European Journal of Soil Biology 38 (2002) 255−259 www.elsevier.com/locate/ejsobi
Antarctic soil nematode response to artificial climate amelioration Peter Convey *, David D. Wynn-Williams British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK Received 13 August 2000; accepted 30 May 2001
Abstract There is increasing evidence supporting rapid trajectories of environmental change in the Antarctic. This study describes preliminary data on soil faunal responses to artificial environmental amelioration obtained using a ‘greenhouse’ methodology, over the first year of a manipulative study of part of the soil ecosystem of Mars Oasis, Alexander Island in the southern Maritime Antarctic. The methodology, which used two types of UV-absorbing perspex cloche, influences a range of environmental variables, the most significant of which in this study are thought to be temperature and UV-radiation. The fauna of this site is dominated by Nematoda. Responses to amelioration included large increases in nematode population densities, particularly those of the microbivorous genus, Plectus, combined with changes in the relative abundance of taxa. These faunal changes are likely to be mediated via the responses of autotrophs to the environmental manipulations. © 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. Keywords: Antarctic; Climate change; Nematoda; Soil fauna
1. Introduction Within the Antarctic, clear regional warming trends have been demonstrated over the last 30–50 years, particularly along the Antarctic Peninsula and its associated islands [14]. Over the last two decades, the continent has also suffered spring depletion of stratospheric ozone levels [5], allowing greater levels of potentially damaging UV-B radiation to reach terrestrial ecosystems. Antarctic ecosystems are simple, with faunas consisting almost entirely of soil micro-invertebrates [2], including microarthropods, nematodes, tardigrades and rotifers; and floras comprising bryophytes, lichens, algae and cyanobacteria [17]. Biotic diversity decreases along an environmental gradient between the sub-Antarctic islands and continental Antarctica, with nematodes forming an increasingly important element of the terrestrial fauna [1,15,19]. At the extreme, soil communities of the Dry Valley region of continental Antarctica contain only one to three species of
* Corresponding author. Fax: +44-1223-362616. E-mail address:
[email protected] (P. Convey).
Nematoda and at most two trophic levels, and have been identified as probably the simplest faunal assemblages on earth [7,8]. Simple communities such as those of the Dry Valleys are thought to be particularly susceptible to disturbance or change processes [7]. The combination of known regional climatic trends, ozone hole development and simple, sensitive communities makes the Antarctic an important testing ground for identifying the biological consequences of climate change. Despite recognition of this potential, few studies have yet addressed the consequences of change on the Antarctic soil biota [11,23]. We describe here results obtained during the first year of a manipulative study of a sandy soil ecosystem at Mars Oasis (Two Step Cliffs, south-east Alexander Island) in the southern Maritime Antarctic. This simple ecosystem is based on autotrophic microbes (cyanobacteria, algae), with a nematode-dominated fauna. The aim of the study is to monitor over a period of years, changes in the nematode fauna associated with a range of environmental manipulations. This will test the hypothesis that realistic levels of local climate manipulation lead to consistent changes (= responses) in soil faunal communities.
© 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S 1 1 6 4 - 5 5 6 3 ( 0 2 ) 0 1 1 5 5 - X
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Fig. 1. Climatic data obtained at the Mars Oasis study site throughout 1998. Soil surface temperature indicated by solid line, air temperature by dashed line.
