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Low-diversity Antarctic soil nematode communities: distribution and response to disturbance.

INTRODUCTION

The biodiversity of soil is estimated to be in the thousands of species/[m.sup.2] in the majority of ecosystems (Groombridge 1992). Because most of these organisms are undescribed, it is difficult to determine the impact of disturbance on soil biodiversity and its associated effects on ecosystem function (Verhoef and Brussaard 1990). Nematodes are dominant soil microfauna in all terrestrial ecosystems, but their biodiversity and the ecological and edaphic factors controlling their distribution and populations are poorly known even for intensively studied agricultural and forest systems (Bernard 1992, Handel 1993). Much of our knowledge about nematodes and ecosystem processes is derived from microcosm experiments (Ingham et al. 1985) and controlled-environment studies (Dyer et al. 1993). These studies show that nematodes perform numerous functions within multiple trophic levels in soil food webs and are important to carbon and nutrient cycling and trace-gas flux. For example, microcosm experiments show that increasing the complexity with three levels of organisms, a predaceous nematode species, a microbivorous nematode species, and bacteria, results in increased nitrogen mineralization and respiration (Allen-Morley and Coleman 1989, Bouwman et al. 1994). However, the taxonomic complexities of soil biota have not allowed species-level experiments to be tested in the field. Studies of naturally occurring low-diversity nematode communities should provide an important link between these simple experimental systems and the overwhelming species complexity of most ecosystems. Additionally, study of limited-diversity soil communities in extreme environments can contribute insights to complex relationships among diversity, stability, and productivity, as well as contributing to knowledge about the environmental factors determining the length of food chains (Moore et al. 1996).

Low-diversity soil communities are expected only in very extreme environments where productivity is low and water and nutrients are limiting (Procter 1984). The ice-free Dry Valleys of Southern Victoria Land ([approximately equal to]4000 [km.sup.2] in area; 78 [degrees] S, 164 [degrees] E), are extreme desert ecosystems with low precipitation and soil-water availability (annual average of 45 mm water equivalent), extremely low air temperatures (average -20 [degrees] C), and high winds (Weller et al. 1983, Vincent 1988, Wynn-Williams 1990). Antarctic soils are similar to those in other deserts and are poorly developed, coarsely textured, have low organic matter, alkaline pH, low soil moistures and high concentrations of soluble salts (Campbell and Claridge 1987).

In warm desert systems, nematode distribution and diversity are related to plant distribution and organic matter accumulation (Freckman and Virginia 1989). Surprisingly, nematode distribution and diversity are not related to soil moisture status in arid grasslands (Ingham et al. 1982) and warm deserts (Freckman and Virginia 1989) even though nematodes require water films for their activity. This paradox may be explained in that nematodes can survive extreme desiccation and freezing by entering into anhydrobiosis and cryobiosis (Pickup and Rothery 1991, Wharton and Block 1993) and may live in microsites in the soil where moisture and water-vapor movement is sufficient for activity, but difficult to measure (Freckman and Virginia 1989). Whether the extreme low moisture and productivity of polar deserts limit nematode distribution and diversity in Antarctic soils is unknown.

The biomass and metabolic activity of the ahumic Dry Valley soils are considered the lowest of any soil ecosystem, and environmental constraints are at the limits to life for many groups of organisms (Friedmann 1993). The most complex Antarctic soil communities contain mosses, lichens, blue-green and green algae, microflora, and microscopic invertebrates such as protozoa, rotifers, tardigrades, nematodes, collembola, and mites, and are restricted to small areas of moist habitats near glaciers, or along moat edges of frozen lakes or streams, and snowmelt depressions. It has been suggested that nematodes, which require water for activity, would be limited to these moist habitats (Wharton and Brown 1989, Kennedy 1993). The remaining, vast dry-soil habitats not supplied by melt streams appear uninhabitable (Vishniac 1993) and their nematode communities have been largely ignored.

