The Society for Integrative and Comparative Biology
Soil Nematodes and Desiccation Survival in the Extreme Arid Environment of the Antarctic Dry Valleys1
1 Department of Biology, University of Richmond, Richmond, Virginia 23173
2 Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, Colorado 80523
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 SYNOPSIS INTRODUCTIONNEMATODE ANHYDROBIOSIS IN DRY...ANHYDROBIOSIS AND NEMATODE...References |
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Soil nematodes are capable of employing an anhydrobiotic survival strategy in response to adverse environmental conditions. The McMurdo Dry Valleys of Antarctica represent a unique environment for the study of anhydrobiosis because extremes of cold, salinity, and aridity combine to limit biological water availability. We studied nematode anhydrobiosis in Taylor Valley, Antarctica, using natural variation in soil properties. The coiled morphology of nematodes extracted from dry valley soils suggests that they employ anhydrobiosis, and these coiled nematodes showed enhanced revival when re-hydrated in water as compared to vermiform nematodes. Nematode coiling was correlated with soil moisture content, salinity, and water potential. In the driest soils studied (gravimetric water content <2%), 20–80% of nematodes were coiled. Soil water potential measurements also showed a high degree of variability. These measurements reflect microsite variation in soil properties that occurs at the scale of the nematode. We studied nematode anhydrobiosis during the austral summer, and found that the proportion of nematodes coiled can vary diurnally, with more nematodes vermiform and presumably active at the warmest time of day. However, dry valley nematodes uncoiled rapidly in response to soil wetting from snowmelt, and most nematode activity in the Dry Valleys may be confined to periods following rare snowfall and melting events. Anhydrobiosis represents an important temporal component of a dry valley nematode's life span. The ability to utilize anhydrobiosis plays a significant role in the widespread distribution and success of these organisms in the Antarctic Dry Valleys and beyond.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONNEMATODE ANHYDROBIOSIS IN DRY...ANHYDROBIOSIS AND NEMATODE...References |
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Nematodes are ubiquitous residents of soils and sediments in most ecosystems. These microscopic roundworms are widely distributed even in extreme environments where water availability is limited (Freckman and Mankau, 1977
; Treonis et al., 1999; Wall and Virginia, 1999; Porazinska et al., 2002). Some soil nematode species feed on bacteria or fungi, while others are omnivorous, predaceous, or parasites of plant roots (Yeates et al., 1993). Nematodes play important roles in belowground carbon and nutrient cycling and influence ecosystem functions such as plant growth and decomposition (Freckman, 1988; Wardle et al., 2004). Soil nematodes range in size from 0.3–3 mm and are active in water-filled pores in the soil matrix and in water films that coat soil particles. Due to their small size and inability to migrate over long distances, soil nematodes are closely dependent on the immediate environmental conditions in soil pores to feed and reproduce. However, the soil environment is heterogeneous, both temporally and spatially, and nematodes must adapt to these changing conditions in order to survive.
Nematode anhydrobiosis
Survival strategies enable nematodes to persist in soils where their activity may be limited for long periods by temperature extremes and/or desiccation (Freckman and Womersley, 1983; Wharton, 1995). Nematode survival strategies encompass a gradient of responses from quiescence to cryptobiosis (Keilin, 1959; Cooper and VanGundy, 1971; Demeure et al., 1979b; Wharton 1986). These two states are distinguished primarily upon the degree to which activity ceases, with quiescence indicated by cessation of activity (feeding, reproduction) and cryptobiosis or "latent" life typically defined by an absence of motility and metabolism (Keilin, 1959; Clegg, 2001). Nematode survival strategies have further been characterized based on the environmental stress to which the organism is responding (e.g., cryobiosis, anhydrobiosis, osmobiosis, aerobiosis) (Keilin, 1959; Clegg, 2001). Anhydrobiosis or "life without water" (Giard, 1894) has been studied extensively and is the inactive state employed in response to desiccation (Keilin, 1959; Cooper and VanGundy, 1971; Crowe et al., 1992). The ability to use anhydrobiosis is found among taxonomically diverse organisms including mosses, lichens, bacteria, yeasts, protozoa, nematodes, rotifers, tardigrades, some arthropods, "resurrection" plants, and the seeds of some higher plants.
