ECOSYSTEMS
Ecosystems (2004) 7: 55– 62 DOI: 10.1007/s10021-003-0130-3
© 2004 Springer-Verlag
Earthworm Invasion, Fine-root Distributions, and Soil Respiration in North Temperate Forests Melany C. Fisk,1* Timothy J. Fahey,2 Peter M. Groffman,3 and Patrick J. Bohlen4 1 Department of Biology, Appalachian State University, Boone, NC 28608, USA; 2Department of Natural Resources, Cornell University, Ithaca, New York 14853, USA; 3Institute of Ecosystem Studies, Box AB, Millbrook, New York 12545, USA; 4Archbold Biological Station, Lake Placid, Florida 33852, USA
ABSTRACT The efflux of carbon from soils is a critical link between terrestrial ecosystems and the atmosphere. Current concerns about rising atmospheric carbon dioxide (CO2) concentrations highlight the need to better understand the dynamics of total soil respiration (TSR, sum of root and heterotroph respiration) in changing environments. We investigated the effects of exotic earthworm invasion on TSR, fine-root distributions, and aboveground litterfall flux in two sugar maple-dominated forests in two locations in New York State, USA. The Arnot Forest in central New York was harvested in the late 19th century and has no history of cultivation. Tompkins Farm in eastern New York regenerated following abandonment from cultivation approximately 75 years ago. Arnot had 20% higher total soil CO2 efflux (880 g C m⫺2year⫺1) than Tompkins (715 g C m⫺2year⫺1). The presence of earthworms had no influence on TSR at either location. However, fine-
root (⬍ 1 mm diameter) biomass in earthworm plots (350 g/m2) was significantly lower than in worm-free reference plots (440 g/m2) at Arnot. Fine-root nitrogen (N) concentrations were not influenced by earthworms, and total fine-root N content was significantly reduced in the presence of earthworms at Arnot. Our results indicate that the presence of exotic earthworms is not presently affecting net C emission from soil in these forests. They also suggest a change in root function in earthworm plots that is not associated with higher fine-root N concentration, but that increases efficiency of nutrient uptake and also may enhance the belowground supply of C for heterotroph metabolism.
INTRODUCTION
human or natural agents, with consequent feedbacks owing to greenhouse forcing. Empirical and theoretical study of local responses of soil C fluxes to such changes can contribute to our ability to predict these complex interactions. Soil respiration is one of the largest flux pathways of C in terrestrial ecosystems and the source of much of the atmospheric loading of carbon dioxide (CO2). Total soil respiration (TSR) represents the sum of autotrophic (roots and mycorrhizae) and heterotrophic respiration processes. A variety of interacting factors can contribute to changes in TSR,
Key words: soil respiration; fine roots; earthworms; forest floor.
Improving our understanding of soil carbon (C) dynamics is an important challenge to ecosystem scientists because of the potentially important role of soil C flux in the global C budget (Raich and Schlesinger 1992). Soil C dynamics may respond to changes in climate, biota, and site fertility caused by
Received 13 February 2002; accepted 11 December 2002; published online 12 January 2004. *Corresponding author; e-mail:
[email protected]
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including physical factors like soil temperature; chemical factors like soil organic matter quantity and quality; and biotic factors, including root biomass and activity and the composition and activity of soil heterotrophs. Understanding the interactions among these factors and their responses to humanaccelerated environmental change represents a major challenge to ecosystem scientists. The invasion of temperate forest soils by exotic earthworms often is accompanied by a reduction in soil C storage (Langmaid 1964; Lee 1985; Alban and Berry 1994) as a result of some combination of physical, chemical, and biological changes in the soil. Invasion of two northern hardwood forests in New York State by several European earthworm species resulted in differing responses of soil C storage: in three second-growth stands C storage was reduced by 25%, whereas no significant changes were observed in three postagricultural stands (Bohlen and others 2004b). These differing responses provided an interesting situation in which to compare and contrast the mechanisms contributing to changes in TSR resulting from the invasion of exotic earthworms. Previous studies have demonstrated that elimination of organic horizons (forest floor), mixing of organic material into mineral soil, and highly localized redistributions of organic matter in earthworm casts and burrows are all mechanisms that influence heterotroph activity and hence CO2 emission from soil (Scheu 1987; Haimi and Huhta 1990; Wolters and Joergensen 1992; Beare and others 1994; McLean and Parkinson 1997; Burtelow and others 1998; Li and others 2002). The effects of earthworm activity on root respiration and on total C allocation belowground have received less attention. Any effects of earthworms on site productivity could feed back to plant C allocation and hence C supply to heterotrophs. For instance, Pare´ and Bernier (1989) suggested that earthworm activity impacted sugar maple nutrition and health in Quebec. Such reductions in nutrient availability could stimulate increased plant C allocation belowground and also contribute to changes in soil CO2 emission. Our objectives were (a) to determine the influence of earthworms on TSR, and (b) to investigate effects of earthworms on aboveground and belowground C sources that would contribute to TSR. Based on previous observations of earthworm-induced changes in forest soil profiles and organic matter distribution (Langmaid 1964; Alban and Berry 1994), we hypothesized that the net effect of earthworms would be a reduction in TSR. To address these objectives and this hypothesis, we measured TSR in two north temperate forest ecosystems
with contrasting land-use histories (previously harvested but no cultivation, and postcultivation forest) that were both experiencing invasion by exotic earthworms. We quantified litterfall C flux to assess aboveground contributions to TSR. We also characterized the vertical distributions of fine and coarse roots to provide indications as to the effects of earthworms on belowground contributions to TSR.
