Exotic Earthworms & Northern Temperate Forests

Earthworms are an invasive species in northern temperate forests. European in origin, they arrived in the US with settlers during the 1800's. Invasive non-native species are of concern to ecologists due to their ability to alter the environments they invade. This project tests the hypothesis that exotic earthworm invasions will impact nutrient retention and uptake in forests.

Project Summary

In this Project

Project Summary


Introduction

This project tested the global hypothesis that earthworm invasion of north temperate forests is having large consequences for nutrient retention and uptake in these ecosystems. We addressed this hypothesis with a two-pronged approach. The first approach involved controlled introduction of earthworms into forest plots that lack earthworm populations. The second approach involved comparing forest stands already invaded by earthworms with adjacent stands lacking earthworms, viewing these stands as endpoints along a gradient of earthworm invasion. The "introduction plots" were supposed to provide insight into the transition that occurs immediately following earthworm invasion. However, we were not successful in inducing colonization of our introduction plots. Questions about the transition phase of invasion were therefore investigated by analyzing transition zones between worm-colonized and reference areas.

Methods

The experiments took place in forests at two different geographic locations, one in eastern (Tompkins Farm, near Millbrook) and the other in central (Arnot Forest, near Ithaca) New York. We documented the obvious and expected decline in forest floor depth and redistribution of surface organic matter in the soil profile following earthworm invasion. We also determined how these changes affected the ability of these forests to retain exogenous N and provide nutrients to support plant growth. Retention of atmospheric N was assessed by tracing the movement of small additions of 15N and Br- through the top 30 cm of the soil profile. We measured pools of available N and P, and the biomass, distribution and function of roots. We analyzed litter and foliar chemistry to determine whether the presence of earthworms affected foliar nutrient content and ratios. Hydrologic nutrient losses were measured using zero-tension lysimeters and gaseous N losses were measured using soil cores.

After extensive field surveys we located three replicate forest stands at both the Arnot and Tompkins Farm sites. In each stand, we established three plots; a 20 m x 20 m plot that had been colonized by earthworms, a 20 m x 20 m non-invaded "reference" plot and a 5 m x 5 m "introduction" plot. The introduction plots (which were not successful) were areas not previously colonized, to which we added earthworms in both 1999 and 2000. Given this lack of success, factors that control the local distribution of exotic earthworms in northern temperate forests were examined by studying the composition of exotic earthworm communities along transects that ran across earthworm invasion fronts at the Arnot site. This work was done to provide information on the "transition phase" of earthworm invasion that we had hoped to investigate with our introduction plots. We also assessed the influence of soil moisture and the effects of tree species in the distribution of exotic earthworms by examining earthworm populations in pure plantations of sugar maple, spruce, black locust, ash, white pine and red pine located at the Turkey Hill experimental area near Ithaca.

In each of the large plots, zero-tension lysimeters were installed at 10 and 40 cm depth by excavating soil pits and installing lysimeters beneath undisturbed soil profiles. Tension lysimeters were installed at the same depths in all plots. Soil respiration flux chambers and litterfall collectors were also installed in each plot.

As the lysimeter pits were dug, soil samples were taken at several depths to quantify the effects of existing earthworm invasion on soil profile characteristics. Samples were taken of forest floor and of mineral soil at 3 cm increments to 12 cm depth and at 15, 25 and 35 cm depth.