2. Methods 2.1. Study site The study utilized passive greenhouses (cloches) placed over the central area of sorted soil polygons at Mars Oasis on 27/11/97 (71°52’40’’S 68°15’57’’W). The site is c. 10–20 m from the southern shore of a shallow, unnamed lake at the foot of Two Step Cliffs, and forms part of a long-term study of the effects of climate manipulation on Antarctic soil microbial flora. Cloches manufactured from two types of perspex have been deployed, ‘VE’ and ‘OX’. Both transmit visible light, with VE additionally transmitting longer wavelengths of UV-A radiation, and OX transmitting UV-A and UV-B [22]. These cloche types also increase ground temperatures by 2.2–3.8 °C [23]. Summary air and soil surface temperatures recorded at the Mars Oasis site throughout 1998 are presented in Fig. 1 2.2. Sample collection and extraction Single soil samples of approximately 5 cm diameter × 5 cm depth (surface area c. 0.002 m2, c. 100–200 g dry mass) were obtained from individual cloches or control sites. Three sets of samples were collected between 18/12/98 and 14/1/99:
(1) 18/12/98, 12 samples from cloches (six each from separate VE and OX) over coarse sandy soil, with a further six bare ground control samples from adjacent (< 1 m) non-manipulated soil polygons. (2) 21/12/98, four samples from cloches (two each from separate VE and OX) over fine waterlogged silt with a further three bare ground controls. (3) 14/1/99, five samples obtained from vegetated ground in a small drainage gully c. 100 m east of the cloche site; these were obtained for comparison after the presence of a thin moss carpet was identified in the cloche samples from (1) which was absent in the bare ground controls (however, the later date of collection may have allowed a natural increase in nematode populations, reducing the comparative value of these samples). Cores were extracted and nematodes preserved following Hooper [9,10]. Soil moisture content was not measured, although all soils collected were visibly damp. After extraction, soils were dried at 60 °C, to express nematode densities kg–1 dry soil. Organic content was determined by ashing soil at 475 °C for 24 h and re-weighing. Larger nematode genera were identified following Maslen [15]. Nematodes from each extraction were counted using a sorting dish under a dissecting microscope at a minimum of × 25 magnification.
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Table 1 Summary nematode density data obtained in extractions of Mars Oasis cloches and associated control samples. To indicate the scale of variability, density range is also presented Treatment (N)
Mean (SE) nematode density (ind. kg–1)
Nematode density range (ind. kg–1)
Soil organic content (%)
Open sandy control (6) Sandy OX (6) Sandy VE (6) Waterlogged control (3) Waterlogged OX (2) Waterlogged VE (2) Vegetated ground (5)
11.9 (4.8) 5366 (3021) 18059 (14315) 89.6 (47.8) 183 (113) 579 (3.2) 3347 (1347)
0–33 779–19679 2110–89600 10–175 70–296 576–582 498–8207
2.55 3.05 2.93 3.27 3.15 2.95 4.56
3. Results Extraction data are given in Table 1. Five nematode taxa were present—the distinctive species Enchodelus signyensis Loof, 1975, the genera Eudorylaimus, Mesodorylaimus and Plectus, plus smaller individuals tentatively identified as Tylenchidae. Nematode densities varied widely between replicates within a treatment, but were greater under both cloche types than in the adjacent bare soil controls (Table 1). These differences were significant between the replicates on sandy soil (Kruskal-Wallis test across all treatments, H = 13.85, P = 0.003; both treatments and vegetated ground significantly greater than bare sandy soil density (MannWhitney U-tests, P < 0.05), but no other significant differences were found. Small sample size led to no significant differences being present between waterlogged soil treatments and controls, although the same density pattern was observed (Kruskal-Wallis H = 3.93, P = 0.14). Although large variability led to no significant treatment differences being found, greatest densities were obtained from VE cloches on both drier sandy and waterlogged soils, with those of the former being 1–2 orders of magnitude greater than the latter. The proportional contribution of the different nematode taxa varied across the treatment, vegetated and bare soil control samples (Table 2). On drier sandy soils, Plectus dominated OX and VE cloche treatments relative to the bare soil control or comparable vegetated soil. Only Plectus and Tylenchidae were present in VE samples, while single individuals of Enchodelus and Eudorylaimus were found in
OX extractions. In contrast, all four taxa contributed significant proportions of the vegetated soil fauna, which also included Mesodorylaimus. Identical taxa were present in control and cloche samples from waterlogged soil (Table 2). The waterlogged soil cloche samples also showed an increase in population densities and a change in the abundance of taxa relative to the controls, with Mesodorylaimus and/or smaller tylenchids being better represented.
