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Do plant species encourage soil biota that specialise in the rapid decomposition of their litter?
Soil Biology & Biochemistry 38 (2006) 183–186 www.elsevier.com/locate/soilbio
Short communication
Do plant species encourage soil biota that specialise in the rapid decomposition of their litter? Edward Ayres*, Karsten M. Dromph1, Richard D. Bardgett Department of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK Received 19 November 2004; received in revised form 18 April 2005; accepted 19 April 2005
Abstract Plants are often nutrient limited and soil organisms are important in mediating nutrient availability to plants. Thus, there may be a selective advantage to plants that alter the soil community in ways that enhance the decomposition of their litter and, hence, their ability to access nutrients. We incubated litter from three tree species (Fagus sylvatica, Acer pseudoplatanus and Picea sitchensis) in the presence of biota extracted from soil beneath a stand of each species to test the hypothesis that litter decomposes fastest in the presence of biota derived from soil where that species is locally abundant. We found that respiration rate, a measure of decomposer activity and carbon mineralisation, was affected by litter type and source of soil biota, whereas, mass loss was only affected by litter type. However, litter from each tree species did not decompose faster in the presence of indigenous soil biota. These findings, therefore, provide no support for the notion that woodland plants encourage the development of soil communities that rapidly decompose their litter. q 2005 Elsevier Ltd. All rights reserved. Keywords: Leaf litter; Decomposition; Mass loss; Soil biota; Flora; Fauna; Community structure; Respiration; Nutrient cycling; Local adaptation
Soil nutrient availability often limits plant productivity; therefore, plants that alter their environment in ways that enhance their ability to access nutrients may have a selective advantage. Litter decomposition is critical in determining soil nutrient cycling rates (Swift et al., 1979) and it has been hypothesised that some plants may encourage the development of a soil community suited to the rapid decomposition of their litter (Wardle, 2002), since this would increase nutrient availability to the plant and hence its competitive status within the plant community. Whilst this idea has not been explicitly tested, there is evidence from the literature to suggest that it could occur. First, it is well established that litter differs in chemical composition between plant species, influencing its rate of decomposition, and that individual plant species can affect the biomass and community * Corresponding author. Present address: Natural Resource and Ecology Laboratory, Colorado State University, Fort Collins, CO 80521, USA. Tel.: C1 970 491 1984; fax: C1 970 491 1965. E-mail address: [email protected] (E. Ayres). 1 Present address: Department of Ecology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark.
0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2005.04.018
structure of the microbial community (Bradley and Fyles, 1995; Groffman et al., 1996; Grayston et al., 1998; Bardgett et al., 1999; Priha et al., 1999; Porazinska et al., 2003; Bardgett and Walker, 2004), as well as the abundance of animals that feed on them (Parmelee et al., 1989; Blair et al., 1990; Griffiths et al., 1992; Hansen, 1999). Second, soil microbes are directly responsible for most decomposition, and soil animals, such as microarthropods (Seastedt, 1984), isopods (Ha¨ttenschwiler and Bretscher, 2001), and earthworms (Cortez and Bouche´, 2001) can stimulate decomposition via litter fragmentation and defecating into the soil, and through altering the activity and composition of the microbial community (Wardle, 2002). There is limited experimental evidence that soil biota beneath a plant species decomposes litter from that species faster than litter from other species, however, the pattern appears inconsistent. Triticum aestivum residue decomposed faster in soil incorporated with T. aestivum residue, than in ‘residue-removed’ soil, whereas, decomposition of residue from two other species did not differ between the soils (Cookson et al., 1998). In a 2-year litter addition study, Hansen (1999) found that Quercus rubra litter decomposed faster in the second year, while litter decomposition from two other species did not differ. Increased decomposition