In some ecosystems the structure of nematode communities at the family taxonomic level has been suggested as a reliable predictor of anthropogenic disturbance (Freckman and Ettema 1993). Antarctic terrestrial ecosystems are expected to experience increased stress from global environmental change (increased UV-B and temperature) and direct human impacts from tourism and other activities (Lewis-Smith 1994, Weiler and Penhale 1994). Scientists are looking at possible biological and physical indicators of these effects through the United States National Science Foundation's Long-Term Ecological Research Program in the McMurdo Dry Valleys.

Our objectives were to determine if: (1) the factors limiting distribution and diversity of soil nematode communities were similar to other deserts; and, (2) whether the soil nematode communities were sensitive to changes in temperature, moisture, and carbon availability and thus could act as indicators of environmental change for the Dry Valleys.

METHODS

We sampled a total of 130 moist and dry soil habitats in three Dry Valleys [Garwood Valley (78 [degrees] 02[minutes] S, 164 [degrees] 10[minutes] E) (n = 35), Taylor Valley (77 [degrees] 37 [minutes] S, 163 [degrees] 11[minutes] E) (n = 57), and Wright Valley (77 [degrees] 31[minutes] S, 161 [degrees] 50[minutes] E) (n = 38)], defined by geomorphologic features: (1) dry polygons (sorted and non-sorted), (2) other dry-soil, large expanses of unstructured xeric soils (soil moisture [less than]5%), and (3) moist habitats supplied by glacier meltwater (soil moisture [greater than]5%).

We tested whether Dry Valley nematode communities are sensitive to changes in the soil environment by instituting a 1-yr field experiment manipulating soil moisture, carbon, and temperature at a site in Taylor Valley, Antarctica, where the microbivore Scottnema lindsayae and omnivore-predator Eudorylaimus antarcticus co-occurred. The third nematode species, the microbivore Plectus antarcticus does not occur at this field site, but occurs elsewhere in the Dry Valleys. Moisture, carbon, and temperature are environmental factors that are likely to be changed with human intervention and disturbance, and which could impose constraints on the productivity of the soil-nematode community. The experiment (randomized block, five replicates per treatment), compared nematodes in control plots (no manipulations) to five manipulations of soil conditions: increased water content (W), soil carbon (C), and soil temperature (T). Plot size was 0.5 [m.sup.2] with the center of the plot used for treatment and sampling. The treatments were (1) (W): NANOpure water (Barnsteed/Thermodyne, Dubuque, Iowa, USA) added to field capacity to 10 cm depth (5 L per plot); (2) (W + C): carbon (sucrose) in 5-L solution (0.1 mol/L per plot), which provides the same moisture level as (W); (3) (T): closed, clear polycarbonate chambers (32.5 x 53.0 x 15.0 cm), similar to those used in Signy Island, Antarctica (see Wynn-Williams 1994), positioned on the soil to increase soil temperature; (4) (W + T); (5) (W + T + C). Soil was sampled to 10 cm depth prior to treatment and 1 yr later in late austral summer (January). Soil temperatures were measured at 10 cm depth prior to sampling.

Samples were collected with NASCO pre-sterilized plastic scoops and placed in sterile polyethylene Whirl-Pak bags (Freckman and Virginia 1993). All soils were kept in insulated coolers while in transit to the McMurdo Station laboratory facilities, where they were immediately placed into temporary storage at 1 [degrees] C. Nematodes, tardigrades, and rotifers were extracted from the soils within 48 h using standard sugar centrifugation procedures, modified to keep the soils and all extraction materials at a constant cold temperature (Freckman and Virginia 1993). Extracted nematodes were identified to genus. All nematode counts were adjusted for soil moisture to give number of nematodes per kilogram of dry soil. Nematode numbers were transformed to log (x + 1) for statistical analysis.

The soil moisture content of each sample was determined gravimetrically (mass of water per unit soil mass) at the time of nematode extraction. Soil-saturation extracts were prepared and pH of the saturated paste was measured using a glass electrode. Cations in the saturation extracts were determined by inductively coupled plasma atomic emission spectroscopy, and total salinity (electrical conductivity) was measured using a conductivity meter. Soil [N[O.sub.3].sup.-] and [N[H.sub.4].sup.+] were determined from extractions with 2 mol/L KCl solution and [P[O.sub.4].sup.3-] from extractions with 1 mol/L NaHC[O.sub.3] solution using an automated ion analyzer (Technicon Autoanalyzer, Technicon Instruments, Tarrytown, New York, USA). Soil organic C was determined by wet [TABULAR DATA FOR TABLE 1 OMITTED] oxidation, and total N by Kjeldahl digestion procedures followed by determination of [N[H.sub.4].sup.+] as above (see Virginia et al. 1992 for methods for all soil analyses).