An increasing degree of desiccation tolerance is afforded to organisms as they progress from quiescence to cryptobiotic anhydrobiosis. At the extreme end of the continuum, anhydrobiosis is characterized by a radical loss of body water (greater than 99% in some cases) and a cessation of metabolic activity that is reversed by re-hydration (Crowe et al., 1992). Anhydrobiotic nematodes, rotifers, and tardigrades can revive following exposure to 0% relative humidity (Crowe and Madin, 1975; Higa and Womersley, 1993; Wharton and Barclay, 1993) and freezing temperatures (Tsai and VanGundy, 1989; Pickup and Rothery, 1991; Forge and MacGuidwin, 1992; Wharton et al., 2003). Anhydrobiotic nematodes are known to survive in this state 30 years or more (Wharton, 1986; Womersley et al., 1998). Nematodes extracted from dry soils generally regain motility within minutes to hours (Fig. 1). Laboratory studies of nematodes and other organisms indicate anhydrobiosis typically is accompanied by the production of large quantities of non-reducing sugars, such as trehalose, which stabilize molecules (proteins, membrane lipids) within the cells of anhydrobiotes (Higa and Womersley, 1993; Womersley and Higa, 1998; Crowe and Crowe, 1999; Crowe, 2002). Recent research suggests anhydrobiotes synthesize many other compounds (primarily proteins) that are essential to survival (Solomon et al., 2000; Browne et al., 2002; Oliver et al., 2002; Tunnacliffe and Lapinski, 2003), and our understanding of this complex process is increasing. Several reviews of the physiology and biochemistry of desiccation survival and anhydrobiosis in nematodes have been published (Wharton, 1986; Perry 1999; Barrett, 1991; Crowe et al., 1992; Womersley et al., 1998, Perry, 1999).
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Nematode anhydrobiosis in soils
Many laboratories have studied induction and emergence from anhydrobiosis in nematodes and other invertebrates. However, less research has addressed the role anhydrobiosis plays in the biology and ecology of nematodes in their natural habitat, e.g., in soil. The main obstacle to studies of anhydrobiosis in soil is that the nematodes are not directly observable and must be extracted from the soil for microscopic observation. All nematode extraction techniques utilize water and potentially re-hydrate any anhydrobiotic nematodes.
Whether or not nematodes utilized an anhydrobiotic survival strategy while in the soil was unknown until the work of Freckman and colleagues (Freckman et al., 1975; Demeure et al., 1979a; Freckman and Mankau, 1986). Laboratory studies showed nematodes coiled their vermiform bodies in response to desiccation and as they entered into the anhydrobiotic state (Crowe and Madin, 1974; Freckman et al., 1977; Townshend, 1984; Freckman and Mankau, 1986; Freckman et al., 1987; Womersley and Ching, 1989). Coiling reduces the surface area of the nematode cuticle that is exposed to the environment and slows drying (Womersley et al., 1998). Using soils from the Mojave Desert, Freckman et al. (1975) observed coiled nematodes in solution immediately (<1 hr) after extraction using a density centrifugation technique. Based on this observation, Freckman et al. (1977) developed a technique that replaced water with high molarity (2 M and 1.25 M) sucrose solutions to prevent nematode uncoiling. Freckman et al. (1977) reported coiled nematodes extracted with this technique represented diverse taxa and life stages, and suggested that anhydrobiosis is a widespread survival strategy among soil nematodes.