METHODS Study Sites This study took place in two locations in New York State, USA: at Cornell University’s Arnot Forest in central New York and at the Institute of Ecosystem Studies’ Tompkins Farm in eastern New York. Arnot Forest is situated in the northern Allegheny Plateau physiographic province (42°16⬙N, 76°28⬙W). It was harvested over a century ago but was never cleared for agriculture (Volk and Fahey 1994). Dominant overstory species include sugar maple (Acer saccharum Marsh), red maple (Acer rubrum L.), beech (Fagus grandifolia Ehrh.), white ash (Fraxinus americana L.), basswood (Tilia americana L.), and hemlock (Tsuga canadensis L.). Annual rainfall at Arnot Forest is 100 cm, and temperatures average 22.0°C in the summer and ⫺4.0°C in the winter. Tompkins Farm is located on the northern extension of the Great Appalachian Valley of the Ridge and Valley physiographic province (41°50⬙N, 73°45⬙W). Tompkins Farm was previously under cultivation, and the forest regenerated after agricultural abandonment approximately 75 years ago. Sugar maple is the dominant overstory species. Tompkins Farm receives 98 cm rainfall annually and has a mean summer temperature of 21.8°C and winter temperature of ⫺2.4°C. In both locations, soils are primarily acidic (pH 4.2–5.0) Dystrochrepts with an organic horizon (forest floor) overlying mineral soil. The forest floor is better developed at Arnot Forest (average, 4 cm) than at Tompkins farm (average, 1.5 cm). Three replicate forest stands were chosen for study at each location. These stands were chosen after extensive surveying of the field sites and were discrete stands separated by clear changes in topography and by forest of varying overstory composition. At each of these forest stands, we established a pair of 20 ⫻ 20-m plots: a reference plot in which there was no evidence of earthworms (⬍ 2 individuals per square meter), and a worm plot in which earthworm activity was evident [⬎ 150 individuals/m2 (Bohlen and others 2004a)]. These paired plots were 50 –100 m apart at each site. The paired
Earthworm Invasion, Fine-root Distributions, and Soil Respiration plots that were chosen within each stand did not differ in soils, vegetation, or topography. Reference and worm plots generally were located at different distances from wet areas or streams that were probably earthworm refugia, but were in similar slope positions with similar vegetation. Earthworm plots at Arnot were dominated by Lumbricus rubellus, L. terrestris, and Octolasion tyrtaeum. Tompkins plots were dominated by L. terrestris (Bohlen and others 2004a).
Respiration Eight PVC collars (10-cm diameter and 6-cm height) were permanently placed in each plot for soil respiration measurement. Each collar was placed approximately 1 cm deep in the forest floor. Roots were not severed by placement of the collars. Collars were fixed securely in place by galvanized nails that were embedded in the bottom edge. A PP Systems infrared gas analyzer with a soil respiration chamber was used to quantify CO2 flux from PVC collars. Measurements were made approximately monthly from fall 1998 through summer of 2001. Soil temperature also was recorded at 5-cm depth. Total annual soil C efflux was estimated as the sum of mean monthly C efflux from March through November, plus estimated respiration of 16 g C m⫺2 mo⫺1 during the winter months. This estimate is based on winter measurements in northern hardwood forest at Hubbard Brook, New Hampshire (T. J. Fahey and P. M. Groffman unpublished data). It is our best estimate of winter fluxes, but may be a slight underestimate given climate differences between sites. To compare respiratory activity among the sites and between the presence or absence of earthworms, soil respiration data were fitted with an exponential model: Y ⫽ xe(kT), where Y ⫽ soil respiration (g C m⫺2 h⫺1) and T ⫽ temperature (°C). Q10 was estimated by the equation Q10 ⫽ e(10*k).