  1. Soil profile samples were analyzed for fine root biomass, total C and N and 13C and 15N content. Soil P fractions (total, resin extractable, bicarbonate extractable, hydroxide extractable, hydrochloric acid extractable, occluded) were measured on all mineral soil samples.
  2. Soil respiration. Measured in situ monthly (but not during winter) with a PP systems infrared gas analyzer.
  3. Soil solution chemistry. Both zero-tension and tension lysimeters were sampled monthly during summer and fall, weekly during spring, and not during winter from fall 1998 - fall 2000. Samples were analyzed for inorganic and organic N and P.
  4. The influence of worm presence and land-use history on the ability of forest soils to retain nitrate was studied by installing a separate set of lysimeters in two 2 m2 subplots within each of the previously established worm and no-worm plots. We added a combination of 15NO3- and Br- in tracer quantities to one subplot within each worm and no-worm plot and collected lysimeter leachate at daily and then weekly intervals to track the movement of 15NO3- and Br- out of the soil profile. 
  5. In situ net N mineralization and nitrification. Measured using an intact core method (Robertson et al. 1999) on a monthly basis from fall 1998 - fall 2000, except overwinter, when one multi-month incubation was done.
  6. Denitrification. Measured using an intact core method (Groffman et al. 1999) on all samples processed for in situ N mineralization and nitrification.
  7. Litterfall. Collected in fall 1998, 1999 and 2000. Analyzed for total C, N and P content.
  8. Foliar chemistry. Collected in summer 1998, 1999 and 2000. Analyzed for total C, N and P content.
  9. We used a root uptake bioassay as an integrated measure of soil nutrient supplying capacity. The assay, which involves measuring the uptake of isotopically labelled nutrients by excised roots, is based on the finding that nutrient uptake rate in the assay is related to soil nutrient availability (Dighton et al. 1993). 
  10. Effects of exotic earthworms in the rates of litter disappearance were investigated using litter boxes placed in worm, transition and no-worm areas at the Arnot Forest site. We compared the disappearance of sugar maple and red oak leaves in sites dominated by the anecic species i, and in sites dominated by the epigeicL.rubellus
  11. Microbial biomass. Measured by chloroform fumigation three times per year (spring, summer, fall) from fall 1998 - fall 2000. An REU student (Kristin Strassner) measured fungal and bacterial biomass using substrate induced respiration with selective inhibitors and direct count methods in summer 1999. A visiting scientist, Xuyong Li did detailed studies on seasonal variation in the metabolic state of microbial biomass in spring and summer 2000.
  12. Earthworm/salamander interactions. An REU student (Evan Grant) examined relationships between salamander and earthworm numbers during fall 1999.
  13. Mycorrhizae. An REU student (Beth Lawrence) compared colonization rates and mycorrhizal fungal structures (vesicles and hyphal coils) in different soil horizons in earthworm-invaded and reference plots, and quantified a seasonal cycle of mycorrhizal colonization of sugar maple roots.


Results

Our results led to the development of a conceptual model of the effect of earthworm invasions on forest ecosystems (Figure 1). The model begins with the idea that the invasions are catalyzed by human introduction associated with fishing, commerce in soil and plant materials and cultivation and commerce of earthworms themselves, e.g. vermicomposting (Hendrix and Bohlen 2002). Our results suggest that persistence and spread of earthworms depends on site factors such as vegetation type, which influences food quality, and topography, which influences soil moisture (Bohlen et al. 2004a,b, Suárez et al. 2006, in press).

Figure 1.  Factors that influence earthworm invasions, the three main categories by which invasion influences ecological systems, and the consequences of invasion for ecosystem processes and ecological communities.  From Bohlen et al. (2004a).Figure 1. Factors that influence earthworm invasions, the three main categories by which invasion influences ecological systems, and the consequences of invasion for ecosystem processes and ecological communities. From Bohlen et al. (2004a).

Earthworms influence ecosystem nutrient cycling processes by modifying soil structure and redistributing organic matter as a by-product of their feeding and burrowing activities (Suárez et al., submitted - d, Figure 1). These activities vary with different earthworm species; some reside mainly in the upper organic layer (epigeic species), whereas others mix organic and mineral layers together (endogeic species). Still other species, such as L. terrestris, the common nightcrawler, form nearly vertical permanent burrows up to 1-2 m deep and incorporate litter into the soil and bring mineral soil from different depths to the surface (anecic species). However, our results suggest that earthworm effects on soil C depend more strongly on land use history than on earthworm species.

At a site with no history of cultivation and a thick (3 - 5 cm) forest floor (Arnot Forest), earthworm invasion reduced soil C in the top 12 cm of the soil profile by 28%, while at a site with a history of cultivation and thin forest floors (Tompkins Farm), there was no difference in soil C between invaded and reference sites (Figure 2). Our results imply that while northern forests are thought to be important global C sinks (McKane et al. 1997, Hobbie et al. 2002, Lal 2004), earthworm invasions may turn them into C sources. Our Arnot Forest site has likely been a source of C to the atmosphere as earthworms have invaded over the past 20 - 30 years. The Tompkins Farm site should be accumulating C as it recovers from past agricultural land use, but we suggest that earthworm invasion has greatly reduced the potential of soils at this site to sequester C. It is likely that a large proportion of C was lost at Arnot in the initial years of earthworm invasion (Alban and Berry 1994). Now the critical need is to understand whether earthworm-invaded sites continue to have a reduced capacity for C accumulation over the longer- term. Sustained higher soil C loss is suggested by higher microbial respiration rates that we observed at both the Arnot and Tompkins Farm sites (Groffman et al. 2004, Li et al. 2002, Fisk et al. 2004). Clearly there is a need for further research to evaluate the effects of earthworm invasion on soil C processing and storage and to quantify the importance of invasion relative to other regional scale regulators of storage such as soil texture, topography and land use history.

 Figure 2. Soil carbon in earthworm invaded and reference sites with (Tompkins Farm) and without (Arnot Forest) a history of cultivation. At Arnot Forest, earthworms eliminated the forest floor and reduced total soil C by 28% over the top 12 cm of the soil profile while there was no net loss of C from the soil profile at Tomkins Farm. From Bohlen et al. (2004c).