Coiled nematodes are easily distinguished with low power microscopy from vermiform (uncoiled) nematodes. Studies of soil nematodes consistently show that as soils dry, the proportion of coiled nematodes increases (Table 1). Therefore, nematode coiling is a good indicator of the use of anhydrobiosis and is particularly useful for comparison studies of nematode activity and survival in soils across landscapes and temporal scales, and between ecosystems. We studied soil nematode anhydrobiosis in Taylor Valley, Antarctica (site of the NSF McMurdo Dry Valleys Long Term Ecological Research program) to understand the role this survival strategy plays in nematode ecology and soil processes. Nematodes are the most abundant animal in the Dry Valleys, despite severe temperature and moisture limitations, as well as low soil organic content and high salinity. We define anhydrobiosis as inactivity of the nematode (as indicated by coiled morphology) occurring in response to desiccation of the soil habitat.
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NEMATODE ANHYDROBIOSIS IN DRY VALLEY SOILS |
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SYNOPSISINTRODUCTIONNEMATODE ANHYDROBIOSIS IN DRY...ANHYDROBIOSIS AND NEMATODE...References |
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Study site
The McMurdo Dry Valleys of Antarctica (77°S 163°E; Fig. 2) are the coldest and driest terrestrial ecosystem on Earth (Priscu, 1998
). Over 98% of Antarctica is covered with snow and ice. Extensive areas of ice-free ground occur only in the coastal areas of the continent, primarily in the Dry Valleys. Landscape features of these valleys include glaciers, glacial meltponds and streams, closed-basin lakes, and large expanses of barren, rocky soils. Gradients of temperature and desiccation are found within this ecosystem along many axes (e.g., elevation, soil depth, distance from lakes or streams, seasonally, and diurnally) presenting an ideal environment to investigate the impacts of these factors on nematode biology and ecosystem function.
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Dry valley soils generally are ahumic, coarse, poorly weathered, and desiccated (Bockheim, 1997
; Campbell et al., 1998). Soil chemical and physical properties vary across the landscape as a function of topography, microclimate, and the paleohistory of the valleys (Freckman and Virginia, 1997; Campbell et al., 1998; Powers et al., 1998; Wall and Virginia, 1999; Burkins et al., 2000; Barrett et al., 2004). Dry valley soils are saline due to lack of precipitation and accumulation of salts via weathering and atmospheric deposition (Bockheim, 1997). Annual precipitation, in the form of snow, is less than 10 cm water equivalent but most snowfall sublimates quickly in the austral summer (Fountain et al., 1999; Doran et al., 2002). The primary source of water in the ecosystem is glacial melt, although some soils receive moisture pulses from melting snowdrifts or snowfall (Campbell et al., 1997a; Treonis et al., 2000; Gooseff et al., 2003). Soil moisture content ranges from 5% (by weight) in coastal areas to <1% further inland, although soils saturated by seasonal glacial or lake melting may be even wetter (Campbell et al., 1997a). Soil moisture contents at or near 0% are routinely measured (Treonis and Wall, personal observations). Mean annual temperature in the Dry Valleys ranges from –14.8°C to –30.0°C, but maximum air temperatures can reach as high as 10.0°C in the summer (Doran et al., 2002). Since soils are dark and non-vegetated and day length is 24 hr during the austral summer, soil temperature is often higher than air temperature (Campbell et al., 1997b; Treonis et al., 2000).
Dry valley soil organic content is very low (<1% by weight) due to the lack of vascular plants (Freckman and Virginia, 1997; Campbell et al., 1998; Burkins et al., 2000, 2001). Until recently, the source of carbon and energy to sustain soil food webs was cryptic. Studies of soil organic matter in Taylor Valley, Antarctica indicate that the small amount of material present today is a relic from a warmer climate period when the closed-basin lakes presently found on the valley floor were much larger (Moorehead et al., 1999; Burkins et al., 2000; Lawson et al., 2004). When those lakes receded (most recently, 1,500–1,000 ybp), the biomass (i.e., microbial mats) present in their benthic sediments was left behind to decompose slowly. This legacy organic material may be supplemented by contemporary productivity from algae or cyanobacteria, either in situ or from an allochthonous source (wind-distributed from lakes or streams) (Barrett et al., 2005).
