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Soil nematodes indicate food web responses to elevated atmospheric CO2
Pedobiologia 44, 725–735 (2000) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo
Soil nematodes indicate food web responses to elevated atmospheric CO2 Jason D. Hoeksema1, John Lussenhop2 and James A. Teeri3 Department of Environmental Science and Policy, 1 Shields Avenue, University of California – Davis, Davis, CA 95616 2 Biological Sciences Department, University of Illinois at Chicago, 845 W. Taylor, Room 3262, Chicago, IL 60607 3 Director, University of Michigan Biological Station, 1111 Natural Science Building, University of Michigan, Ann Arbor, MI 48109-1048 1
Accepted: 30. July 2000
Summary To understand the impact of rising levels of atmospheric CO2 on ecosystems, we need to understand plant responses to elevated CO2, as well as how those plant responses in turn affect their environment. An important component of the environment of a plant is the soil biota living near plant roots. Soil nematodes are representative of a large portion of this biota, since they are abundant and trophically diverse in most soils. In a three-year field experiment, we studied the responses of soil nematodes to increased root growth of trees growing in high and low nitrogen soils under ambient and twiceambient atmospheric CO2, a two-by-two factorial experimental design. Our hypothesis was that in the high-N soil, increased root growth resulting from twice-ambient atmospheric CO2 would positively affect nematode density, supporting a more abundant and trophically complex nematode community. Trembling aspen (Populus tremuloides) were grown in twenty open-top chambers under the four treatments, replicated five times. In low-N soil, twice-ambient CO2 was associated with higher density of the most abundant plant-feeding taxon (Trichodoridae), lower density of one bacteriafeeding taxon (Rhabditidae), and lower evenness of the community, compared to ambient CO2. In high-N soil, twice-ambient CO2 was associated with higher density of predator/omnivores, lower diversity, and a larger value of Bonger’s Maturity Index, compared to ambient CO2. In soils under young deciduous trees, such as the aspens in this experiment, increased root growth under elevated CO2 may result in significant Corresponding author: Jason D. Hoeksema, e-mail: [email protected]
0031–4056/00/44/06–725 $ 15.00/0
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changes in soil food web community structure that may provide clues about the fate of carbon under elevated CO2. Key words: elevated carbon dioxide, global change, soil food webs, nematodes, Populus
Introduction Impacts of increased root growth on soil food webs are little known and may be useful indicators of the ecological effects of elevated CO2 and the fate of carbon under elevated CO2 (O’Neill 1994; Weiner 1996). Plants often respond to elevated CO2 by increasing root growth (Rogers et al. 1994; Curtis & Wang 1998). As a result of this plant response, the amount of carbon input into the soil ecosystem due to root turnover and herbivory may increase. It has been suggested that populations of organisms feeding on live root material, dead organic matter derived from plant roots, or root exudates may respond to the increased carbon with changes in biomass, activity, or community composition (e.g., Zaller & Arnone 1997). These changes could affect the structure of the soil food web and influence whether soil systems will store carbon under elevated CO2. Nematodes are ubiquitous and important components of soil food webs and can influence ecosystem processes (Coleman et al. 1984). They are abundant and trophically diverse, acting as plant-feeders, bacteria-feeders, fungus-feeders, predators, and omnivores (Yeates et al. 1993). Thus, soil nematodes are a useful component of the soil biota by which the impact on soil food webs of increased root growth under elevated CO2 can be examined. The goal of this investigation was to use soil nematodes as indicators of the fate of carbon and the impact on soil food webs of increased belowground carbon input by young aspen (Populus tremuloides) trees under elevated CO2. In this experiment, fine root biomass and turnover were significantly greater under elevated CO2 for P. tremuloides growing in a high-N soil, but were not significantly affected by elevated CO2 in a low-N soil (Pregitzer et al. 2000; Zak et al. 2000b). Thus, our basic hypothesis about the herbivory path in the food web was that in the high-N soil, carbon flow through this path would be higher, potentially resulting in higher densities of plantfeeding nematodes in response to increased fine root biomass and turnover under elevated CO2. Microbial biomass and community structure were largely unaffected by elevated CO2 in both soils (Zak et al. 2000a). Thus, our basic hypothesis about the decomposer path in the soil food web was that carbon flow through this path would be lower, and that microbe-feeding nematodes in both soils would not respond to elevated CO2. Though various models make different predictions about the correlation between predator numbers and prey numbers (see discussion by Arditi et al. 1991), most predict that the top predators will respond positively to increases in basal resources. Thus, we predicted that predaceous nematodes would increase in response to increased fine root production under elevated CO2 in the high-N soil.
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Materials and Methods The experiment was conducted at the University of Michigan Biological Station in northern lower Michigan, USA (45° 34’ N, 84° 40’ W). Twenty raised beds were constructed in October, 1993. In an open field, the top 20 cm of soil was removed, beds (square, 3.3 meters on a side, 0.4 meters tall) were built with pressure treated lumber, and filled with soil. In order to prevent roots from growing into the beds from the outside, perimeters were trenched to 1.5 m, plastic barriers inserted, and the trenches backfilled. Two contrasting soil treatments were established by filling the beds with either high-N soil (100 % Kalkaska series A horizon, Typic Haplorthod), or low-N soil (homogenized 80 % Rubicon series C horizon, Entic Haplorthod, and 20 % Kalkaska series A horizon). These mixtures resulted in large differences between the low N and high N soils in organic matter content (Low N = 3559 mg C·kg-1; high N = 12489 mg C·kg-1) and average net mineralization rate (low N = 61 ng N g-1 d-1; high N 319 ng N g-1 d-1) (Zak et al. 2000a). These rates of N mineralization are within the range of values commonly encountered in the field by P. tremuloides (Zak et al. 2000a). A complete summary of soil physical and chemical properties can be found in Curtis et al. (2000). Twelve P. tremuloides seedlings derived from locally collected root cuttings were planted in each bed and exposed to ambient or twice-ambient CO2 throughout their growing seasons (approximately May through November) from planting, June 7, 1994, until harvest, July, 1996. Open-top chambers (3 m diam. × 2.3 m high; Heagle et al. 1989) made of polyethylene film supported by aluminum frames were placed over the beds. CO2 partial pressure inside the chambers was increased by dispensing 100 % CO2 into an input blower. The atmosphere inside the chambers was continuously monitored by an infra-red gas analyzer (LI-6252, LICOR Inc., Lincoln, NB) that logged data to a personal computer. CO2 concentrations were adjusted using manual flowmeters. Analysis of air samples taken hourly from within chambers during the experiment showed that mean seasonal daytime CO2 partial pressures (± SE) in twice-ambient and ambient chambers were 70.5 (±0.94) and 35.7 (±0.99) Pa in 1994, 70.7 (±0.97) and 35.7 (±0.77) Pa in 1995, and 72.1 (±1.40) and 36.3 (±1.02) Pa in 1996 respectively. Each treatment combination of high or low N with ambient or twice-ambient CO2 was replicated five times, with the twenty chambers arranged in a randomized complete block design with five blocks of four chambers each.