Root Mass and Nitrogen Six quantitative soil pits (15 ⫻ 15 ⫻ 12 cm) were excavated at random locations in each study plot. Material from each pit was divided into organic horizon (forest floor: Oi, Oe, and Oa horizons), and 0- to 3-cm, 3- to 6-cm, 6- to 9-cm, and 9- to 12-cm depth of mineral soil. In addition, four soil cores (5-cm diameter) were collected from the face of soil pits in each plot at 15-, 25-, and 35-cm depth. All roots were removed from each sample and divided into three size classes: less than 1-mm diameter, 1to 2-mm diameter, and larger than 2-mm diameter.
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Table 1. Soil Carbon (C) Efflux and Litterfall C Flux in Worm and Reference Plots at Arnot Forest and Tompkins Farm
Arnot Reference Worm Tompkins Reference Worm
Total Soil Respiration
Litterfall C Flux
900 (68.4) 859 (64.8)
218 (6.9) 235 (20.8)
738 (41.3) 690 (61.2)
245 (15.6) 252 (10.9)
Soil respiration was measured by a static chamber method, and mean monthly rates (averaged for 3 years: fall 1998 to fall 2001) were summed over 9 months (March through November). For December, January, and February, average values of 16 g C m⫺2 mo⫺1 were used (T. J. Fahey and P. M. Groffman unpublished data). Litterfall C flux is annual leaf plus fine (⬍ 2 mm diam) litterfall, averaged over 3 years. All values are in g C m⫺2 year⫺1, standard errors are in parentheses (n ⫽ 3 plots).
Roots were cleaned, dried at 60°C, and weighed. Roots less than 1 mm in diameter were ground and analyzed for C and nitrogen (N) content by using a Carlo Erba CHN analyzer (Milan, Italy).
Litterfall Annual litterfall was collected in baskets, 0.1 m2 at Arnot and 0.2 m2 at Tompkins Farm. Eight baskets were placed randomly within each plot. Litter was collected in August and again in November, following the completion of leaf litterfall. Litter was sorted by species, dried at 60°C, and weighed.
Statistical Analyses Minitab General Linear Model was used to test effects of earthworms and location (Arnot or Tompkins) on soil respiration. This was a repeated measures design with month sampled as the withinsubjects factor. Three-way analysis of variance (ANOVA) was used to test effects of earthworm presence (earthworm/reference), location, and horizon (depth) on fine-root biomass. Two-way ANOVA was used to test earthworm and location effects on litterfall C flux.
RESULTS The presence of earthworms had no influence on TSR at either Arnot Forest or Tompkins Farm (Table 1 and Figure 1). TSR was higher at Arnot than Tompkins (F ⫽ 7.5 and P ⫽ 0.02), and also differed over time (F ⫽ 73.0 and P ⬍ 0.001) (Figure 1). TSR peaked around 150 g C m⫺2 mo⫺1 in late summer at both Arnot and Tompkins (Figure 1). Higher TSR
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Figure 1. Mean monthly soil C efflux over three years (fall 1998 –fall 2001) from reference and earthworm plots in two hardwood forest ecosystems in New York. Bars are standard errors of the mean, n ⫽ 3 replicate plots. Respiration was not measured in December, January or February.
at Arnot resulted from a more rapid increase in respiration rates in the spring months and a slower decline in the autumn, compared with Tompkins Farm (Q10 ⫽ 2.4 at Arnot and 3.7 at Tompkins). There were no differences in the relationship between TSR and temperature of reference and earthworm plots for either location (Figure 2). There was a slight effect of earthworms on soil temperature: Li and others (2002) reported 1°–1.5°C higher soil temperature in earthworm plots at the Arnot sites over the growing season of 2000. Fine-root (⬍ 1-mm diameter) mass in the forest floor plus the surface 12 cm of mineral soil was higher in reference plots at Arnot (F ⫽ 7.4 and P ⫽ 0.008) and was higher at Arnot than Tompkins (F ⫽ 13.9 and P ⫽ 0.0004). Of total fine-root biomass, 85%–90% occurred in the surface 12 cm in all plots; no effect of earthworms was found for fineroot biomass from 12- to 35-cm depth. Roots larger than 1-mm diameter were not influenced by the presence of earthworms in the surface 12-cm or in deeper soils, and were far more abundant at Arnot (Table 2). Earthworms significantly altered the vertical distribution of fine roots in the surface 12 cm at Arnot
Figure 2. Relationship between soil C efflux and soil temperature at 5 cm depth in earthworm and reference plots (fall 1998 –fall 2001). Each point is the mean of 8 chambers per plot per sample date.