Simple communities of invertebrates exist in many dry valley soils (Powers et al., 1995; Freckman and Virginia, 1997; Treonis et al., 1999; Porazinska et al., 2002). Invertebrate diversity is low, but species of tardigrades, rotifers, collembola, and mites can be found (Strandtmann, 1967; Stevens and Hogg, 2002; Porazinska et al., 2004). The distribution of many species is restricted to soils and sediments associated with streams, lakes, glacial meltponds, and cryoconite holes (meltponds on the surface of glaciers) (Treonis et al., 1999; Moorhead et al., 2003; Porazinska et al., 2004). Visible colonies of moss, algae, and cyanobacteria occur in these wet areas (McKnight et al., 1999). Nematodes have the widest distribution and highest diversity of the invertebrates in the Dry Valleys (Fountain et al., 1999; Treonis et al., 2000), with four species: Scottnema lindsayae, Eudorylaimus antarcticus, Plectus sp., and Geomonhystera antarcticola (Timm, 1971; Wharton and Brown, 1989; Freckman and Virginia, 1991). Scottnema lindsayae Timm (Nematoda: Cephalobidae) dominates invertebrate communities and frequently is the sole species in dry valley soils with lower organic carbon and moisture (Treonis et al., 1999; Porazinska et al., 2002). This nematode is a microbial feeder (bacteria, yeast) endemic to the Dry Valleys. Although the organic content of soils is minimal and productivity perhaps negligible, decomposition rates are also very slow, suggesting that the activity of the soil decomposer food web is limited in dry valley soils (Treonis et al., 2002).
Methods
First, to determine the relationship between nematode coiling and survival, we compared the revival abilities of coiled versus vermiform nematodes in the laboratory. Soil samples were collected from two field sites near Lake Hoare, Taylor Valley (Fig. 2). After counting and within 4 hr of extraction with sucrose solutions, coiled and vermiform nematodes were individually transferred from sucrose solution into tap water and revival (based on movement) was determined within 24 hr.
Second, in order to elucidate the relationship between nematode coiling and soil physiochemical properties, we initiated a survey of soils across Taylor Valley. We studied nematode coiling in relation to soil moisture, electrical conductivity (EC, as a proxy for salinity), and water potential. Water potential is a soil property that reflects the availability of water for biological use by plants and soil organisms. Water potential is a function of the overall soil moisture content and is influenced by soil salinity (osmotic potential) and structure and texture (matric potential). Sixty-seven soil samples that contained nematodes were collected from three sites in Taylor Valley during the austral summer (December–January) (Fig. 2).
Finally, in order to determine how dry valley nematodes respond to changes in their environment, we studied nematode anhydrobiosis in soils over diurnal cycles and in response to a natural moisture pulse. Soil temperature varies widely during the austral summer (Dana et al., 1998; Treonis et al., 2000). Although the sun does not set, it does move behind mountain peaks, shadowing Taylor Valley (Dana et al., 1998). Soils were collected (every 6 hr over 24 hr) on both a sunny and a cloudy day during December from plots on the south side of Lake Hoare in Taylor Valley (Fig. 2). Soil moisture content and temperature were recorded for each sampling point and compared to the proportion of nematodes coiled in samples. Soil moisture changes quickly following rare precipitation events in the Dry Valleys. To study the response of nematodes to soil wetting, we sampled soils near Lake Hoare (Fig. 2) 24 hr after a rare 0.5 cm water equivalent January snowfall event. On this day, sunny conditions immediately followed the snowfall, causing snowmelt.