Six soil cores (2 cm diameter, 26 cm deep) were taken from each chamber in a block immediately before the four chambers in that block were excavated between July 7 and July 31, 1996. For each chamber, the six soil cores were composited on site and refrigerated. Within 48 hours, each sample was passed through a 2 mm sieve to remove debris and roots, mixed thoroughly and subdivided for analyses (100g for nematode extraction and ~100g for gravimetric analysis of water content). Nematodes were extracted from 100 g (fresh mass) of soil from each sample using sugar flotation and centrifugation (Viglierchio & Yamashita 1983; Dropkin 1989). All extracted nematodes in each sample were counted, and up to 100 nematodes in each sample were identified to order, family, or genus when possible. Approximately 18 % of all observed nematodes could not be identified, often because damage from the extraction procedure was too severe or because the nematodes were extracted dead. In samples from which fewer than 100 nematodes were extracted (1 of 10 high-N chambers, and 9 of 10 low-N chambers), all individuals were identified. In samples from which greater than 100 nematodes were extracted, the abundance of each taxon in the 100 g sample was estimated from the proportion of that taxon among the identified nematodes. Soil moisture at time of extraction was determined gravimetrically, and nematode counts were converted to units of number per 100 grams of dry soil. Each nematode taxon was classified as either a plant-feeder, bacteria-feeder, fungus-feeder, or predator/omnivore, according to known feeding habits or stoma and esophageal morphologies (Yeates et al. 1993). Four diversity indices were calculated both for total nematodes and for the plant-feeding group separately. Diversity indices were chosen based on recommendations by Ludwig and Reynolds (1988). N0 was determined as the total number of taxa, N1 as an estimate of the number of abundant taxa, N2 as an estimate of the number of very abundant taxa, and E5 as an index of the evenness of the community (Hill 1973; Ludwig & Reynolds
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1988). N1 was calculated as eH’, where H’= – Σ[pi(lnpi)] or the Shannon index (Shannon & Weaver 1964) with pi the proportion of each of the i taxa present. N2 was calculated as 1/λ, where λ=Σ(pi)2 or Simpson’s index (Simpson 1949). E5, the modified Hill’s ratio, was calculated as (N2-1)/(N1-1). Following Bongers and Bongers (1998), we gave each nematode taxon a value from one to five on a “colonizer” to “persister” (c-p) scale. We used these values to calculate the Maturity Index (MI) as Σfivi, where fi is the proportion of each of the nematode taxon i in the sample, and vi is the c-p scale value assigned to taxon i. Based on life history characteristics and empirical observations, Bongers (1990) developed this index of soil “maturity” based on nematode taxonomic composition. A separate index, the plant parasite index (PPI) was calculated similarly to the MI, but only includes plant-feeding nematode taxa. Since the nematode count data could not be transformed to meet the assumptions of parametric statistical tests, randomization tests with 10,000 repetitions were used for paired contrasts of nematode abundances between ambient and twice-ambient CO2 treatments (Edgington 1987; Manly 1991). All statistical comparisons were made only between ambient and twice-ambient treatments within each soil type (high- or low-N) because differences in soil type may have affected nematode extraction efficiency (Barker 1985).
Results The total density of nematodes did not differ significantly between ambient and twiceambient CO2 for either soil type (Table 1). Population-level and Trophic Group Responses Low-N soil. The Trichodoridae, which were the most abundant plant-feeders in low-N soil, were significantly more abundant in the twice-ambient CO2 treatment (p<0.001; Table 1). Overall, the plant-feeding trophic group tended to be more abundant in the twice-ambient CO2 treatment (p=0.092). One family of bacteria-feeding nematodes, the Rhabditidae, was less abundant in twice-ambient CO2 (p=0.027). The fungus-feeding nematode genus Aphelenchus tended to be more abundant with twiceambient CO2 (p=0.089). As trophic groups, bacteria-feeders, fungus-feeders, and predator/omnivores did not respond to twice-ambient atmospheric CO2 in the low-N soil. Under ambient CO2, the order of trophic groups from low-N soil ranked by abundance was: predator/omnivores > plant-feeders > bacteria-feeders > fungus-feeders (Table 1). Under twice-ambient CO2, the ranks were: plant-feeders > predator/omnivores > bacteria-feeders > fungus-feeders (Table 1). High-N soil. In high-N soil, the omnivorous Dorylaimida were more abundant under twice ambient CO2 (p=0.019), the predaceous Mononchidae tended to be more abundant (p=0.094), and the predaceous/omnivorous nematodes as a group were significantly more abundant under twice-ambient atmospheric CO2 (p=0.011). Abundance of plant-feeding, bacteria-feeding, and fungus-feeding nematode groups was not significantly different between ambient and twice-ambient CO2 treatments. One family of bacteria-feeding nematodes, the Cephalobidae, tended to be less abundant with twice-ambient CO2 (p=0.067). Under both ambient and twice-ambient CO2, the order of trophic groups from high-N soil ranked by abundance was the same: plantfeeders > bacteria-feeders > predator/omnivores > fungus-feeders (Table 1).