Table 2. Root Biomass in Forest Floor and the Surface 35 cm of Mineral Soil in Reference and Worm-invaded Plots at Arnot Forest and Tompkins Farm, July 1998 Root Diameter Class
Arnot Reference Worm Tompkins Reference Worm
⬍ 1 mm
1–2 mm
2–10 mm
444 (66.1) 347 (49.4)
165 (26.7) 176 (29.6)
581 (171.1) 540 (111.0)
321 (20.7) 317 (8.4)
103 (5.2) 120 (33.4)
120 (33.4) 239 (65.4)
Standard errors of the mean are in parentheses (n ⫽ 3 plots).
(treatment by depth interaction, F ⫽ 14.5 and P ⫽ 0.001) (Figure 3). The majority (50%) of fine-root biomass occurred in the thick (average 4 cm) forest floor horizon of reference plots at Arnot. Earthworms had eliminated the forest floor, and the
Earthworm Invasion, Fine-root Distributions, and Soil Respiration
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worm plots at Arnot (F ⫽ 35.80 and P ⬍ 0.001) but not at Tompkins (F ⫽ 0.14 and P ⫽ 0.71) (Table 3). Litterfall C flux did not differ between reference and earthworm plots, and was slightly higher at Tompkins than Arnot (Table 1). Litterfall C was 24%–27% of TSR at Arnot, compared with 33%– 36% of TSR at Tompkins.
DISCUSSION
Figure 3. Distribution of fine root biomass in the forest floor (FF) and surface 12 cm of soil in earthworm-invaded and reference (no-worm) plots, July 1998. Bars are standard errors of the mean, n ⫽ 3 replicate plots. Stars indicate significant differences between reference and earthworm plots. *p ⬍ 0.05 ** p ⬍ 0.01*** p ⬍ 0.001
compensatory shift in fine-root biomass to upper mineral horizons resulted in much higher root density there in earthworm plots (Figure 3). The thin forest floor horizon (almost all Oi) at Tompkins Farm contained almost no roots in either earthworm or reference plots, and changes in the vertical distribution of fine roots were small relative to Arnot. Nevertheless, the treatment by depth interaction was significant at Tompkins (F ⫽ 2.9 and P ⫽ 0.03). Nitrogen concentrations of fine roots (⬍ 1-mm diameter) did not differ between earthworm and reference plots at either Arnot Forest (F ⫽ 0.02 and P ⫽ 0.88) or Tompkins Farm (F ⫽ 2.16 and P ⫽ 0.16) (Table 3). Nitrogen concentrations declined steadily and significantly with depth at Arnot (F ⫽ 16.01 and P ⬍ 0.001) but not at Tompkins (F ⫽ 2.15 and P ⫽ 0.13), where fine-root N concentrations were higher overall. Total N content of fine roots in the surface 12 cm was greater in reference than
The invasion of temperate forests by earthworms can have profound effects on physical and chemical characteristics of soil (Langmaid 1964; Lee 1985; Alban and Berry 1994), depending on the species composition of earthworms (Scheu and others 2002) and on site history and preinvasion soil conditions (Bohlen and others 2004b). In this study, and as noted in other papers in this special feature of Ecosystems, the mixing of the organic horizon into mineral soil was the most obvious effect of earthworms, and corresponded to a reduction in the mass and change in the vertical distribution of organic carbon in the soil profile at the Arnot Forest site (Bohlen and others 2004b), which bears no legacy of agricultural land use. No response in soil C was observed at the postagricultural Tompkins Farm site. In the present study, it was surprising that neither of these temperate forest ecosystems exhibited an effect of earthworms on TSR. Despite the obvious effects of earthworms on the surface soil environment, where microbial and root activity are concentrated, our results indicate that the presence of exotic earthworms is not presently affecting net C emission from soil in the forests that we studied. The absence of an earthworm effect on TSR at Tompkins Farm is consistent with other data reported in this special feature (Bohlen and others 2004b; Groffman and others 2004). In contrast, the lack of worm effects on TSR at the Arnot Forest site is more intriguing, given clear changes in soil organic matter quantity and distribution (Bohlen and others 2004b) and increased soil heterotrophic activity (Groffman and others 2004; Li and others 2002) in response to earthworms. However, we also observed significantly lower fine-root biomass in the earthworm-invaded than the reference plots at Arnot Forest (Table 2). Hence, the simplest explanation for the lack of a TSR response at Arnot would seem to be the offsetting effects of increased heterotrophic respiration and decreased root respiration, assuming there was no change in the specific respiration rate of roots in response to earthworms. Direct evidence for this simple interpretation of the absence of TSR response at Arnot Forest is