Soil samples from field sites were collected (0–10 cm depth) in polyethylene bags (Freckman and Virginia, 1993). Soil samples (100 ml) for extraction of anhydrobiotic nematodes were immediately "preserved" in the field by transferring soils to bottles containing 300 ml 1.25 M sucrose. This step prevented changes in the anhydrobiotic state of the nematodes following collection. Within 48 hr, nematodes were extracted using a density centrifugation technique with high molarity sucrose solutions (Freckman et al., 1977). Extracted nematodes were observed with a compound microscope (25–50x) and classified as coiled or vermiform. Most samples contained a mixture of the two, representing micro-site heterogeneity in nematode status and/or the presence of active or dead individuals. We considered a nematode to be coiled when one end of the body curled around to touch or overlap with the inside of the body. Separately, nematodes were also extracted directly from soils (100 g) with water in order to assess the species composition and viability (based on movement) of nematodes in the sample (Freckman and Virginia, 1993). Soil moisture content was determined gravimetrically, and EC was measured for a 1:5 soil slurry using a conductivity meter (YSI, Inc., Yellow Springs, Ohio). Soil water potential (MPa) was measured using a thermocouple psychrometer (Model SC10X, Decagon Devices, Inc., Pullman, Washington).
Results and discussion: nematode coiling and survival
Ninety-five percent of the nematodes extracted from these samples were identified as S. lindsayae. Samples were placed into three categories based on the proportion of coiled nematodes that they contained (<15%, 15–85%, or >85%). All soils had a gravimetric moisture content of <2.5%, but we failed to detect a statistical relationship between soil properties (moisture and salinity) and nematode coiling. The proportion of coiled nematodes that revived in water after extracting with sucrose solutions was similar between the categories, ranging from 50–63% (Fig. 3), although reduced slightly as compared to extraction with water (71% alive). Although some coiled nematodes did not regain movement, they did re-hydrate and uncoil in water. These nematodes were assumed to have been dead in the soils prior to extraction or due to the physical and osmotic stress of extraction and revival.
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In most soils, a smaller proportion of the vermiform nematodes regained movement as compared to coiled nematodes derived from the same sample (Fig. 3). This suggests that coiling confers survival benefits, either in the field or to the stress of extraction and revival. However, in the soils containing the fewest coiled nematodes (<15%; i.e., most nematodes were vermiform), there was no difference in revival in water for vermiform nematodes compared to coiled (Fig. 3). These vermiform nematodes may have been active above a moisture, salinity, or water potential threshold that existed in these samples. We assumed soils with fewer coiled nematodes were a more favorable environment for nematode activity, and the vermiform and possibly active nematodes in these samples survived the brief stress of extraction and revival. Overall, these field results further confirm laboratory studies showing a positive relationship between coiling and nematode survival.
Results and discussion: soil spatial variation and nematode anhydrobiosis
Eighty-six percent of the nematodes extracted from these soils were identified as S. lindsayae. Soil moisture content, EC, and water potential all were related to the proportion of nematodes coiled (Fig. 4). The proportion of coiled nematodes increased as soils dried, as water potential decreased, and as EC increased (Fig. 4). The soil moisture data seems to confirm a threshold for nematode anhydrobiosis that was previously reported (Treonis et al., 1999). Only a small proportion (<20%) of dry valley nematodes were coiled in soils with a gravimetric moisture content exceeding 2%. Based on this observed pattern, we divided the soils into two groups: 1) "wet" soils with a soil moisture content >2%, and 2) "dry" soils with <2% soil moisture (Fig. 4). Within the "dry" soils, soil moisture and EC spanned a relatively small range, but the proportion of coiled nematodes was extremely variable, ranging from 20–80% (Fig. 4). Soil water potential showed a different pattern than soil moisture and EC. Most of the variation in water potential that our survey captured was in soils drier than 2% soil moisture content (Fig. 4). Water potential, which was correlated with soil moisture and EC, should most accurately reflect biological water availability in the nematode's environment, but coiling was not correlated with water potential in the driest soils analyzed (Fig. 4). The extreme variability in water potential, as compared to EC and soil moisture for the same samples, could simply be a function of the differences in soil sample sizes used for measurement of soil properties (2 g for water potential, 50 g for gravimetric moisture, 90 g for EC). This discrepancy suggests that dry valley soil properties vary on a fine spatial scale as noted by other researchers (Campbell et al., 1998). The soils that cover most of the landscape rarely are saturated, even following a significant snowfall. Water from snowmelt sublimates or seeps into the soil and does not reach or fill all soil pores. This variability is an important consideration for study of nematode anhydrobiosis in these dry soils. The nematode habitat exists on the micro-scale and is subject to heterogeneity in the soil environment demonstrated by these water potential measurements. Furthermore, the anhydrobiotic status of nematodes may be influenced by factors other than those measured, including temperature or the abundance of a microbial food source in the environment. Dry valley soils exhibit small-scale spatial variation that may influence nematode activity at least as much as the large-scale variation that exists across the landscape.