4. Discussion Representatives of Plectus, Eudorylaimus and Mesodorylaimus have been recorded previously from a single site on Alexander Island (Ablation Valley, c. 100 km north of the present study site) although the taxonomic status of some of these is yet to be confirmed. The presence of the maritime Antarctic species Enchodelus signyensis increases the recorded nematode diversity of Alexander Island. The low species richness found is typical of studies of the southern Maritime Antarctic [15,19], while the communities of bare soils at Mars Oasis are only slightly richer in terms of species number and population density, than the extreme communities of continental Dry Valley desert soils (cf. [6,7]). Nematode density in naturally vegetated sandy soils of Mars Oasis was considerably greater than that of bare soil, equating to approximately 1.5 × 105 ind. m–2, although there was no associated increase in species richness. This density is at the lower end of ranges found in studies of the
Table 2 Proportional contributions (%) of different nematode taxa found in extractions of soil cores from each cloche type and associated control samples Taxon
Open sandy control
Plectus 83.3 Eudorylaimus 8.3 Mesodorylaimus 0 Enchodelus 0 Other 8.3
Sandy OX
Sandy VE
Waterlogged control
Waterlogged OX
Waterlogged VE
Vegetated ground
95.6 0.02 0 0.02 4.4
97.5 0 0 0 2.5
47.7 2.3 27.3 0 22.7
14.3 14.3 5.7 0 65.7
50.4 0.7 23 0 25.9
63.2 7.3 0.2 5.8 23.6
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nematode faunas of soils associated with various vegetation types at Signy Island, in the northern Maritime Antarctic [3,16,20,21]. Large increases in nematode density relative to bare soil controls were observed in samples obtained from within both cloche types at Mars Oasis (Table 1). This effect was most pronounced in VE cloches, although not significantly greater than OX cloches or vegetated soil samples. Comparison of the taxa found in bare ground control samples and cloches over sandy soil with those of naturally vegetated ground indicate that the population increases resulted from multiplication of the fauna present on a local scale. Although the two sites are separated by only 50–100 m, there was no evidence of colonization of cloches by omnivorous Enchodelus, Eudorylaimus and Mesodorylaimus from the neighbouring vegetated site. Instead, population increases involved predominantly, the microbivorous genus Plectus. Plectus antarcticus has the potential for rapid population increases, with completion of the life cycle possible in 43 days at 10 °C in laboratory culture, and individual fecundity > 200 eggs [4]. Similar information is not available for the other taxa found in this study. Nevertheless, the population increases observed here have been achieved in a period of just over one year, including the majority of two short summer seasons. Throughout this period soil temperatures at the Mars Oasis site, even within cloches, will have been positive for three to four months, but typically below c. 5 °C (Fig. 1). Passive greenhouse manipulation experiments are difficult to interpret, changing both physical (e.g. temperature, wind, hydration, UV) and biological (e.g. plant colonization, substrate stabilisation) factors concurrently, often in detail not providing a close analogue of the changes predicted by climate models [12,13]. The methodology in use at Mars Oasis alters a suite of inter-related environmental factors, with the overall effect of providing a more favourable microclimate for biological activity (WynnWilliams [22] lists 13 factors). The two most important variables altered here are likely to be temperature and exposure to wavelengths of UV radiation. The few other studies of the consequences of local microclimate amelioration on Antarctic soil flora and fauna have given analogous results. Large increases have been recorded, over periods of three and six years, in microalgal (predominantly cyanobacterial) colonization of the soil surface in cloches on Signy Island [23]. Preliminary results indicate that similar microbial development occurs at Mars Oasis in as little as two years (Wynn-Williams, unpublished), resulting from the greater insolation experienced at this more southerly site. Similar large increases were found in soil microarthropod populations at the same Signy Island site over an eight-year period [11], while Smith [18] provided a spectacular illustration of rapid development of a lush bryophyte carpet within a cloche at a site with no visible adjacent bryophytes.
Examination of the soil cores obtained within both types of cloche at Mars Oasis revealed the presence of a thin and largely buried bryophyte carpet, not present in adjacent controls. The increase in soil flora (both microalgae and bryophytes) under cloches at Mars Oasis will provide resources required by heterotrophs, and is likely to form the proximate cause underlying faunal population increases (cf. [11]).
Acknowledgements We thank Andrew Rosaak and Paul Geissler for collection of soil samples from Mars Oasis and the British Antarctic Survey Air Unit, Rothera Field Operations Manager (Tudor Morgan) and Field General Assistants (Rachel Duncan, Martin Cooper) for their support of the fieldwork. Paul Geissler is also thanked for plotting Fig. 1. Dr Philip Pugh and two anonymous referees have provided helpful comments in the development of this paper.
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