, K., Leinaas, H.P., Ims, R.A., 1994. Patterns of abundance and demography: Collembola in a habitat patch gradient. Ecography 17, 349– 359. Holding, A.J., Collins, V.G., French, D.D., D’Sylva, T., Baker, J.H., 1974. Relationship between viable bacterial counts and site characteristics in tundra. In: Holding, A.J., Heal, O.W., Maclean, S.F., Flanagan, P.W. (Eds.), Soil Organisms and Decomposition in Tundra, Swedish IBP Committee, Stockholm, pp. 49 –64. Joosse, E.N.G., 1971. Ecological aspects of aggregation in Collembola. Revue d’Ecologie et de Biologie du Sol 8, 91–97. Joosse, E.N.G., 1981. Ecological strategies and population regulation of Collembola in heterogeneous environments. Pedobiologia 21, 346– 356. Kennedy, A.D., 1993. Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arctic and Alpine Research 25, 308–315. Leinaas, H.P., Fjellberg, A., 1985. Habitat structure and life history strategies of two, partly sympatric and closely related, lichen feeding Collembola species. Oikos 44, 448–458. Lindberg, N., Engtsson, J.B., Persson, T., 2002. Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. Journal of Applied Ecology 39, 924 –936. Lippert, G., 1971. Occurrence of arthropods in mosses at Anvers Island, Antarctic Peninsula. Pacific Insects Monograph 25, 137 –144. Llano, G.A., 1956. Botanical research essential to a knowledge of Antarctica. In: Crary, A.P., Gould, L.M., Hulbert, E.O., Odishaw, H., Smith, W.E. (Eds.), Antarctica in the Geophysical Year
934
S.A.L. Hayward et al. / Soil Biology & Biochemistry 36 (2004) 927–934
(Geophysical Monograph No. 1), American Geophysical Union, Washington, DC, pp. 124– 133. Madge, D.S., 1964. The humidity reactions of Oribatid mites. Acarologia 6, 566– 591. Pickup, J., Rothery, P., 1991. Water-loss and anhydrobiotic survival in nematodes of Antarctic fellfields. Oikos 61, 379–388. Richard, K.J., Convey, P., Block, W., 1994. The terrestrial arthropod fauna of the Byers Peninsular, Livingston Island, South Shetland Islands. Polar Biology 14, 371–379. Ring, R.A., Block, W., Sømme, L., Worland, M.R., 1990. Body water content and desiccation resistance in some arthropods from Subantarctic South Georgia. Polar Biology 10, 581–588. Schenker, R., Block, W., 1986. Micro-arthropod activity in three contrasting terrestrial habitats on Signy Island, maritime Antarctic. British Antarctic Survey Bulletin 71, 31 –43. Scriber, J.M., 1977. Limiting effects of low leaf-water content on the nitrogen utilisation, energy budget and growth of Hyalophora cercropia (Lepidoptera: Saturniidae). Oecologia 28, 269–287. Smith, R.I.L., 1988. Recording bryophyte microclimate in remote and severe environments. In: Glime, J.M., (Ed.), Methods in Bryology, Hattori Botanical Laboratory, Nichinan, pp. 275–284. Testerink, G.J., 1982. Metabolic adaptations to seasonal changes in humidity and temperature in litter-inhabiting springtails. Oikos 40, 234– 340. Tilbrook, P.J., 1967. The terrestrial invertebrate fauna of the maritime Antarctic. Philosophical Transactions of the Royal Society of London B 252, 261–278.
Tilbrook, P.J., Block, W., 1972. Oxygen uptake in an Antarctic collembole, Cryptopygus antarcticus. Oikos 23, 313–317. Usher, M.B., Booth, R.G., 1984. Arthropod communities in a maritime Antarctic moss-turf habitat: three dimensional distribution of mites and Collembola. Journal of Animal Ecology 53, 427–441. Usher, M.B., Booth, R.G., 1986. Arthropod communities in a maritime Antarctic moss-turf habitat: multiple scales of pattern in the mites and collembola. Journal of Animal Ecology 55, 155–170. Usher, M.B., Edwards, M., 1986. The selection of conservation areas in Antarctica: an example using the arthropod fauna of Antarctic islands. Environmental Conservation 13, 115–122. Verhoef, H.A., van Selm, A.J., 1983. Distribution and population dynamics of Collembola in relation to soil moisture. Holarctic Ecology 6, 387 –394. Wallwork, J.A., 1973. Zoogeography of some terrestrial micro-Arthropoda in Antarctica. Biological Reviews 48, 233 –259. Winston, P.W., Bates, D.H., 1960. Saturated solutions for the control of humidity in biological research. Ecology 41, 232 –237. Wise, K.A.J., Shoup, J., 1971. Entomological investigations in Antarctica, 1964–65 season. Pacific Insects Monograph 25, 27–56. Worland, M.R., Block, W., 1986. Survival and water loss in some Antarctic arthropods. Journal of Insect Physiology 32, 579–584. Worland, M.R., Lukesˇova´, A., 2000. The effect of feeding on specific soil algae on the cold-hardiness of two Antarctic micro-arthropods (Alaskozetes antarcticus and Cryptopygus antarcticus). Polar Biology 23, 766–777.