Oecologia (2002) 133:254–260 DOI 10.1007/s00442-002-1023-4
COMMUNITY ECOLOGY
Stefan Scheu · Natalie Schlitt · Alexei V. Tiunov John E. Newington · T. Hefin Jones
Effects of the presence and community composition of earthworms on microbial community functioning Received: 28 February 2002 / Accepted: 9 July 2002 / Published online: 22 August 2002 © Springer-Verlag 2002
Abstract Earthworms are a major component of many terrestrial ecosystems. By modifying decomposition processes and soil structure, they function as driving factors of the soil microbial community. Using microcosms, we investigated the effects of the presence and community composition of earthworms on the in situ respiratory response of a microbial community to an array of organic substrates including carbohydrates, amino acids, a polymer and an amide. Both the actual in situ catabolic response of non-growing microorganisms and the potential response of growing microorganisms were investigated. Three questions were studied: (1) does the presence of one of the main functional groups of earthworms (endogeic species) affect microbial community functioning; (2) does the presence of two functional groups (endogeic and epigeic species) alter microbial community functioning; (3) does the number of species within functional groups matter. The presence of endogeic earthworms significantly reduced microbial biomass and affected the physiological profile and functioning of the microbial community. In contrast, in the presence of endo- and epigeic species microbial biomass was not reduced significantly, indicating that epigeic species counteracted the effect of endogeic species. The physiological profile of the microbial community significantly differed between the treatment with endogeic species only and the treatment with both endo- and epigeic species. Also, the S. Scheu (✉) · N. Schlitt Darmstadt University of Technology, Institute of Zoology, Schnittspahnstrasse 3, 64287 Darmstadt, Germany e-mail:
[email protected] Tel.: +49-6151-163006, Fax: +49-6151-166111 A.V. Tiunov Institute of Ecology and Evolution, Laboratory of Soil Zoology, Leninsky Prospect 33, 117071 Moscow, Russia J.E. Newington · T.H. Jones NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK Present address: T.H. Jones, Cardiff School of Biosciences, Cardiff University, P.O. Box 915, Cardiff CF10 3TL, UK
physiological profile of the microbial community was significantly affected by the number of species per functional group, which at least in part may have been caused by a sampling effect. Overall, the actual in situ catabolic response of non-growing microorganisms appears to be more sensitive than the potential response of growing microorganisms. In addition, the direction of the actual response (negative) was diametrically opposed to that of the potential response (positive). We conclude that the catabolic response of growing microorganisms does not reflect the actual case in situ. For earthworms, loss in both species number and functional group number has the potential to change soil microbial community functioning. Keywords Soil fauna · Lumbricidae · Diversity · Functional groups · Microbial respiration
Introduction Earthworms are a major component of many terrestrial ecosystems (Lee 1985; Edwards and Bohlen 1995). In non-acidic soils they usually dominate the biomass of soil invertebrates and function as ecosystem engineers by structuring the environment of the decomposer community (Jones et al. 1994; Lavelle et al. 1997; Scheu and Setälä 2002). It has been documented that they affect the density and distribution of other soil invertebrates and modify microbial activity (Brown 1995; Tiunov and Scheu 1999; Tiunov et al. 2001). However, the relationship between community structure of earthworms and functioning of the soil microbial community is poorly understood. This is surprising considering the dominance of earthworms in soil systems and the fundamental ecological importance of soil microorganisms in nutrient turnover, decomposition and plant growth. Open habitats in central Europe typically are inhabited by six to ten earthworm species (Lee 1985; Edwards and Bohlen 1995). The species belong to the three functional groups of endogeic, epigeic and anecic species (sensu
255 Table 1 Experimental treatments with composition of the earthworm species (cf. Sims and Gerard 1999) Treatment
Replicate
Species Endogeic
(i) Control
1–4
(ii) Two species – one functional group
1 2 3 4
Epigeic
Aporrectodea caliginosa caliginosa Aporrectodea rosea Aporrectodea rosea Octolasion cyaneum Aporrectodea nocturna Aporrectodea caliginosa tuberculata Allolobophora chlorotica Octolasion cyaneum
(iii) Two species – two functional groups
1 2 3 4
Aporrectodea nocturna Octolasion cyaneum Allolobophora chlorotica Aporrectodea caliginosa caliginosa
Dendrodrilus rubidus Dendrodrilus rubidus Eisenia fetida Eisenia fetida
(iv) Six species – two functional groups
1
Allolobophora chlorotica Aporrectodea caliginosa tuberculata Octolasion cyaneum Aporrectodea caliginosa caliginosa Aporrectodea nocturna Octolasion cyaneum Allolobophora chlorotica Aporrectodea nocturna Aporrectodea caliginosa tuberculata Aporrectodea caliginosa caliginosa Allolobophora chlorotica Octolasion cyaneum