RESULTS AND DISCUSSION

Soil fauna such as mites and collembola were not found in any of the soils, and tardigrades and rotifers were found in only 14% of the soil sites and were associated with higher soil moistures. Nematodes occurred in each valley and were recovered from 62% of the samples (Table 1). The absence of living and dead nematodes in one third of the samples is a unique finding, [TABULAR DATA FOR TABLE 2 OMITTED] since nematodes are ubiquitous on earth. As in warm deserts, nematode abundance was not correlated with moisture for all samples (r = 0.059, n = 130). Neither was soil moisture a primary variable in multiple-regression equations relating soil properties to nematode abundance (Table 2). These results suggest that moisture is not the primary limiting factor for nematodes in the Dry Valleys and that other soil factors and climate may account for the heterogeneous nematode distribution across Dry Valley landscapes. Analysis of variance and Fischer's protected least-significant difference (PLSD) test showed significant variation in nematode density by habitat type (df = 2; F = 7.097; P = 0.0012) and in soil moisture by habitat type (df = 2; F = 88.189; P [less than] 0.0001; [ILLUSTRATION FOR FIGURE 1 OMITTED]). Nematode densities were higher in dry soils and significantly higher (by a factor of three) in the dry polygon habitat as compared to moist habitats. That nematodes dominated in the drier soil habitats suggests they are well adapted to the physiological stresses resulting from low moisture and the desiccation associated with soil freeze-and-thaw cycles. In fact, excessively moist soils along melt streams and near lakes appear to be less suitable habitats. Although mean Dry Valley nematode densities were much lower than in higher productivity ecosystems, peak densities were comparable to warm desert ecosystems (Freckman and Mankau 1986, Freckman and Virginia 1989). Our results from this geographic soil-habitat survey of an extreme environment [TABULAR DATA FOR TABLE 3 OMITTED] indicate that nematodes are the most abundant complex invertebrate in the Dry Valley soils.

We questioned why nematodes had not established in all soils of the Dry Valleys, if moisture was not the limiting factor. This finding suggests that either nematodes had not dispersed to these locations (unlikely since nematodes occur in the same valleys on different soils) or the soil habitat sampled was unsuitable for community establishment. Nematodes were absent in soils with high inorganic ion accumulation, indicating salinity may limit biotic activity in these soils (Table 1). For soil samples with nematodes, electrical conductivity was associated with Scottnema abundance (Table 2). Although the electrical conductivities of the Dry Valley soils are similar to other arid systems where nematodes survive, the osmotic concentration of the soil solution surrounding nematodes is likely to periodically reach very high levels as the soils dry or begin to freeze. For this reason soil ion concentrations may be a significant factor in biological activity in Antarctic soils (Campbell and Claridge 1987).

In more productive desert ecosystems supporting higher plants, the abundance and diversity of nematodes is correlated with organic C and N, and their spatial distribution is closely tied to that of plants (Robertson and Freckman 1995). The organic C content of the Dry Valley soils was extremely low (0.08%) even when compared with highly desertified warm-desert soils in New Mexico where organic C values are 3-25 times higher (Virginia et al. 1992). In the Dry Valleys the sources of C to the soil ecosystem are poorly understood, and information on rates and spatial patterns of productivity in the Dry Valley soils is presently not available to link this aspect of the carbon cycle to nematode distribution and function. We did not find a relationship (i.e., a significant difference between soils containing and those lacking nematodes, Table 1) between nematode presence and soil properties associated with organic-matter accumulation and decomposition (organic C, total N, P, inorganic N). For soils with nematodes, relationships between soil properties and abundance were weak, with [R.sup.2] values [less than]0.4 for multiple-regression equations (Table 2). It is interesting however, that the three taxa had different groups of soil variables associated with their numbers in soil. Scottnema lindsayae was best related to soil salinity factors (pH and EC), Plectus antarcticus to N and P, and Eudorylaimus antarcticus, to moisture and organic C. A much more extensive survey would be required to determine if Dry Valley nematodes segregated by soil variables.