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coincided with changes in the mite community, suggesting Q. rubra litter encouraged soil biota that increased its decomposition rate (Hansen, 1999). Evidence of an ecosystem-level enhancement of litter decomposition is more compelling. Litter from a dominant tree species decomposed faster in forest soil than in prairie or meadow soil, however, decomposition of litter from a dominant prairie or meadow species did not differ between ecosystems (Hunt et al., 1988). Similarly, litter from a broadleaf tree decomposed faster in ‘broadleaf habitats’ than in ‘coniferous habitats’, however, habitat had no effect on conifer litter decomposition (Gholz et al., 2000). We tested the hypothesis that a plant species’ litter decomposes faster in the presence of biota derived from the soil of that plant species, than in the presence of biota from soils of other species. This was conducted under laboratory conditions by incubating litter from three tree species with biota extracted from soil beneath pure stands of each species and quantifying respiration and litter mass loss. Naturally senesced leaf litter and soil were collected from pure stands of beech (Fagus sylvatica), sycamore (Acer pseudoplatanus) and sitka spruce (Picea sitchensis) surrounding Lancaster University, in north-west England. The stands were separated by less than 500 m, therefore, environmental influences were considered comparable. Five soil cores (8 cm diameter, 5 cm deep) and five samples of litter (50 g) were collected from each stand. The litter was sterilised (autoclaved: 121 8C for 20 min), dried (70 8C), and broadleaf litter was cut into 1.5 cm squares; needles were not cut. One of the five litter samples for each tree species was allocated to one of five blocks and used exclusively for that block. Forty-five McCartney bottles (29 ml) were filled with 0.5 g litter from one of the three species. As with the litter, one of the five soil cores for each tree species was allocated to one of five blocks. Each soil core was mixed with 500 ml distilled water and filtered (Whatman No. 1) to create an inoculum. The inoculum probably contained bacteria, fungi and protozoa, and possibly smaller nematodes. However, larger nematodes, enchytraeid worms, mites, collembolans, earthworms and other macrofauna were excluded. If larger soil fauna been included in the inoculum it is possible that the results would have differed from those reported here. However, it should be noted that whilst larger animals play an important role in litter fragmentation, and, hence, its mass loss, soil microbes are directly responsible for the majority of decomposition (Bardgett, 2005). Inoculum (2 ml) from each soil core was added to three bottles (one per tree species), resulting in nine treatments with five replicates. The litter was incubated without soil so that soil respiration would not mask changes in respiration derived from litter. However, we note that this simplification is likely to have altered its decomposition rate and probably does not truly reflect what occurs in the field. The bottles were arranged in a randomised block design and incubated at 10 8C.
Respiration, a measure of the metabolic activity of the decomposer community and carbon mineralisation, was determined by sealing the bottles for 50 min using No. 37 subaseals and measuring the CO2 concentration in headspace gas using an infra-red gas analyser (IRGA) (Analytical Development, Hoddesdon, UK). After 103 days, the litter was removed, dried (70 8C) and litter mass loss was measured. Data were analysed using generalised linear models (GLM) (Nelder and Wedderburn, 1972) with the GENMOD procedure in SAS 8.0 (SAS Institute, 1990). Date was included as a repeated measure (Liang and Zeger, 1986). Both date and litter type affected respiration rate and accounted for most of the variation in this measure (Table 1; Fig. 1a). Initially, respiration rate decreased over time, however, it stabilised after day 70. Respiration rate and mass loss from A. pseudoplatanus litter were greater than from the other species (Tables 2 and 3; Figs. 1a and 2), suggesting it is of superior quality. In agreement with this, Ha¨ttenschwiler and Bretscher (2001) showed A. pseudoplatanus litter had a greater nitrogen (N) content than F. sylvatica litter, and was consumed more rapidly, and preferentially, by an isopod. Respiration rate was greater from P. sitchensis litter than from F. sylvatica litter until day 55, after which CO2 evolution was slightly greater from F. sylvatica litter (Fig. 1a). There was no difference in mass remaining between these two species (Table 3; Fig. 2). In contrast, in a 7-day experiment, Dursun et al. (1993) observed respiration rates that were three times greater from F. sylvatica litter than from P. sitchensis litter. Both species have similar concentrations of nutrients that correlate with litter decomposition rate: litter concentrations of N ranging from 9.2 to 16.6 mg gK1 (Pedersen and Bille-Hansen, 1999; Zeller et al., 2000; Kavvadias et al., 2001; Sariyildiz and Anderson, 2003) and phosphorus (P) from 0.5 to 0.9 mg gK1 (Pedersen and Bille-Hansen, 1999) have been reported for F. sylvatica, and concentrations of N from 12.5 to 14.1 mg gK1 (Pedersen and Bille-Hansen, 1999) and P from 0.5 to 0.8 mg gK1 (Pedersen and Bille-Hansen, 1999) have been reported for P. sitchensis. Furthermore, reported phenolic concentrations in F. sylvatica and P. sitchensis leaves are 35–100 mg g K1 (Johnson et al., 1997) Table 1 Output from a repeated measures GLM on the effect of date, litter type and source of soil biota on respiration rate from litter
Date Litter Soil biota Date!litter Date!soil biota Litter!soil biota Date!litter!soil biota
df
F
P
1 2 2 2 2 4 4
288.2 69.8 6.1 20.1 0.6 1.5 2.6
!0.0001 !0.0001 0.0025 !0.0001 NS NS 0.0344
NS, not significant (PO0.05); df, degrees of freedom.