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Table 3. Nitrogen Concentration (%) and Total Content (g N/m2) in Fine Roots (⬍ 1 mm Diameter) in Forest Floor and the Surface 12 cm of Mineral Soil in Reference and Worm-invaded Plots at Arnot Forest and Tompkins Farm, July 1998 Mineral Soil Depth Nitrogen Concentration (%) Arnot Reference Worm Tompkins Reference Worm Nitrogen Content (g/m2) Arnot Reference Worm Tomkins Reference Worm
Forest Floor
0 –3 cm
3– 6 cm
6 –9 cm
9 –12 cm
Total to 12 cm
1.61 (0.207) NA
1.55 (0.107) 1.57 (0.110)
1.35 (0.059) 1.28 (0.099)
1.13 (0.056) 1.16 (0.054)
1.05 (0.052) 1.09 (0.031)
NA NA
2.01 (0.108) 2.13 (0.194)
1.73 (0.149) 1.87 (0.112)
1.62 (0/104) 1.86 (0.122)
1.74 (0.198) 1.81 (0.186)
3.44 (0.534) NA
0.84 (0.107) 2.03 (0.196)
0.54 (0.040) 0.76 (0.153)
0.38 (0.023) 0.61 (0.050)
0.32 (0.055) 0.36 (0.043)
5.52 (0.691) 3.76 (0.432)
NA NA
2.46 (0.250) 2.14 (0.033)
1.17 (0.196) 1.20 (0.148)
0.63 (0.069) 0.80 (0.093)
0.64 (0.092) 0.60 (0.087)
4.90 (0.580) 4.74 (0.272)
Standard errors of the mean are in parentheses (n ⫽ 3 plots). NA, not applicable because no roots were present.
lacking, and additional complications need to be considered. In particular, nutrient uptake in the earthworm plots remained similar to or higher than that in the reference plots as indicated by N and P flux in aboveground litterfall (Sua´ rez and others 2004), suggesting that the smaller root systems in the earthworm plots were more active in accessing soil nutrients. The higher respiratory cost of a higher specific root uptake rate might be expected to offset the hypothesized effect of lower fine-root biomass on total root respiration. Also, because we observed no effect of earthworms on aboveground litterfall, increased soil heterotrophic activity must have been stimulated by larger belowground sources of carbon. These sources could include mineral soil organic carbon, increased root mortality (that is, higher root turnover rates), or increased root exudation, rhizodeposition, and allocation to mycorrhizal fungi. Distinguishing among these possible responses was beyond the scope of the present study, but some of our observations and literature interpretations provide additional insights into this intriguing result. We observed significant differences in TSR between the two study locations even though the sites were comparable in terms of macroclimate, forest composition, and soil type. We cannot conclusively evaluate what factors are responsible for TSR differences between these sites, but the difference in TSR is consistent with the effects of contrasting site histories. Whereas Arnot Forest was logged more
than a century ago but never cultivated, the Tompkins Farm site is a postagricultural forest that has been recovering for approximately 75 years. Two consequent differences in soil C dynamics could contribute to the much lower TSR of the postagricultural stands. First, it is likely that soil C was accumulating in the postagricultural stands; for example, Gaudinski and others (2000) estimated soil C accumulation of 10 –30 g C m⫺2year⫺1 in 100year-old postagricultural hardwood forests in Massachusetts. Second, fine and coarse root biomass, and total fine-root N content, were markedly lower in the postagricultural stands (Table 2), and consequently the contribution of root respiration to TSR may have been lower. However, fine-root N concentrations were much higher at Tompkins Farm (Table 3), and specific root respiration rate in sugar maple is positively correlated with root N concentration (Zogg and others 1996; Pregitzer and others 1998). The lower root biomass (especially coarse roots) in the postagricultural stands probably resulted in part from the younger age of those stands (75 years) compared with the second-growth stands at Arnot Forest (older than 100 years). In addition, soil N availability appeared to be higher in the postagricultural stands (Groffman and others 2004), consistent with previous studies that have indicated that agricultural legacy can significantly influence soil N status even as much as a century after abandonment (Compton and Boone 2000). Higher N availability can cause either increases or