Group/Taxon Plant-feeders Criconemella Ditylenchus Longidorinae Pratylenchus Trichodoridae Tylenchidae Xiphinema Bacteria-feeders Cephalobidae Monhysteridae Plectidae Prismatolaimidae Rhabditidae Fungus-feeders Aphelenchus Nothotylenchus Predator/omnivores Dorylaimida Mononchidae Total nematodes
High-N Soil ———————————————————— Ambient Elevated 148.5 (75.3) 208.3 (63.2) 11.9 (5.0) 3.9 (1.5) 1.8 (0.8) 0.00 4.3 (4.0) 5.6 (5.6) 0.4 (0.4) 0.8 (0.5) 54.0 (26.0) 81.8 (44.5) 75.7 (41.9) 103.4 (27.7) 0.4 (0.3) 12.7 (12.7) 42.4 (12.5) 25.8 (2.3) 21.4 (4.6) 12.0 (3.1)* 1.8 (1.4) 0.00 14.7 (6.4) 9.9 (1.5) 0.00 0.00 4.5 (1.9) 3.9 (2.7) 2.9 (1.6) 2.3 (1.2) 2.7 (1.6) 1.9 (1.2) 0.2 (0.2) 0.4 (0.4) 7.2 (1.1) 20.2 (6.9)** 3.5 (1.1) 13.8 (5.7)** 3.7 (1.3) 6.4 (1.5)* 243.3 (110.0) 308.3 (75.0)
Low-N Soil ———————————————————— Ambient Elevated 13.2 (4.3) 27.5 (9.6)* 0.00 1.2 (1.0) 0.2 (0.2) 0.4 (0.4) 1.0 (0.6) 1.4 (0.5) 0.00 0.00 6.6 (1.2) 15.8 (2.6)*** 2.7 (2.2) 6.7 (6.0) 2.7 (1.5) 1.9 (0.7) 6.4 (2.4) 4.5 (1.3) 2.5 (1.3) 2.5 (0.8) 0.00 0.00 1.0 (0.7) 1.0 (0.6) 0.6 (0.6) 0.8 (0.6) 2.3 (1.1) 0.2 (0.2)** 0.6 (0.6) 0.6 (0.4) 0.2 (0.2) 0.6 (0.4)* 0.4 (0.4) 0.00 16.9 (2.4) 18.1 (7.3) 10.9 (3.6) 14.2 (5.7) 6.0 (1.6) 3.9 (1.9) 44.7 (7.7) 62.6 (23.0)
Table 1. Density (individuals per 100g soil dry wt.) of nematode taxa and trophic groups at ambient and elevated (twice-ambient) CO2 in two soil types (high-N and low-N). Each value is the average (standard error) of 5 replicate experimental units. Significance is indicated (*0.05
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Group/Taxon Plant-feeder Diversity Total taxa (NO) Abundant taxa (N1) Very abundant taxa (N2) Evenness (E5) Total Nematode Diversity Total taxa (NO) Abundant taxa (N1) Very abundant taxa (N2) Evenness (E5) Nematode Community Structure Indices Plant Parasite Index (PPI) Maturity Index (MI) 3.0 (0.2) 2.96 (0.12)**
(0.4)* (0.2)** (0.2)** (0.05)
2.9 (0.1) 2.70 (0.04)
3.4 2.3 2.1 0.83 8.8 4.42 (0.40)* 3.25 (0.32)** 0.65 (0.04)*
(0.4) (0.02) (0.1) (0.07)
9.8 5.95 (0.86) 4.70 (0.78) 0.73 (0.03)
4.6 2.7 2.5 0.87
High-N Soil ———————————————————— Ambient Elevated (0.73) (0.5) (0.5) (0.19)
4.0 (0.2) 3.59 (0.18)
7.2 5.41 (0.82) 4.52 (0.65) 0.80 (0.04)
2.8 2.4 2.3 0.73
(0.58) (0.3) (0.3) (0.05)
3.9 (0.2) 3.68 (0.13)
8.2 4.96 (0.56) 3.77 (0.51) 0.68 (0.05)**
3.8 2.2 1.9 0.65
Low-N Soil ———————————————————— Ambient Elevated
Table 2. Community indices for nematodes at ambient and elevated (twice ambient) CO2 in two soil types (high-N and low-N). Each value is the average (standard error) of 5 replicate experimental units. Significance is indicated (*0.05
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Community-level Responses In the low-N soil, evenness was significantly lower under twice-ambient CO2 for the whole nematode community together (p=0.041; Table 2). In the high-N soil, a number of diversity index values differed significantly between ambient and twice-ambient CO2 (Table 2). Within the plant-feeding trophic group, the effective number of abundant taxa, as well as the effective number of very abundant taxa, were significantly lower with twice-ambient CO2, and the richness tended to be lower (p=0.074). For all nematodes together, the effective number of very abundant taxa was significantly smaller with twice-ambient CO2 (p=0.043). Both the effective number of abundant taxa (p=0.059) and evenness (p=0.065) tended to be smaller with elevated CO2. Bongers’ Maturity Index was significantly greater with twice-ambient CO2 in the high-N soil (p=0.018).
Discussion Since microbial biomass and community composition (based on phospholipid fatty acid profiles) were relatively unchanged under elevated CO2 in this experiment (Zak et al. 2000a), we did not expect to see increases in bacteria-feeding and fungus-feeding nematodes in response to elevated CO2. In fact, while some families of bacteriafeeders were actually less abundant under twice-ambient CO2 (for example the Rhabditidae in low-N soil), most bacteria-feeding and fungus-feeding taxa were not significantly affected by the elevated CO2 treatment in either soil. Thus, the results for the decomposition path of the soil food web are not unexpected. More puzzling, however, are the results for the herbivore path of the soil food web. Since elevated CO2 significantly increased the biomass and turnover of fine roots in high-N soil (final biomass was 66 % higher and net cumulative production was approximately 25 % higher under elevated CO2), but had no statistically significant effect on fine roots in the low-N soil (Pregitzer et al. 2000; Zak et al. 2000b), then according to our basic initial hypothesis plant-feeding nematodes should have been more abundant under elevated CO2 in the high-N soil, but not in the low-N soil. However, significant positive effects of elevated CO2 were seen for the dominant taxon of plant-feeding nematodes (Trichodoridae) in low-N soil. The only trophic group that increased in response to elevated CO2 in the high-N soil was the predaceous nematodes. In summary, the abundances of all nematode trophic groups did not simply track the availability of their resources. The response of the nematode community to elevated CO2 was not a simple overall increase in response to more belowground carbon input as would be predicted by ratio-dependent predation models. Such models predict a positive correlation between numbers of predators and numbers of their prey, such that an increase in basal resources should cause an increase in herbivores and predators (a strictly “bottom-up” effect, see Arditi et al. 1991). One explanation for these data is that while belowground carbon input in the highN soil increased in response to elevated CO2, resource quality decreased, preventing strong trophic responses by soil organisms to increased plant biomass. In fact, tissue N concentrations were significantly lower for plants grown under elevated CO2 for both soil types (Zak et al. 2000a). This result may explain why plant-feeding nematodes did not respond significantly to elevated CO2 in the high-N soil, despite signifi-