E. Ayres et al. / Soil Biology & Biochemistry 38 (2006) 183–186 Table 3 Mass remaining from each litter type after 103 days Species
Mass remaining (%)
F. sylvatica A. pseudoplatanus P. sitchensis
93.1 (1.0) 87.5 (1.4) 93.3 (0.9)
60
Litter
40
Values are means (SE) (nZ5).
20
0 0
20
40
60
80
100
120
80
100
120
Day
(b) 80
60
40
20
0 0
20
40
60
Day
Fig. 1. Respiration rate from (a) litter of each tree species (averaged across source of soil biota) and (b) soil biota derived from a stand of each tree species (averaged across litter type). Dotted, F. sylvatica; solid, A. pseudoplatanus; broken, P. sitchensis. Values are meansGSE.
and 52 mg gK1 (Raymond et al., 2002), respectively. Our results, combined with the literature, suggest F. sylvatica and P. sitchensis litter decompose at similar rates during the initial stage of decomposition. The source of soil biota also affected respiration rate, but accounted for less variation than date and litter type (Table 1; Fig. 1b). This provides some evidence that tree species can modify the soil community to influence litter decomposition. However, contrary to our hypothesis, indigenous soil biota did not result in enhanced respiration (Table 1) or mass loss (Table 2; Fig. 2). There was a significant three-way interaction on respiration (Table 1); Table 2 Output from a GLM on the effect of litter type and source of soil biota on litter mass remaining after 103 days
Litter Soil biota Litter!soil biota
df
F
P
2 2 4
10.5 0.4 0.6
0.0012 NS NS
NS, not significant (PO0.05); df, degrees of freedom.
however, the effect was inconsistent (data not shown). Our results do not support the findings of Cookson et al. (1998) or Hansen (1999), who suggested plant species encourage soil biota that specialise in the rapid decomposition of their litter. However, the experiment conducted by Hansen (1999) was not designed to explicitly test this hypothesis and Cookson et al. (1998) used plant residues, not naturally senesced litter, which differs markedly in chemical composition (Chapin and Kedrowski, 1983; Aerts, 1996). Litter from different habitats may decompose faster in soils from their own habitat type than in soils from other habitats (Hunt et al., 1988; Gholz et al., 2000), however, the results from our study suggest that at the species level, plants species do not encourage the development of a soil microbial community that specialises in decomposing their litter rapidly, at least during the early phase of decomposition. It is possible that the role of soil biota in decomposition may increase as labile substances are lost and decomposition rate declines, but it is not possible to infer this from the results presented here. This study investigated the hypothesis that plants engineer the soil community to enhance the decomposition rate of their litter. However, its design has certain limitations, notably the exclusion of larger soil fauna and its relatively short duration. Therefore, this hypothesis requires further examination under both laboratory and field conditions, with a broader selection of the soil biota and over time scales that encompass later stages of decomposition. Nonetheless, since soil microbes are directly responsible for the majority of litter decomposition, 100
Mass remaining (%)
Respiration rate (µl CO2 h–1)
(a) 80
Respiration rate (µl CO2 h–1)
185
95
90
85
80
F. sylvatica
A. pseudoplatanus
P. sitchensis
Litter type Fig. 2. Litter mass remaining from each combination of litter type and source of soil biota. Dark grey, light grey, and white bars represent soil biota from F. sylvatica, A. pseudoplatanus and P. sitchensis stands, respectively. Values are meansGSE.