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Results and discussion: soil temporal variation and nematode anhydrobiosis
On a sunny day, soil temperature varied from 2 to 14°C (5 cm depth), and the fewest nematodes were coiled (13%) at the warmest time of the day (Fig. 5). Soil moisture did not change over time, averaging 1.7%. These data contrast with similar data collected on a cloudy day from an adjacent plot, where soil temperature and nematode coiling exhibited far less variation over the diurnal cycle (Fig. 5). These results suggest that nematodes can respond to diurnal changes in soil temperatures that affect soil moisture status. Radiative soil warming may raise the relative humidity of the soil pores by drawing moisture up from deeper layers, triggering nematode uncoiling. Soil moisture averaged 0.24% 14 days prior to the snowfall and 2.7% the day after the snow. 54.4% of nematodes were coiled prior to the snowfall, and 100% were uncoiled afterwards. This indicates nematodes respond rapidly to soil wetting from natural sources. Soil temperatures can be warm enough during January to prevent diurnal freezing, allowing nematode activity for hours or days.
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ANHYDROBIOSIS AND NEMATODE ECOLOGY |
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SYNOPSISINTRODUCTIONNEMATODE ANHYDROBIOSIS IN DRY...ANHYDROBIOSIS AND NEMATODE...References |
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Studies of nematode anhydrobiosis in the dry valley environment help explain how soil properties influence the biology and function of soil nematodes. Our studies show that dry valley nematodes routinely survive conditions that would be considered to be extreme to most other forms of life. The use of an anhydrobiotic survival strategy by these nematodes is associated with increased desiccation of the soil environment. Soil physical and chemical properties vary greatly across the landscape, on fine spatial scales, and over short, diurnal time scales. While we find that a portion of the nematode population always is vermiform, either dead or actively utilizing wet microsites, the majority of nematodes in dry valley soils may be anhydrobiotic and depend on rare precipitation pulses for activity. Although a diurnal change in soil moisture and temperature had a small effect on nematode anhydrobiotic status, soil moisture pulses appear to be the strongest inducement for nematodes to uncoil, as noted in hot desert soils (Whitford et al., 1981
; Freckman et al., 1987). In the dry valley soils, long periods of inactivity by decomposer biota contribute to slow decomposition rates and explain how soil food webs are sustained on very small amounts of soil organic carbon (<0.1% by weight [Treonis et al., 2002]). Long periods of decomposer inactivity also help to explain how organic material can persist in the dry valley soils for thousands of years (Burkins et al., 2000; Treonis et al., 2002; Lawson et al., 2004; Barrett et al., 2005).
The distribution of nematodes across a wide range of soil habitats in the dry valleys is enhanced by their ability to use anhydrobiosis. This survival strategy allows nematodes to persist where a high degree of spatial and temporal variability exist in soils near the limits for life (Treonis et al., 2000; Weicht and Moorhead, 2004). Furthermore, nematodes are distributed throughout the ecosystem by the wind in an anhydrobiotic state (Nkem et al., 2005). Anhydrobiosis ensures survival, and dry valley soil nematodes may spend a significant portion of their lives in this state, extending their life span. Ricci and Pagani (1997) reported that the nematode Panagrolaimus rigidus ages while in anhydrobiosis, but the rate of aging slows as the period of desiccation is extended. Rotifers, however, do not appear to age while in anhydrobiosis (Ricci et al., 1987). Overhoff et al. (1993) determined that the life cycle of S. lindsayae was 218 days at 10°C in the laboratory. If this estimation applies to the field, this species could need years or even decades to complete their life cycle. The age of a typical dry valley soil nematode is enigmatic, and its determination poses an interesting research challenge.