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cant increases in fine root biomass and turnover in the high-N soil. If this is true, however, then why were plant-feeding nematodes more abundant under elevated CO2 in the low-N soil? Furthermore, what caused the increase in predaceous/omnivorous nematodes in response to elevated CO2 in the high-N soil if neither plant-feeding nor bacteria-feeding nematodes increased? A potential answer to these questions is that under elevated CO2 in both soils the soil fauna responded to increased belowground carbon input by aspen roots in the manner of a trophic cascade (sensu Carpenter et al. 1985; Carpenter & Kitchell 1993). According to this explanation, a small increase in root production in low-N soil under twice-ambient CO2 was balanced by increased numbers of (and root consumption by) plant-feeding nematodes (the most abundant family, Trichodoridae), so that we did not observe an increase in root standing biomass. However, the total resource base was not large enough to impact higher trophic levels (predaceous/omnivorous nematodes). In the high-N soil, a larger increase in root production under elevated CO2 was sufficient to support a larger food web such that increases were seen in higher trophic levels (predaceous/omnivorous nematodes), which suppressed the middle trophic levels (bacteria-feeders and plant-feeders), allowing us to observe an increase at the lowest trophic level (increased root biomass). Such a response of predaceous nematodes to increased availability of their prey has been observed previously (e.g., Wardle et al. 1995); however, since a time lag in this response is likely, sequential sampling would probably be necessary to confirm such a strong trophic link. Furthermore, without sequential sampling it is impossible to tell whether low numbers of a nematode group indicate low reproduction of that group, or high reproduction and high mortality. In summary, though these data do not demonstrate that a trophic cascade occurred in response to elevated CO2, they are consistent with this hypothesis. Most models of food web response to increased basal resources, including both trophic cascade models (Carpenter et al. 1985; Carpenter & Kitchell 1993) and ratiodependent predation models (Arditi et al. 1991), predict that the total biomass of the organisms above the basal resource will be greater. In the high-N soil, we observed statistically significant increases in the predaceous/omnivorous nematodes, and no statistically significant changes in the other trophic groups. Since predaceous/omnivorous nematodes are usually much larger than bacteria-feeding and fungus-feeding nematodes (e.g., Yeates 1973), and as large or larger than most plant-feeding nematodes, total nematode biomass probably increased in the high-N soil in response to elevated CO2. If soil food webs do respond to increased belowground production under elevated CO2 by increasing in biomass, then they may provide some degree of storage for carbon. While evenness was significantly lower under twice-ambient CO2 in the low-N soil, responses of nematode community structure to twice-ambient CO2 were generally stronger in high than in low-N soil. For example, in high-N soil, the number of abundant taxa was significantly smaller for all nematodes and the number of very abundant taxa was significantly smaller for plant-feeders in the twice-ambient CO2 treatment (Table 2). Because the total number of taxa was not different between CO2 treatments, the nematode community had relatively fewer common and relatively more rare taxa under twice-ambient CO2 than under ambient CO2. Most previous studies examining responses of soil nematodes to increased root production resulting from experimentally elevated atmospheric CO2 have reported increased total densities (Yeates & Orchard 1993; Runion et al. 1994; Klironomos et al.
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1996; Yeates et al. 1997), while one observed no changes in soil nematodes in response to elevated CO2 (Newton et al. 1995). Two previous studies (Yeates & Orchard 1993; Yeates et al. 1997), both in grazed pasture plant communities, identified the taxonomic identity of nematodes in an experiment with elevated CO2 (though Yeates and Orchard (1993) do not present abundance data for all taxa identified). One pattern common to those two studies and ours (high-N soil) is that the nematodes responding most consistently to elevated CO2 are the predaceous/omnivorous nematodes, which increased under elevated CO2 in all three studies. That the abundance of higher trophic levels increased under elevated CO2 in these two different systems is consistent with the hypothesis that soil food webs can respond to increased belowground carbon inputs under elevated CO2 by increasing in biomass. Another response observed only in the high-N soil in our study was a significantly greater Maturity Index for total nematodes (excluding plant-feeders) under twice-ambient compared with ambient CO2 (Table 2). Using the means for each taxon reported by Yeates et al. (1997) we calculated the same two nematode community structure indices calculated for our data (MI and PPI). Similarly to the high-N soil in our study, MI increased by approximately 20 % under elevated CO2 (from 1.18 to 1.45), while PPI changed little (1.44 to 1.35). Thus, in these two studies (ours and that reported by Yeates et al. 1997), the nematode community shifted in response to elevated CO2 to include a higher relative abundance of taxa having lower reproductive rate, lower colonization ability, and higher sensitivity to pollutants (according to Bongers 1990). A close examination of the nematode portion of the soil foodweb indicates that twice-ambient atmospheric CO2, most likely through increased root production by plants, was associated with significant changes in the soil nematode community that were not reflected in total density changes. While we were not able to examine other important members of the soil fauna (e.g., predaceous mites), soil nematodes are good indicators of the structure of the soil food web, and the results presented here suggest that responses of soil biota to climate change may be significant and may provide clues as to the fate of carbon under elevated CO2.
Acknowledgments We thank M. Byrny and F. Warner for advice, H. Ferris, M. W. Schwartz, and R. Venette for help with data analysis and interpretation, and Tony Sutterley and Richard Spray for help in the field. C. A. Brigham and A. Treonis provided helpful comments on earlier drafts of this manuscript. This research was supported by the National Institute for Global Environmental Change through the U.S. Department of Energy (Cooperative Agreement No. DE-FC0390ER61010), DOE Grant 93PER6166, and the University of Michigan Biological Station. Any opinions, findings, and conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the DOE.