A number of studies suggest that biodiversity is related to ecosystem stability and promotes resistance to [TABULAR DATA FOR TABLE 4 OMITTED] disturbance (Vitousek and Hooper 1993, Naeem et al. 1994, Tilman and Downing 1994). Alternatively, if diverse systems have many species performing the same function, species redundancies may protect ecosystem function even if diversity declines. In temperate ecosystems, soil nematode species richness and potential redundancy is high, with [greater than]75 nematode species within four to five functional (ecosystem) groups (Table 3). Microbivorous (including the bacterivorous) nematodes are usually the dominant functional taxa. Besides nematodes, there are many additional phyla of invertebrates with a rich species diversity that may perform similar tasks or functions as nematodes do in the soil food web (Moore et al. 1993). In contrast, the extreme dry-soil environments of the Dry Valleys we sampled have unusually simple communities with nematodes as the primary higher invertebrate [ILLUSTRATION FOR FIGURE 2 OMITTED]. Ninety percent of the soils (n = 86) we sampled had only one or two species, and rarely a maximum of three species. One species, S. lindsayae, dominated all nematode communities. Soil moisture did not differ significantly across any of the nematode species communities (P [less than] 0.05). These communities supported only two nematode functional groups, the two microbivorous species S. lindsayae and P. antarcticus (Overhoff et al. 1993), and the omnivore-predator, E. antarcticus (Yeates et al. 1993). In most Dry Valley soils it is not unusual to find a single nematode species occupying a single trophic level. This places these communities with one-link food webs (microbes grazed upon by microbivorous nematodes) among the simplest soil food webs on earth (de Ruiter et al. 1995). The unusually low diversity and low redundancy of the Dry Valley soils suggest that these systems will be highly disrupted by the loss or decline of even a single species that is sensitive to environmental change.

The two nematodes found at the field-experiment site responded differently to the manipulations of soil resources and climate (Table 4). Paired comparisons indicate that Scottnema and Eudorylaimus have a significantly different pattern in population change in plots where soils have been manipulated (df = 24, t = 3.45, P = 0.0014) in comparison to the control (df = 4, t = 0.19, P = 0.8610). The density of the rarer omnivore-predator species, E. antarcticus, declined in response to changes in the soil environment, while the more abundant and possibly prey nematode species, S. lindsayae, generally increased. This could be due to (1) a direct effect of the treatments altering the soil environment and perhaps increasing the microbial food source for S. lindsayae, and/or (2) an indirect effect of the reduction of the predator, allowing the prey species to increase in numbers. Similar population increases of prey have been observed when predators are removed from other systems (Carpenter and Kitchell 1993). The largest effect for either species occurred for the treatment combination where soil temperature, moisture, and carbon were all increased. Mean soil temperature (0-10 cm depth) at time of sampling 1 yr after treatment, was 14.7 [degrees] C inside the temperature chambers and 10 [degrees] C outside the chambers (n = 15). These field results show that disturbances that alter soil resources and soil climate can have an impact on individual species within soil communities, resulting in changes in the soil food webs and community structure. The results from our field experiment suggest that nematodes may be a useful indicator organism for detecting change in the Dry Valley soil system. We suggest that the low-diversity soil systems of the Dry Valleys are sensitive to anthropogenic disturbance.

ACKNOWLEDGMENTS

We thank D. P. Coffin, M. Ho, R. K. Niles, L. E. Powers, T. R. Seastedt, D. R. Strong, and D. Tilman for helpful comments on the manuscript, and the USA NSFA VXE-6 for helicopter support. This research was supported by NSF grant DPP 8818049 to D. W. Freckman and R. A. Virginia and is a contribution to the McMurdo Dry Valley LTER program.

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Author:Freckman, Diana W.; Virginia, Ross A.
Publication:Ecology
Date:Mar 1, 1997
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