Earthworm Invasion, Fine-root Distributions, and Soil Respiration decreases in belowground C allocation (Keyes and Grier 1981; Hendricks and others 1993; Haynes and Gower 1995; Burton and others 2000; Nadelhoffer 2000), depending on the responses of individual tree species and the variation in site conditions (Burton and others 2000). Perhaps lower TSR at Tompkins Farm is explained by postagricultural reduction in forest N limitation, but additional research is needed to test this hypothesis. The present study provides additional evidence concerning the C dynamics of earthworm-invaded forest soils and raises the question of the likely sources of increased belowground C supply to soil heterotrophs. Mixing of the thick forest floor into the upper mineral soil during the initial stage of earthworm invasion at the Arnot Forest site was accompanied by a large net reduction in total soil C storage (Bohlen and others 2004b). The magnitude of this reduction was relatively large (1550 g C/m2) compared with annual TSR at this site (900 g C/m2year). At the time of the present study, the forest floor was essentially gone at all the earthworm plots, and the upper 6 cm of mineral soil contained significantly more C than did corresponding layers in the reference plots. Heterotrophic activity in these C-enriched mineral soil layers was clearly stimulated by earthworm mixing (Groffman and others 2004; Li and others 2002). But, in addition, total soil heterotrophic respiration throughout the soil profile (that is, even including forest floor in reference plots) was stimulated by earthworm activity (Groffman and others 2004), whereas both TSR and aboveground litterfall remained unchanged. Hence, either mineral soil C storage continues to decline or the root-associated supply of C to heterotrophs has increased. Although fine-root biomass has declined in the earthworm plots, increased turnover rates of fine roots or increased root exudation, rhizodeposition, and allocation to mycorrhizal fungi could result in higher belowground C inputs. Fine-root dynamics and function responded to the invasion of earthworms at the Arnot Forest site, but, lacking direct measurements, we can only speculate on the exact nature of these responses. First, root dynamics differ markedly between forest floor and mineral soil horizons in northern temperate forests (Fahey and Hughes 1994; Hendrick and Pregitzer 1996), and the elimination of the forest floor by worms resulted in a profound alteration of the rooting medium, as half of fine-root biomass was located in the forest floor in reference plots. Second, despite the significant reduction in total fine-root biomass in the earthworm plots, aboveground litterfall N and P flux did not decline,
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suggesting that uptake per unit root biomass increased. Lawrence and others (2003) observed much lower mycorrhizal infection of sugar maple roots in earthworm than reference plots at Arnot Forest, as well as indications of higher stress to mycorrhizae. They suggested that earthworm mixing of soil could disrupt mycorrhizae and increase mycorrhizal turnover. Hence, we hypothesize that root and mycorrhizal turnover, and possibly also rhizodeposition and exudation, increased in response to earthworm invasion resulting in a stimulation of root and rhizosphere activity, C supply to heterotrophs, and nutrient uptake rates by younger (on average) root systems (Bouma and others 2001). These observations, taken together with the lack of response of fine-root N concentrations, suggest that specific root activity in earthworm-invaded soils involves mechanisms that are different from those noted for other northern temperate forests where fine-root N concentration has been shown to be strongly related to root function (Zogg and others 1996; Pregitzer and others 1998). In summary, we found no influence of earthworms on the total CO2 efflux from soil in two northern temperate forests. In our postagricultural site (Tompkins), this was consistent with other indicators of C transformations (Bohlen and others 2004b; Groffman and others 2004) and was also consistent with a lack of earthworm influence on fine-root biomass and distributions. The relative abundance of available N may have more important effects on patterns of TSR in this forest site. In our second-growth forest ecosystem (Arnot), earthworms had marked effects on fine-root biomass and distribution in surface soil horizons, but no influence on TSR. Soil heterotroph activity was enhanced by earthworms at this site, and detailed study of fine-root turnover and activity would aid our understanding of how earthworms influence different soil processes to produce no net effect on C efflux.
ACKNOWLEDGEMENTS We thank Suzanne Bartholf, Kevin Blinkoff, Dana Briel, Jena Ferrarese, Doug Krisch, and Suzanne Wapner for assistance in the field and laboratory. This research was supported by a grant from the National Science Foundation (DEB-9726869).
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