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Viglierchio, D.R., Yamashita, T.T. (1983) On the methodology of nematode extraction from field samples: density flotation techniques. Journal of Nematology 15, 444–449. Wardle, D.A., Yeates, G.W., Watson, R.N., Nicholson, K.S. (1995) Development of the decomposer food-web, trophic relationships, and ecosystem properties during a three-year primary succession in sawdust. Oikos 73, 155–166. Weiner, J. (1996) Problems in predicting the ecological effects of elevated CO2. In: Körner, C., Bazzaz, F.A. (eds) Carbon dioxide, populations, and communities. Academic Press, San Diego, pp. 431–441. Yeates, G.W. (1973) Nematoda of a Danish beech forest. II. Production estimates. Oikos 24, 179–185. Yeates, G.W., Orchard, V.A. (1993) Decomposition processes to elevated carbon dioxide and temperature—a climate chamber experiment. In: Prestige, R.A. (ed) Proceedings of the 6th Australasian Grassland Invertebrate Ecology Conference. AgResearch, Hamilton, New Zealand, pp.148–154. Yeates, G.W., Bongers, T., de Goede, R.G.M., Freckman, D.W., Georgieva, S.S. (1993) Feeding habits in soil nematode families and genera—An outline for soil ecologists. Journal of Nematology 25, 315–331. Yeates, G.W., Tate, K.R., Newton, P.C.D. (1997) Response of the fauna of a grassland soil to doubling of atmospheric carbon dioxide concentration. Biology and Fertility of Soils 25, 307–315. Zak, D.R., Pregitzer, K.S., Curtis, P.S., Holmes, W.E. (2000a) Atmospheric CO2 and the composition and function of soil microbial communities. Ecological Applications 10, 47–59. Zak, D.R., Pregitzer, K.S., Curtis, P.S., Vogel, C.S., Holmes, W.E., Lussenhop, J. (2000b) Atmospheric CO2 , Soil-N availability, and allocation of biomass and nitrogen by Populus tremuloides. Ecological Applications 10, 34–46. Zaller, J.G., Arnone, J.A. (1997) Activity of surface-casting earthworms in a calcareous grassland under elevated atmospheric CO2. Oecologia 111, 249–254.
Soil nematodes indicate food web responses to elevated atmospheric CO2 Jason D. Hoeksema1, John Lussenhop2 and James A. Teeri3 Department of Environmental Science and Policy, 1 Shields Avenue, University of California – Davis, Davis, CA 95616 2 Biological Sciences Department, University of Illinois at Chicago, 845 W. Taylor, Room 3262, Chicago, IL 60607 3 Director, University of Michigan Biological Station, 1111 Natural Science Building, University of Michigan, Ann Arbor, MI 48109-1048 1
Accepted: 30. July 2000
Summary To understand the impact of rising levels of atmospheric CO2 on ecosystems, we need to understand plant responses to elevated CO2, as well as how those plant responses in turn affect their environment. An important component of the environment of a plant is the soil biota living near plant roots. Soil nematodes are representative of a large portion of this biota, since they are abundant and trophically diverse in most soils. In a three-year field experiment, we studied the responses of soil nematodes to increased root growth of trees growing in high and low nitrogen soils under ambient and twiceambient atmospheric CO2, a two-by-two factorial experimental design. Our hypothesis was that in the high-N soil, increased root growth resulting from twice-ambient atmospheric CO2 would positively affect nematode density, supporting a more abundant and trophically complex nematode community. Trembling aspen (Populus tremuloides) were grown in twenty open-top chambers under the four treatments, replicated five times. In low-N soil, twice-ambient CO2 was associated with higher density of the most abundant plant-feeding taxon (Trichodoridae), lower density of one bacteriafeeding taxon (Rhabditidae), and lower evenness of the community, compared to ambient CO2. In high-N soil, twice-ambient CO2 was associated with higher density of predator/omnivores, lower diversity, and a larger value of Bonger’s Maturity Index, compared to ambient CO2. In soils under young deciduous trees, such as the aspens in this experiment, increased root growth under elevated CO2 may result in significant Corresponding author: Jason D. Hoeksema, e-mail: [email protected]
0031–4056/00/44/06–725 $ 15.00/0
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changes in soil food web community structure that may provide clues about the fate of carbon under elevated CO2. Key words: elevated carbon dioxide, global change, soil food webs, nematodes, Populus
Introduction Impacts of increased root growth on soil food webs are little known and may be useful indicators of the ecological effects of elevated CO2 and the fate of carbon under elevated CO2 (O’Neill 1994; Weiner 1996). Plants often respond to elevated CO2 by increasing root growth (Rogers et al. 1994; Curtis & Wang 1998). As a result of this plant response, the amount of carbon input into the soil ecosystem due to root turnover and herbivory may increase. It has been suggested that populations of organisms feeding on live root material, dead organic matter derived from plant roots, or root exudates may respond to the increased carbon with changes in biomass, activity, or community composition (e.g., Zaller & Arnone 1997). These changes could affect the structure of the soil food web and influence whether soil systems will store carbon under elevated CO2. Nematodes are ubiquitous and important components of soil food webs and can influence ecosystem processes (Coleman et al. 1984). They are abundant and trophically diverse, acting as plant-feeders, bacteria-feeders, fungus-feeders, predators, and omnivores (Yeates et al. 1993). Thus, soil nematodes are a useful component of the soil biota by which the impact on soil food webs of increased root growth under elevated CO2 can be examined. The goal of this investigation was to use soil nematodes as indicators of the fate of carbon and the impact on soil food webs of increased belowground carbon input by young aspen (Populus tremuloides) trees under elevated CO2. In this experiment, fine root biomass and turnover were significantly greater under elevated CO2 for P. tremuloides growing in a high-N soil, but were not significantly affected by elevated CO2 in a low-N soil (Pregitzer et al. 2000; Zak et al. 2000b). Thus, our basic hypothesis about the herbivory path in the food web was that in the high-N soil, carbon flow through this path would be higher, potentially resulting in higher densities of plantfeeding nematodes in response to increased fine root biomass and turnover under elevated CO2. Microbial biomass and community structure were largely unaffected by elevated CO2 in both soils (Zak et al. 2000a). Thus, our basic hypothesis about the decomposer path in the soil food web was that carbon flow through this path would be lower, and that microbe-feeding nematodes in both soils would not respond to elevated CO2. Though various models make different predictions about the correlation between predator numbers and prey numbers (see discussion by Arditi et al. 1991), most predict that the top predators will respond positively to increases in basal resources. Thus, we predicted that predaceous nematodes would increase in response to increased fine root production under elevated CO2 in the high-N soil.