Lumbricus rubellus Dendrodrilus rubidus Eisenia fetida Lumbricus rubellus Dendrodrilus rubidus Eisenia fetida Lumbricus rubelluss Dendrodrilus rubidu Eisenia fetida Lumbricus rubellus Dendrodrilus rubidus Eisenia fetida
2 3 4
Bouché 1977), with endogeic species usually being the most diverse group (Lee 1985; Edwards and Bohlen 1995). Endogeic species are medium-sized pale earthworms that colonize the upper mineral soil and ingest organic matter together with large amounts of mineral soil. In contrast, epigeic species live in organic layers on the soil surface and predominantly feed on organic matter. Anecic species also feed on organic matter but live in permanent vertical burrows extending deep into the soil. Due to permanent horizontal burrowing and the ingestion of large amounts of mineral soil, endogeic species have been shown to be major soil-forming agents (Shaw and Pawluk 1986; Scheu 1987; Scheu and Parkinson 1994). Therefore, in the present study, we focussed on this functional group of earthworms. Generally, the relationship between soil animal community composition and ecosystem functioning has been assumed to be weak or, at the very least, inconsistent (Huhta et al. 1998; Mikola and Setälä 1998; Laakso and Setälä 1999; Griffiths et al. 2000; Wardle et al. 2000). In soil, the redundancy of species appears to be high (Bardgett and Cook 1998; Scheu and Setälä 2001) and this finding has led to the generally held conclusion that the presence of particular keystone species is more important than the number of species or functional groups (Bengtsson 1998; Huhta et al. 1998). Other studies, however, have shown that the diversity of soil microorganisms does affect soil processes and, in some cases, even primary production. The diversity of mycorrhizal fungi, for example, may have a strong influence on plant bio-
mass production (van der Heijden et al. 1998), while the community composition of denitrifying bacteria has been found to regulate denitrification processes in soil (Cavigelli and Robertson 2000). Using model terrestrial communities in the Ecotron controlled environment facility (Lawton et al. 1993), we investigated whether the presence and community composition of earthworms affects the in situ respiratory response of the microbial community to an array of organic substrates (in situ physiological profiles; Degens and Harris 1997; Degens et al. 2000). More specifically, we studied (1) whether the presence of endogeic earthworm species affects microbial community functioning, (2) whether the addition of another functional group (epigeic species) alters microbial community functioning and (3) whether the number of species within functional groups matters.
Materials and methods Experimental set up Model communities were constructed in pots of 1-m2 surface area filled with a basal layer of gravel for drainage and a 30- to 35-cm soil layer. The soil consisted of a sand (40%):loam (60%) mixture to which a low-nutrient compost and leaf litter (predominantly beech, Fagus sylvatica) were added in the ratio of 1:1:0.5 (v/v) (pH 6.4, 2.1% C, 0.095% N). All soil components were partially sterilized by methyl bromide fumigation prior to use. Each model community received 120 ml of a microbial inoculum of Silwood Park soil (Naeem et al. 1994; Jones et al. 1998).
256 The model community consisted of microbi-detritivores, soil predators, plants, herbivores and parasitoids. Soil animals included a mixture of collembola species (Sphaeridia pumilis, Folsomia candida, Protaphorura armata, Proisotoma minuta, Pseudosinella alba) and an isopod (Philoscia muscorum). The plant community consisted of Senecio vulgaris, Erigeron canadensis, Stellaria media and Veronica persica. Myzus persicae (Aphidina), Chromatomya syngenesiae (Diptera), Mamestra brassicae (Lepidoptera) and Helix aspersa (Mollusca) functioned as herbivores. The parasitoids Aphidius matricariae (Hymenoptera) and Dacnusa sibirica (Hymenoptera) served as antagonists of M. persicae and C. syngenesiae, respectively. Four earthworm treatments were set up: (i) control without earthworms, (2) two endogeic species (two species – one functional group treatment), (iii) two species from different functional groups (one endo- and one epigeic species; two species – two functional groups treatment), and (iv) two functional groups with three species each (six species – two functional groups treatment) (Table 1). Each Ecotron community was inoculated with 115 g fresh weight of earthworm biomass. Four replicates were established per treatment. Endogeic earthworms were selected at random from a group of six species (Aporrectodea caliginosa caliginosa, A. caliginosa trapezoides, A. rosea, A. nocturna, Allolobophora chlorotica, Octolasion cyaneum) and epigeic earthworms from a group of three species (Dendrodrilus rubidus, Eisenia fetida, Lumbricus rubellus). The experiment was started on 13 October 1998 and ran for 48 weeks. The light regime (maximum illumination 300 µmol s–1 m–2) was set to a day/night cycle of 14/6 h with 2-h dawn and dusk phases. Temperature followed a diurnal cycle with a minimum of 10°C and a maximum of 16°C. Relative humidity ranged between 58 and 70%. Sampling for the microbial response analysis took place after 24 weeks. Analyses Sieved (
