Abstract
Earthworms are among the world’s most important ecosystem engineers because of their effects on soil fertility and plant productivity. Their dependence on plants for carbon, however, means that any changes in plant community structure or function caused by rising atmospheric CO2 or loss of plant species diversity could affect earthworm activity, which may feed back on plant communities. Production of surface casts measured during three consecutive years in field experimental plots (n = 24, 1.2 m2) planted with local calcareous grassland species that varied in plant species richness (diversity levels: high, 31 species; medium, 12; low, 5) and were exposed to ambient (356 μl CO2 l−1) or elevated (600 μl CO2 l−1) CO2 was only consistently stimulated in high diversity plots exposed to elevated CO2 (+120 %, 31 spp: 603 ± 52 under ambient CO2 vs. 1,325 ± 204 g cast dwt. m−2 year−1 under elevated CO2 in 1996; +77 %, 940 ± 44 vs. 1,663 ± 204 g cast dwt. m−2 year−1 in 1998). Reductions in plant diversity had little effect on cast production in ecosystems maintained at ambient CO2, but the stimulatory effect of elevated CO2 on cast production disappeared when plant species diversity was decreased to 12 and 5 species. High diversity plots were also the only communities that included plant species that an earlier field study showed to be among the most responsive to elevated CO2 and to be most preferred by earthworms to deposit casts near. Further, the +87 % CO2-induced increase in cast production measured over the 3 years corresponded to a parallel increase in cumulative total nitrogen of 5.7 g N m−2 and would help explain the large stimulation of aboveground plant biomass production observed in high-diversity communities under elevated CO2. The results of this study demonstrate how the loss of plant species from communities can alter responses of major soil heterotrophs and consequently ecosystem biogeochemistry.
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References
Aldag R, Graff O (1975) N-Fraktionen in Regenwurmlosung und deren Ursprungsböden. Pedobiologia 15:151–153
Arnone JA III, Zaller JG, Spehn EM, Niklaus PA, Wells CE, Körner Ch (2000) Dynamics of root systems in intact native grasslands: effects of elevated atmospheric CO2. New Phytol 147:73–86
Bohlen PJ (2006) Biological invasions: linking the aboveground and belowground consequences. Appl Soil Ecol 32:1–5
Coleman DC, Crossley DA Jr (1996) Fundamentals of Soil Ecology. Academic, San Diego
Edwards CA, Bohlen PJ (1997) Biology and Ecology of Earthworms. Chapman and Hall, London, pp 55–180
Edwards CA, Lofty R (1977) The Biology of Earthworms, 2nd edn. Chapman and Hall, London
Eisenhauer N, Fisichelli NA, Frelich LE, Reich PB (2012) Interactive effects of global warming and “global worming” on the initial establishment of native and exotic herbaceous plant species. Oikos 121:1121–1133
Glasstetter M (1991) Die Bodenfauna und ihre Beziehungen zum Nährstoffhaushalt in Geosystemen des Tafel- und Faltenjura (Nordwestschweiz). Physiogeographica 15:1–231
Huovinen-Hufschmid C, Körner Ch (1998) Microscale patterns of species distribution and biomass in calcareous grassland. Bot Helv 108:69–83
Intergovernmental Panel on Climate Change (2007) Climate Change: the physical science basis—contribution of working group I to the fourth assessment report of the Intergovernmental panel on climate change. In: Solomon S et al. (eds) Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York
Keeling CD, Piper SC, Bacastow RB, Wahlen M, Whorf TP, Heimann M, Meijer HA (2005) Atmospheric CO2 and 13CO2 exchange with the terrestrial biosphere and oceans from 1978 to 2000: observations and carbon cycle implications. In: Ehleringer JR, Cerling TE, Dearing MD (eds) A History of Atmospheric CO2 and its Effects on Plants, Animals, and Ecosystems. Springer, New York, pp 83–113
Lauber W, Körner Ch (1997) In situ stomatal responses to long term CO2 enrichment in calcareous grassland plants. Acta Oecol 18:221–229