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Materials and Methods The experiment was conducted at the University of Michigan Biological Station in northern lower Michigan, USA (45° 34’ N, 84° 40’ W). Twenty raised beds were constructed in October, 1993. In an open field, the top 20 cm of soil was removed, beds (square, 3.3 meters on a side, 0.4 meters tall) were built with pressure treated lumber, and filled with soil. In order to prevent roots from growing into the beds from the outside, perimeters were trenched to 1.5 m, plastic barriers inserted, and the trenches backfilled. Two contrasting soil treatments were established by filling the beds with either high-N soil (100 % Kalkaska series A horizon, Typic Haplorthod), or low-N soil (homogenized 80 % Rubicon series C horizon, Entic Haplorthod, and 20 % Kalkaska series A horizon). These mixtures resulted in large differences between the low N and high N soils in organic matter content (Low N = 3559 mg C·kg-1; high N = 12489 mg C·kg-1) and average net mineralization rate (low N = 61 ng N g-1 d-1; high N 319 ng N g-1 d-1) (Zak et al. 2000a). These rates of N mineralization are within the range of values commonly encountered in the field by P. tremuloides (Zak et al. 2000a). A complete summary of soil physical and chemical properties can be found in Curtis et al. (2000). Twelve P. tremuloides seedlings derived from locally collected root cuttings were planted in each bed and exposed to ambient or twice-ambient CO2 throughout their growing seasons (approximately May through November) from planting, June 7, 1994, until harvest, July, 1996. Open-top chambers (3 m diam. × 2.3 m high; Heagle et al. 1989) made of polyethylene film supported by aluminum frames were placed over the beds. CO2 partial pressure inside the chambers was increased by dispensing 100 % CO2 into an input blower. The atmosphere inside the chambers was continuously monitored by an infra-red gas analyzer (LI-6252, LICOR Inc., Lincoln, NB) that logged data to a personal computer. CO2 concentrations were adjusted using manual flowmeters. Analysis of air samples taken hourly from within chambers during the experiment showed that mean seasonal daytime CO2 partial pressures (± SE) in twice-ambient and ambient chambers were 70.5 (±0.94) and 35.7 (±0.99) Pa in 1994, 70.7 (±0.97) and 35.7 (±0.77) Pa in 1995, and 72.1 (±1.40) and 36.3 (±1.02) Pa in 1996 respectively. Each treatment combination of high or low N with ambient or twice-ambient CO2 was replicated five times, with the twenty chambers arranged in a randomized complete block design with five blocks of four chambers each.
Six soil cores (2 cm diameter, 26 cm deep) were taken from each chamber in a block immediately before the four chambers in that block were excavated between July 7 and July 31, 1996. For each chamber, the six soil cores were composited on site and refrigerated. Within 48 hours, each sample was passed through a 2 mm sieve to remove debris and roots, mixed thoroughly and subdivided for analyses (100g for nematode extraction and ~100g for gravimetric analysis of water content). Nematodes were extracted from 100 g (fresh mass) of soil from each sample using sugar flotation and centrifugation (Viglierchio & Yamashita 1983; Dropkin 1989). All extracted nematodes in each sample were counted, and up to 100 nematodes in each sample were identified to order, family, or genus when possible. Approximately 18 % of all observed nematodes could not be identified, often because damage from the extraction procedure was too severe or because the nematodes were extracted dead. In samples from which fewer than 100 nematodes were extracted (1 of 10 high-N chambers, and 9 of 10 low-N chambers), all individuals were identified. In samples from which greater than 100 nematodes were extracted, the abundance of each taxon in the 100 g sample was estimated from the proportion of that taxon among the identified nematodes. Soil moisture at time of extraction was determined gravimetrically, and nematode counts were converted to units of number per 100 grams of dry soil. Each nematode taxon was classified as either a plant-feeder, bacteria-feeder, fungus-feeder, or predator/omnivore, according to known feeding habits or stoma and esophageal morphologies (Yeates et al. 1993). Four diversity indices were calculated both for total nematodes and for the plant-feeding group separately. Diversity indices were chosen based on recommendations by Ludwig and Reynolds (1988). N0 was determined as the total number of taxa, N1 as an estimate of the number of abundant taxa, N2 as an estimate of the number of very abundant taxa, and E5 as an index of the evenness of the community (Hill 1973; Ludwig & Reynolds
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1988). N1 was calculated as eH’, where H’= – Σ[pi(lnpi)] or the Shannon index (Shannon & Weaver 1964) with pi the proportion of each of the i taxa present. N2 was calculated as 1/λ, where λ=Σ(pi)2 or Simpson’s index (Simpson 1949). E5, the modified Hill’s ratio, was calculated as (N2-1)/(N1-1). Following Bongers and Bongers (1998), we gave each nematode taxon a value from one to five on a “colonizer” to “persister” (c-p) scale. We used these values to calculate the Maturity Index (MI) as Σfivi, where fi is the proportion of each of the nematode taxon i in the sample, and vi is the c-p scale value assigned to taxon i. Based on life history characteristics and empirical observations, Bongers (1990) developed this index of soil “maturity” based on nematode taxonomic composition. A separate index, the plant parasite index (PPI) was calculated similarly to the MI, but only includes plant-feeding nematode taxa. Since the nematode count data could not be transformed to meet the assumptions of parametric statistical tests, randomization tests with 10,000 repetitions were used for paired contrasts of nematode abundances between ambient and twice-ambient CO2 treatments (Edgington 1987; Manly 1991). All statistical comparisons were made only between ambient and twice-ambient treatments within each soil type (high- or low-N) because differences in soil type may have affected nematode extraction efficiency (Barker 1985).
Results The total density of nematodes did not differ significantly between ambient and twiceambient CO2 for either soil type (Table 1). Population-level and Trophic Group Responses Low-N soil. The Trichodoridae, which were the most abundant plant-feeders in low-N soil, were significantly more abundant in the twice-ambient CO2 treatment (p<0.001; Table 1). Overall, the plant-feeding trophic group tended to be more abundant in the twice-ambient CO2 treatment (p=0.092). One family of bacteria-feeding nematodes, the Rhabditidae, was less abundant in twice-ambient CO2 (p=0.027). The fungus-feeding nematode genus Aphelenchus tended to be more abundant with twiceambient CO2 (p=0.089). As trophic groups, bacteria-feeders, fungus-feeders, and predator/omnivores did not respond to twice-ambient atmospheric CO2 in the low-N soil. Under ambient CO2, the order of trophic groups from low-N soil ranked by abundance was: predator/omnivores > plant-feeders > bacteria-feeders > fungus-feeders (Table 1). Under twice-ambient CO2, the ranks were: plant-feeders > predator/omnivores > bacteria-feeders > fungus-feeders (Table 1). High-N soil. In high-N soil, the omnivorous Dorylaimida were more abundant under twice ambient CO2 (p=0.019), the predaceous Mononchidae tended to be more abundant (p=0.094), and the predaceous/omnivorous nematodes as a group were significantly more abundant under twice-ambient atmospheric CO2 (p=0.011). Abundance of plant-feeding, bacteria-feeding, and fungus-feeding nematode groups was not significantly different between ambient and twice-ambient CO2 treatments. One family of bacteria-feeding nematodes, the Cephalobidae, tended to be less abundant with twice-ambient CO2 (p=0.067). Under both ambient and twice-ambient CO2, the order of trophic groups from high-N soil ranked by abundance was the same: plantfeeders > bacteria-feeders > predator/omnivores > fungus-feeders (Table 1).