Earthworms reduced total soil profile fine root biomass, respiration and N content (Fisk et al. 2004) and infection rates of mycorrhizae on sugar maple (Lawrence et al. 2003). Sugar maple roots in earthworm-invaded plots had higher amounts of vesicles (indicate stress) and lower amounts of hyphal coils (important for nutrient transfer). These results suggest that earthworms reduce both the amount and function of fine roots in these forests.

The effects of earthworm invasion on N cycling and retention are more complex than the effects on C transformations. Earthworms have been shown to increase N mineralization and leaching of N from forest soils in lab or microcosm studies (Haimi and Huhta 1990, Scheu and Parkinson 1994, Burtelow et al. 1998, Tiunov and Scheu 2004). However, earthworm invasion did not lead to significant declines in total soil N or to increases in N leaching from surface soil in our plots (Bohlen et al. 2004c). The lack of increase in leaching was particularly surprising given the lower soil C:N ratio in invaded plots compared to uninvaded plots. Many studies have found this ratio to be a strong predictor of N loss (Gunderson et al. 1998, Dise et al. 1998, Lovett et al. 2002, Ross et al. 2004).

One possible mechanism for N retention following earthworm invasion is an increase in total microbial biomass, which may act as a strong immobilization sink for available N in C-rich soils (Groffman et al. 2004). We observed an increase in microbial biomass following invasion at our sites, likely because earthworms moved C processing into the mineral soil, which has a higher preservation capacity for microbial biomass than the forest floor. This reasoning was supported by results from our root uptake bioassays that found that plants were more N limited in earthworm-colonized plots than in reference plots at both the Arnot and Tompkins sites (Figure 3). These results suggest that while earthworm invasion may be reducing forest soil C storage across the northeastern U.S., it does not appear to be reducing N retention. These results will be confirmed by analysis of our 15N:Br- tracer experiments, which is still ongoing.

 

Figure 3. Uptake of ammonium (NH4+) and nitrate (NO3-) by excised roots in earthworm-colonized and reference plots with (Tompkins Farm) and without (Arnot Forest) a history of cultivation. Higher uptake indicates that plants are more limited by N. Tuininga et al. (unpublished data).

In addition to altering C and N processing, earthworms appear to have complex effects on soil P pools that vary with earthworm species (Suárez et al. 2004). Earthworm-invaded plots dominated by L. terrestris had significantly more total P (between 0 and 12 cm) than their corresponding reference plots, while plots dominated by the epigeic L. rubellus, showed significantly less total P than their reference plots. The worm plots that had higher amounts of total P had a proportionally higher amount of unavailable P fixed in Al or Fe hydroxides or primary minerals. The increased amount of unavailable P forms in earthworm-colonized plots suggests that the deep burrowing activity of L. terrestris has mobilized unweathered soil particles from deeper layers of the soil, increasing the stocks of total P. In contrast, the decrease in total P that we observed in plots dominated by L. rubellus could be due to stimulation of rates of P cycling in the soil by the surface activity of this species.

Northern forest ecosystems are being subjected to multiple environmental stresses including continued atmospheric deposition and potentially rapid environmental change. Our results indicate that the effect of these changes on forest nutrient cycles need to be interpreted in light of potential changes in soil biota, in particular invasion of these forests by exotic earthworms. Significant shifts in the distribution of species and communities in forest ecosystems in North America are likely to occur in response to changing climate and land use patterns. Such changes in the biodiversity of these forest ecosystems, including the continued spread and introduction of exotic species are likely to result in important biotic feedbacks on nutrient dynamics and ecological processes. Changing climatic conditions may facilitate the northward spread of different earthworm species by increasing their rates of survival, fecundity or dispersal. Our results suggest that such an accelerated expansion of earthworm populations, due to changing climate, altered land use or other human activities, could increase the potential for soil C loss, significantly change the distribution and quality of soil organic matter, and significantly alter soil C, N and P cycles in forest ecosystems at regional scales.

Literature Cited:

Alban, D. H., and E. C. Berry. 1994. Effects of earthworm invasion on morphology, carbon and nitrogen of a forest soil. Applied Soil Ecology 1:243-49.

Bohlen, P. J., P. M. Groffman, T. J. Fahey and M. C. Fisk. 2004a. Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1-13.

Bohlen, P. J., S. Scheu, C. M. Hale, M. A. McLean, S. Migge, P. M. Groffman and D. Parkinson. 2004b. Invasive earthworms as agents of change in north temperate forests. Frontiers in Ecology and the Environment 8:427-435.

Bohlen P. J., P. M. Groffman, T. J. Fahey and M. C. Fisk. 2004c. Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems 7:13-29.

Burtelow, A. E., P. J. Bohlen and P. M. Groffman. 1998. Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeastern United States. Applied Soil Ecology 9:197-202.