Leadley PW, Niklaus P, Stocker R, Körner Ch (1997) Screen aided CO2 control (SACC): a middle ground between FACE and open top chamber. Acta Oecol 18:207–219
Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic, Sydney
Niklaus PA, Körner Ch (2004) Synthesis of a six-year study of calcareous grassland responses to in situ CO2 enrichment. Ecol Monogr 74:491–511
Niklaus PA, Wohlfender M, Siegwolf R, Körner Ch (2001) Effects of six years atmospheric CO2 enrichment on plant, soil, and soil microbial C of a calcareous grassland. Plant Soil 233:189–202
Niklaus PA, Alphei J, Kampichler C, Kandeler E, Körner Ch, Tscherko D, Wohlfender M (2007) Interactive effects of plant species diversity and elevated CO2 on soil biota and nutrient cycling. Ecology 88:3153–3163
Ogermann P, Spycher B, Schaub D, Sollberger R (1994) Die Land-schaftsstruktur im Raum Nenzlingen—geoökologisch gesehen. Regio Basiliensis 35:91–100
Phillipson J, Abel R, Steel J, Woodell SRJ (1976) Earthworms and the factors governing their distribution in an English beech-wood. Pedobiologia 16:258–285
Satchell JE (ed) (1983) Earthworm Ecology: from Darwin to Vermiculture. Chapman and Hall, London
Scheu S (1993) Analysis of the microbial nutrient status in soil microcopartments: earthworm feces from a basalt limestone gradient. Geoderma 56:575–586
Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856
Spehn EM, Joshi J, Alphei J, Schmid B, Korner Ch (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230
Stocker R, Leadley PW, Körner C (1997) Carbon and water fluxes in a calcareous grassland under elevated CO2. Funct Ecol 11:222–230
Stocker R, Körner Ch, Schmid B, Niklaus PA, Leadley PW (1999) A field study of the effects of elevated CO2 and plant species diversity on ecosystem-level gas exchange in a planted calcareous grassland. Glob Change Biol 5:95–105
Syers JK, Sharpley AN, Keeney DR (1979) Cycling of nitrogen by surface-casting earthworms in a pasture ecosystem. Soil Biol Biochem 11:181–185
von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and Analysis of Ecological Experiments. Chapman and Hall, New York, pp 113–137
Zaller JG, Arnone JA III (1997) Activity of surface-casting earthworms in a calcareous grassland under elevated atmospheric CO2. Oecologia 111:249–254
Zaller JG, Arnone JA III (1999a) Earthworm responses to plant species’ loss and elevated CO2 in calcareous grassland. Plant Soil 208:1–8
Zaller JG, Arnone JA III (1999b) Interactions between earthworm casts and plant species in a calcareous grassland under elevated CO2. Ecology 80:873–881
Zaller JG, Arnone JA III (1999c) Earthworm and soil moisture effects on the productivity and structure of grassland communities. Soil Biol Biochem 31:517–523
Zaller JG, Heigl F, Grabaier A, Lichtenegger C, Piller K, Allabashi R, Frank T, Drapela T (2011) Earthworm-mycorrhiza interactions can affect the diversity, structure and functioning of establishing model grassland communities. PLoS ONE 6:1–9
Zicsi A (1983) Earthworm ecology in deciduous forests in central and southeast Europe. In: Satchell JE (ed) Earthworm Ecology: from Darwin to Vermiculture. Chapman and Hall, London, pp 171–177
Acknowledgments
We thank P. Niklaus and P. Leadley for their assistance in setting up and maintaining the CO2-enrichment and plant biodiversity treatments, T. Morgan and R. Blank for analyzing total N in casts, and J. Larsen and L. Wable for their help in producing the graphics used in the figures of this paper. Financial support for this research was provided by the Swiss National Science Foundation (NF) through grants to Arnone (NF 3100-042401.94/1) and Körner, Schmid and Arnone (NF-SPPU 5001-035214).
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Communicated by Russell Monson.
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Arnone, J.A., Zaller, J.G., Hofer, G. et al. Loss of plant biodiversity eliminates stimulatory effect of elevated CO2 on earthworm activity in grasslands. Oecologia 171, 613–622 (2013). https://doi.org/10.1007/s00442-012-2585-4
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DOI: https://doi.org/10.1007/s00442-012-2585-4