Group/Taxon Plant-feeders Criconemella Ditylenchus Longidorinae Pratylenchus Trichodoridae Tylenchidae Xiphinema Bacteria-feeders Cephalobidae Monhysteridae Plectidae Prismatolaimidae Rhabditidae Fungus-feeders Aphelenchus Nothotylenchus Predator/omnivores Dorylaimida Mononchidae Total nematodes
High-N Soil ———————————————————— Ambient Elevated 148.5 (75.3) 208.3 (63.2) 11.9 (5.0) 3.9 (1.5) 1.8 (0.8) 0.00 4.3 (4.0) 5.6 (5.6) 0.4 (0.4) 0.8 (0.5) 54.0 (26.0) 81.8 (44.5) 75.7 (41.9) 103.4 (27.7) 0.4 (0.3) 12.7 (12.7) 42.4 (12.5) 25.8 (2.3) 21.4 (4.6) 12.0 (3.1)* 1.8 (1.4) 0.00 14.7 (6.4) 9.9 (1.5) 0.00 0.00 4.5 (1.9) 3.9 (2.7) 2.9 (1.6) 2.3 (1.2) 2.7 (1.6) 1.9 (1.2) 0.2 (0.2) 0.4 (0.4) 7.2 (1.1) 20.2 (6.9)** 3.5 (1.1) 13.8 (5.7)** 3.7 (1.3) 6.4 (1.5)* 243.3 (110.0) 308.3 (75.0)
Low-N Soil ———————————————————— Ambient Elevated 13.2 (4.3) 27.5 (9.6)* 0.00 1.2 (1.0) 0.2 (0.2) 0.4 (0.4) 1.0 (0.6) 1.4 (0.5) 0.00 0.00 6.6 (1.2) 15.8 (2.6)*** 2.7 (2.2) 6.7 (6.0) 2.7 (1.5) 1.9 (0.7) 6.4 (2.4) 4.5 (1.3) 2.5 (1.3) 2.5 (0.8) 0.00 0.00 1.0 (0.7) 1.0 (0.6) 0.6 (0.6) 0.8 (0.6) 2.3 (1.1) 0.2 (0.2)** 0.6 (0.6) 0.6 (0.4) 0.2 (0.2) 0.6 (0.4)* 0.4 (0.4) 0.00 16.9 (2.4) 18.1 (7.3) 10.9 (3.6) 14.2 (5.7) 6.0 (1.6) 3.9 (1.9) 44.7 (7.7) 62.6 (23.0)
Table 1. Density (individuals per 100g soil dry wt.) of nematode taxa and trophic groups at ambient and elevated (twice-ambient) CO2 in two soil types (high-N and low-N). Each value is the average (standard error) of 5 replicate experimental units. Significance is indicated (*0.05
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Group/Taxon Plant-feeder Diversity Total taxa (NO) Abundant taxa (N1) Very abundant taxa (N2) Evenness (E5) Total Nematode Diversity Total taxa (NO) Abundant taxa (N1) Very abundant taxa (N2) Evenness (E5) Nematode Community Structure Indices Plant Parasite Index (PPI) Maturity Index (MI) 3.0 (0.2) 2.96 (0.12)**
(0.4)* (0.2)** (0.2)** (0.05)
2.9 (0.1) 2.70 (0.04)
3.4 2.3 2.1 0.83 8.8 4.42 (0.40)* 3.25 (0.32)** 0.65 (0.04)*
(0.4) (0.02) (0.1) (0.07)
9.8 5.95 (0.86) 4.70 (0.78) 0.73 (0.03)
4.6 2.7 2.5 0.87
High-N Soil ———————————————————— Ambient Elevated (0.73) (0.5) (0.5) (0.19)
4.0 (0.2) 3.59 (0.18)
7.2 5.41 (0.82) 4.52 (0.65) 0.80 (0.04)
2.8 2.4 2.3 0.73
(0.58) (0.3) (0.3) (0.05)
3.9 (0.2) 3.68 (0.13)
8.2 4.96 (0.56) 3.77 (0.51) 0.68 (0.05)**
3.8 2.2 1.9 0.65
Low-N Soil ———————————————————— Ambient Elevated
Table 2. Community indices for nematodes at ambient and elevated (twice ambient) CO2 in two soil types (high-N and low-N). Each value is the average (standard error) of 5 replicate experimental units. Significance is indicated (*0.05
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Community-level Responses In the low-N soil, evenness was significantly lower under twice-ambient CO2 for the whole nematode community together (p=0.041; Table 2). In the high-N soil, a number of diversity index values differed significantly between ambient and twice-ambient CO2 (Table 2). Within the plant-feeding trophic group, the effective number of abundant taxa, as well as the effective number of very abundant taxa, were significantly lower with twice-ambient CO2, and the richness tended to be lower (p=0.074). For all nematodes together, the effective number of very abundant taxa was significantly smaller with twice-ambient CO2 (p=0.043). Both the effective number of abundant taxa (p=0.059) and evenness (p=0.065) tended to be smaller with elevated CO2. Bongers’ Maturity Index was significantly greater with twice-ambient CO2 in the high-N soil (p=0.018).