Of the nematodes extracted from each of the dry valley soils sampled for these experiments, 75–100% were S. lindsayae. The remaining nematodes were E. antarcticus, or more rarely, Plectus sp. S. lindsayae has the widest distribution of any animal in the Dry Valleys and has consistently been revived from the anhydrobiotic (coiled) state. E. antarcticus and Plectus sp., as well as tardigrades and rotifers, are relatively more abundant in the higher productivity and wetter locations in the dry valleys, such as within and at the margins of ephemeral streams (Treonis et al., 1999). Gooseff et al. (2003) found higher nematode diversity under a snowpack compared to nearby exposed soil, suggesting that even ephemeral moisture pulses can have significant effects on diversity and population dynamics. Plectus sp. and E. antarcticus, also have been extracted from soils in a coiled form, suggesting an anhydrobiotic survival strategy. Little is known about the biology of dry valley tardigrades and rotifers, but the ability to survive desiccation is likely to be part of their life histories, and both groups are known to be capable of anhydrobiosis (Ricci et al., 1987; Jönsson and Bertolani, 2001; Tunnacliffe and Lapinski, 2003). However, these invertebrates are most abundant in the wettest dry valley habitats, suggesting that they may be less able to survive in drier soils as compared to S. lindsayae.
Conversely, S. lindsayae may be less competitive against other invertebrates in the wettest habitats, suggesting an ecological tradeoff for this nematode's niche specialization in the driest soils where it predominates (Treonis et al., 1999; Wall and Virginia, 1999; Porazinska et al., 2002). We suggest that S. lindsayae has evolved as a dry valley soil specialist and may have enhanced anhydrobiotic abilities compared to other nematode species in Antarctica and elsewhere. For example, these nematodes may survive due to enhanced physiological abilities to retard rapid water loss from their bodies. Alternatively, S. lindsayae may have unique mechanisms to slow molecular damage during long periods of anhydrobiosis. Unfortunately, the long life cycle of this species in the laboratory has limited in-depth study of its physiology and tolerance limits.
Panagrolaimus davidi, a species of nematode found in the wetter, maritime regions of the McMurdo Sound region of Antarctica, is readily cultured and its anhydrobiotic and freeze-tolerance strategies have been studied (Wharton and Barclay, 1993; Wharton and Ferns, 1995; Wharton, 2003; Wharton et al., 2003). Freezing and desiccation both limit biological water availability, but the overlapping nature of nematode responses to these stresses is not well understood (Wharton, 1995; Womersley et al., 1998). Studies of P. davidi suggest that this species can use a "cryoprotective dehydration" strategy of freeze avoidance, but under other conditions simulated in the laboratory, it has the unusual ability to also survive intracellular freezing (Wharton and Ferns, 1995). Dehydration seems to be an important freeze avoidance strategy used by invertebrates in arctic and Antarctic environments (Pickup and Rothery, 1991; Ring and Danks, 1994; Holmstrup et al., 2002; Wharton, 2003). Multiple survival strategies working in tandem, such as those used by P. davidi, might also be relevant for S. lindsayae and contribute to the overall success of invertebrates in polar habitats.