Dighton, J., J. M. Poskitt, and T. K. Brown. 1993. Phosphate influx into ectomycorrhizal and saprotrophic fungal hyphae in relation to phosphate supply; a potential method for selection of efficient mycorrhizal species. Mycological Research 97: 355?358.

Dise, N. B., E. Matzner and M. Forsius. 1998. Evaluation of organic horizon C:N ratio as an indicator of nitrate leaching in conifer forests across Europe. Environmental Pollution 102:453-456.

Fisk, M.C., T.J. Fahey, P.M. Groffman and P.J. Bohlen. 2004. Earthworm invasion, fine-root distributions, and soil respiration in north temperate forests. Ecosystems 7:55-62.

Groffman, P. M., P. J. Bohlen, M. C. Fisk and T. J. Fahey. 2004. Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems 7:45-54.

Groffman, P.M., E. Holland, D.D. Myrold, G.P. Robertson and X. Zou. 1999. Denitrification. Pages 272-288 In Standard Soil Methods for Long Term Ecological Research (G.P. Robertson, C.S. Bledsoe, D.C. Coleman and P. Sollins, editors). Oxford University Press, New York.

Gunderson, P., I. Callensen and W. deVries. 1998. Leaching in forest ecosystems is related to forest floor C/N ratios. Environmental Pollution 102:403-407.

Haimi, J., and V. Huhta. 1990. Effects of earthworms on decomposition processes in raw humus forest soil: a microcosm study. Biology & Fertility of Soils 10:178-183.

Hendrix, P., and P. J. Bohlen. 2002. Exotic earthworm invasions in North America: Ecological and Policy implications. Bioscience 52:801-811.

Hobbie, S. E., K. J. Nadelhoffer and P. Hogberg. 2002. A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant and Soil 242:163-70.

Lal, R. 2004. Soil carbon sequestration impacts on global climate change and food security. Science 304:1623-1627.

Lawrence, B., M. C. Fisk, T. J. Fahey and E. Suàrez. 2003. Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytologist 157:145-153.

Li, X., M. C. Fisk, T. J. Fahey and P. J. Bohlen. 2002. Influence of earthworm invasion on soil microbial biomass and activity in a northern hardwood forest. Soil Biology and Biochemistry 34:1929-1937.

Lovett, G. M., K. C. Weathers and M. A. Arthur. 2002. Control of nitrogen loss from forested watersheds by soil carbon:nitrogen ratio and tree species composition. Ecosystems 5:712-718.

McKane, R. B., E. B. Rastetter, G. R. Shaver, et al. 1997. Reconstruction and analysis of historical changes in carbon storage in arctic tundra. Ecology 78:1188-98.

Robertson, G.P., D. Wedin, P.M. Groffman, J.M. Blair, E.A. Holland, K.J. Nadelhoffer and D. Harris. 1999. Soil carbon and nitrogen availability: Nitrogen mineralization, nitrification and carbon turnover. Pages 258-271. In Standard Soil Methods for Long Term Ecological Research (G.P. Robertson, C.S. Bledsoe, D.C. Coleman and P. Sollins, editors). Oxford University Press, New York.

Ross, D. S., G. B. Lawrence and G. Fredriksen. 2004. Mineralization and nitrification patterns at eight northeastern forested research sites. Forest Ecology and Management 188:317-335.

Scheu, S., and D. Parkinson. 1994. Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains - laboratory studies. Applied Soil Ecology 1:113-25.

Suàrez, E., T.J. Fahey, P.M. Groffman, P.J. Bohlen and M.C. Fisk. 2004. Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests. Ecosystems 7:28-44.

Suàrez, E. R., P. Gerard-Marchant, T. J. Fahey and R. Fahey. Journal of Applied Ecology. Exotic earthworm communities in mono-specific tree plantations: Effects of tree species and soil moisture on earthworm abundance and species composition. Submitted (a) to Journal of Applied Ecology.

Suàrez, E. R., T. J. Fahey, P. M. Groffman, J. B. Yavitt and P. J. Bohlen. Spatial and temporal dynamics of exotic earthworm communities along invasion fronts in a temperate hardwood forest in south-central New York. Biological Invasions. (In Press)

Suàrez, E. R., G. Tierney, T. J. Fahey and R. Fahey. 2006. Exploring patterns of exotic earthworm distribution in a temperate hardwood forest in south-central New York. Landscape Ecology 297-306.

Suàrez, E. R., T. J. Fahey, J. B. Yavitt, P. M. Groffman and P. J. Bohlen. Patterns of litter disappearance in a northern hardwood forest invaded by exotic earthworms. Ecological Applications. ( In Press)

Tiunov, A. V., and S. Scheu. 2004. Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138:83-90.

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