Discussion Since microbial biomass and community composition (based on phospholipid fatty acid profiles) were relatively unchanged under elevated CO2 in this experiment (Zak et al. 2000a), we did not expect to see increases in bacteria-feeding and fungus-feeding nematodes in response to elevated CO2. In fact, while some families of bacteriafeeders were actually less abundant under twice-ambient CO2 (for example the Rhabditidae in low-N soil), most bacteria-feeding and fungus-feeding taxa were not significantly affected by the elevated CO2 treatment in either soil. Thus, the results for the decomposition path of the soil food web are not unexpected. More puzzling, however, are the results for the herbivore path of the soil food web. Since elevated CO2 significantly increased the biomass and turnover of fine roots in high-N soil (final biomass was 66 % higher and net cumulative production was approximately 25 % higher under elevated CO2), but had no statistically significant effect on fine roots in the low-N soil (Pregitzer et al. 2000; Zak et al. 2000b), then according to our basic initial hypothesis plant-feeding nematodes should have been more abundant under elevated CO2 in the high-N soil, but not in the low-N soil. However, significant positive effects of elevated CO2 were seen for the dominant taxon of plant-feeding nematodes (Trichodoridae) in low-N soil. The only trophic group that increased in response to elevated CO2 in the high-N soil was the predaceous nematodes. In summary, the abundances of all nematode trophic groups did not simply track the availability of their resources. The response of the nematode community to elevated CO2 was not a simple overall increase in response to more belowground carbon input as would be predicted by ratio-dependent predation models. Such models predict a positive correlation between numbers of predators and numbers of their prey, such that an increase in basal resources should cause an increase in herbivores and predators (a strictly “bottom-up” effect, see Arditi et al. 1991). One explanation for these data is that while belowground carbon input in the highN soil increased in response to elevated CO2, resource quality decreased, preventing strong trophic responses by soil organisms to increased plant biomass. In fact, tissue N concentrations were significantly lower for plants grown under elevated CO2 for both soil types (Zak et al. 2000a). This result may explain why plant-feeding nematodes did not respond significantly to elevated CO2 in the high-N soil, despite signifi-
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cant increases in fine root biomass and turnover in the high-N soil. If this is true, however, then why were plant-feeding nematodes more abundant under elevated CO2 in the low-N soil? Furthermore, what caused the increase in predaceous/omnivorous nematodes in response to elevated CO2 in the high-N soil if neither plant-feeding nor bacteria-feeding nematodes increased? A potential answer to these questions is that under elevated CO2 in both soils the soil fauna responded to increased belowground carbon input by aspen roots in the manner of a trophic cascade (sensu Carpenter et al. 1985; Carpenter & Kitchell 1993). According to this explanation, a small increase in root production in low-N soil under twice-ambient CO2 was balanced by increased numbers of (and root consumption by) plant-feeding nematodes (the most abundant family, Trichodoridae), so that we did not observe an increase in root standing biomass. However, the total resource base was not large enough to impact higher trophic levels (predaceous/omnivorous nematodes). In the high-N soil, a larger increase in root production under elevated CO2 was sufficient to support a larger food web such that increases were seen in higher trophic levels (predaceous/omnivorous nematodes), which suppressed the middle trophic levels (bacteria-feeders and plant-feeders), allowing us to observe an increase at the lowest trophic level (increased root biomass). Such a response of predaceous nematodes to increased availability of their prey has been observed previously (e.g., Wardle et al. 1995); however, since a time lag in this response is likely, sequential sampling would probably be necessary to confirm such a strong trophic link. Furthermore, without sequential sampling it is impossible to tell whether low numbers of a nematode group indicate low reproduction of that group, or high reproduction and high mortality. In summary, though these data do not demonstrate that a trophic cascade occurred in response to elevated CO2, they are consistent with this hypothesis. Most models of food web response to increased basal resources, including both trophic cascade models (Carpenter et al. 1985; Carpenter & Kitchell 1993) and ratiodependent predation models (Arditi et al. 1991), predict that the total biomass of the organisms above the basal resource will be greater. In the high-N soil, we observed statistically significant increases in the predaceous/omnivorous nematodes, and no statistically significant changes in the other trophic groups. Since predaceous/omnivorous nematodes are usually much larger than bacteria-feeding and fungus-feeding nematodes (e.g., Yeates 1973), and as large or larger than most plant-feeding nematodes, total nematode biomass probably increased in the high-N soil in response to elevated CO2. If soil food webs do respond to increased belowground production under elevated CO2 by increasing in biomass, then they may provide some degree of storage for carbon. While evenness was significantly lower under twice-ambient CO2 in the low-N soil, responses of nematode community structure to twice-ambient CO2 were generally stronger in high than in low-N soil. For example, in high-N soil, the number of abundant taxa was significantly smaller for all nematodes and the number of very abundant taxa was significantly smaller for plant-feeders in the twice-ambient CO2 treatment (Table 2). Because the total number of taxa was not different between CO2 treatments, the nematode community had relatively fewer common and relatively more rare taxa under twice-ambient CO2 than under ambient CO2. Most previous studies examining responses of soil nematodes to increased root production resulting from experimentally elevated atmospheric CO2 have reported increased total densities (Yeates & Orchard 1993; Runion et al. 1994; Klironomos et al.
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1996; Yeates et al. 1997), while one observed no changes in soil nematodes in response to elevated CO2 (Newton et al. 1995). Two previous studies (Yeates & Orchard 1993; Yeates et al. 1997), both in grazed pasture plant communities, identified the taxonomic identity of nematodes in an experiment with elevated CO2 (though Yeates and Orchard (1993) do not present abundance data for all taxa identified). One pattern common to those two studies and ours (high-N soil) is that the nematodes responding most consistently to elevated CO2 are the predaceous/omnivorous nematodes, which increased under elevated CO2 in all three studies. That the abundance of higher trophic levels increased under elevated CO2 in these two different systems is consistent with the hypothesis that soil food webs can respond to increased belowground carbon inputs under elevated CO2 by increasing in biomass. Another response observed only in the high-N soil in our study was a significantly greater Maturity Index for total nematodes (excluding plant-feeders) under twice-ambient compared with ambient CO2 (Table 2). Using the means for each taxon reported by Yeates et al. (1997) we calculated the same two nematode community structure indices calculated for our data (MI and PPI). Similarly to the high-N soil in our study, MI increased by approximately 20 % under elevated CO2 (from 1.18 to 1.45), while PPI changed little (1.44 to 1.35). Thus, in these two studies (ours and that reported by Yeates et al. 1997), the nematode community shifted in response to elevated CO2 to include a higher relative abundance of taxa having lower reproductive rate, lower colonization ability, and higher sensitivity to pollutants (according to Bongers 1990). A close examination of the nematode portion of the soil foodweb indicates that twice-ambient atmospheric CO2, most likely through increased root production by plants, was associated with significant changes in the soil nematode community that were not reflected in total density changes. While we were not able to examine other important members of the soil fauna (e.g., predaceous mites), soil nematodes are good indicators of the structure of the soil food web, and the results presented here suggest that responses of soil biota to climate change may be significant and may provide clues as to the fate of carbon under elevated CO2.
Acknowledgments We thank M. Byrny and F. Warner for advice, H. Ferris, M. W. Schwartz, and R. Venette for help with data analysis and interpretation, and Tony Sutterley and Richard Spray for help in the field. C. A. Brigham and A. Treonis provided helpful comments on earlier drafts of this manuscript. This research was supported by the National Institute for Global Environmental Change through the U.S. Department of Energy (Cooperative Agreement No. DE-FC0390ER61010), DOE Grant 93PER6166, and the University of Michigan Biological Station. Any opinions, findings, and conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the DOE.
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