Generally, between 20–80% of nematodes were coiled in the dry valley soils studied during the austral summer. This broad range is consistent with measurements in diverse ecosystems where nematode anhydrobiosis has also been studied using coiling as an indicator (Table 1). However, the degree of abiotic variability in these ecosystems (Table 1) precludes estimation of a nematode activity threshold or detection of differences between habitats or nematode species. The relative anhydrobiotic abilities of different nematode taxa or nematodes from different habitats are not well understood. The use of anhydrobiosis may be related to the fundamental constraints low water potentials place on their physiology, but different species of nematodes could exhibit different sensitivities and/or survival capabilities in response to environmental stressors. Demeure et al. (1979b) found that the species of nematode Scutellonema brachyurum, isolated from a moist semi-tropical planting, exhibited different anhydrobiotic behavior as compared to Acrobeloides sp. isolated from a hot desert soil. S. brachyurum responded to desiccation by coiling faster than Acrobeloides sp., suggesting that this species was less resistant to drying than the hot desert species (Demeure et al., 1979b). This difference seems to represent adaptation by the nematode species to their respective environments (Demeure et al., 1979b). Anguina tritici and Ditylenchus dipsaci are parasites of aerial plant parts and have long served as model organisms for the study of nematode anhydrobiosis. Womersley et al. (1998) suggested these nematodes have enhanced cryptobiotic abilities compared to soil nematodes because their aboveground habitat experiences more rapid desiccation. Ricci (1998) demonstrated that species of rotifers from aquatic habitats were less able to recover successfully from anhydrobiosis than species from drier, moss habitats. Further comparative research is needed to understand whether the anhydrobiotic response is divergent among nematode functional or taxonomic groups in Antarctica and other terrestrial ecosystems.
Anhydrobiosis is broadly distributed among dissimilar taxa in the biological world, suggesting that this is a deeply-rooted, ancient physiological process. The finding of a plant desiccation gene in a nematode genome supports this idea (Browne et al., 2002), as opposed to anhydrobiosis evolving through repeated convergent evolution. Mechanisms of desiccation tolerance such as anhydrobiosis likely accompanied the spread of life from sediments to soils, from oceans to the land (Oliver et al., 2000). The soils in of the earliest terrestrial environments on Earth were probably very similar in some ways to those of the Antarctic Dry Valleys: desert-like, poorly weathered, with low water holding capacity and low organic content. Nematodes are one of the most desiccation tolerant animals on Earth, and their ability to employ an anhydrobiotic survival strategy may help to explain this phylum's almost ubiquitous distribution. Studies of nematode anhydrobiosis in the Antarctic Dry Valleys and other desiccated environments should help us to understand the adaptations that facilitated the success of life's invasion of terrestrial environments.
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ACKNOWLEDGMENTS |
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We thank Peter Alpert for the invitation to participate in the 2005 Society for Integrative and Comparative Biology Desiccation Symposium. Two anonymous reviewers are thanked for their comments on an earlier version of the manuscript. H. Zadeh, J. Kaufman, K. DeNeve, T. Burk, and D. Gray provided critical assistance for which we are thankful. We also thank R. Virginia, E. Kuhn, A. Parsons, D. Bumbarger, P. Brinkman, L. White, L. Powers, M. Burkins, Antarctic Support Associates, and Petroleum Helicopters, Inc. for field and laboratory assistance. B. Wacker and J. Marley at Decagon Devices, Inc., provided considerable technical assistance. Our field research was supported by NSF (OPP 9211773, OPP 9421025, OPP 9522665, OPP9813061, OPP9810219, OPP0096250, OPP0229836) and is a contribution to the McMurdo Dry Valleys Long-Term Ecological Research Program.
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FOOTNOTES |
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2 E-mail: atreonis{at}richmond.edu
1 From the Symposium Drying Without Dying: The Comparative Mechanisms and Evolution of Desiccation Tolerance in Animals, Microbes, and Plants presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2005, at San Diego, California.
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References |
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SYNOPSISINTRODUCTIONNEMATODE ANHYDROBIOSIS IN DRY...ANHYDROBIOSIS AND NEMATODE...References |
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Barrett, J. 1991. Anhydrobiotic nematodes. Agricult. Zool. Rev, 4:161-176.
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