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and their abundance and community structure can be modified by plant species (Bradley and Fyles, 1995; Groffman et al., 1996; Grayston et al., 1998; Bardgett et al., 1999; Priha et al., 1999; Porazinska et al., 2003; Bardgett and Walker, 2004), it seems likely that an enhancement of litter decomposition rate in the presence of indigenous soil biota would be detectable in the presence of soil micro-flora and -fauna. This study does not support the notion that plant species encourage soil organisms that specialise in rapidly decomposing their litter, at least during the initial stage of decomposition. However, it does not preclude the possibility that plants encourage soil biota that promotes the rapid release of nutrients from their litter. Litter decomposition and nutrient release from litter are related, but not the same. Therefore, experiments that investigate the fate of nutrients (e.g. using 15N or 32P) derived from litter of various plant species decomposing in soils planted exclusively with each of those species are required. Acknowledgements The authors are grateful for the comments of two anonymous reviewers, which greatly improved the manuscript. Funding for this study was provided by the award of a studentship to EA by the Natural Environment Research Council (NERC). References Aerts, R., 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608. Bardgett, R.D., 2005. The Biology of Soil: A Community and Ecosystem Approach. Oxford University Press, Oxford, UK. 256 pp. Bardgett, R.D., Walker, L.R., 2004. Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biology & Biochemistry 36, 555–559. Bardgett, R.D., Mawdsley, J.L., Edwards, S., Hobbs, P.J., Davies, W.J., 1999. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Functional Ecology 13, 650–660. Blair, J.M., Parmelee, R.W., Beare, M.H., 1990. Decay rates, nitrogen fluxes and decomposer communities in single and mixed species foliar litter. Ecology 71, 1976–1985. Bradley, R.L., Fyles, J.W., 1995. Growth of paper birch (Betula papyrifera) seedlings increases soil available C and microbial acquisition of soil nutrients. Soil Biology & Biochemistry 27, 1565–1571. Chapin III., F.S., Kedrowski, R.A., 1983. Seasonal changes in nitrogen and phosphorous fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64, 376–391. Cookson, W.R., Beare, M.H., Wilson, P.E., 1998. Effects of prior crop residue management on microbial properties and crop residue decomposition. Applied Soil Ecology 7, 179–188. Cortez, J., Bouche´, M., 2001. Decomposition of Mediterranean leaf litters by Nicodrilus meridionalis (Lumbricidae) in laboratory and field experiments. Soil Biology & Biochemistry 33, 2023–2035. Dursun, S., Ineson, P., Frankland, J.C., Boddy, L., 1993. Sulphite and pH effects on CO2 evolution from decomposing angiospermous and coniferous tree leaf litter. Soil Biology & Biochemistry 25, 1513–1525. Gholz, H.L., Wedin, D.A., Smitherman, S.M., Harmon, M.E., Parton, W.J., 2000. Long-term dynamics of pine and litter decomposition in
contrasting environments: towards a global model of decomposition. Global Change Biology 6, 751–765. Grayston, S.J., Shenquiang, W., Campbell, C.D., Edwards, A.C., 1998. Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biology & Biochemistry 30, 369–378. Griffiths, B.S., Welschen, R., Vanarendonk, J.J.C.M., Lambers, H., 1992. The effect of nitrate-nitrogen on bacteria-feeding fauna in the rhizosphere of different grass species. Oecologia 91, 253–259. Groffman, P.M., Eagan, P., Sullivan, W.M., Lemunyon, J.L., 1996. Grass species and soil type effects on microbial biomass and activity. Plant and Soil 183, 61–67. Hansen, R.A., 1999. Red oak litter promotes a microarthropod functional group that accelerates its decomposition. Plant and Soil 209, 37–45. Ha¨ttenschwiler, S., Bretscher, D., 2001. Isopod effects on decomposition of litter produced under elevated CO2, N deposition and different soil types. Global Change Biology 7, 565–579. Hunt, H.W., Ingham, E.R., Coleman, D.C., Elliot, E.T., Reid, C.P.P., 1988. Nitrogen limitation of production and decomposition in prairie, mountain meadow, and pine forest. Ecology 69, 1009–1016. Johnson, J.D., Tognetti, R., Michelozzi, M., Pinzauti, S., Minotta, G., Borghetti, M., 1997. Ecophysiological responses of Fagus sylvatica seedlings to changing light conditions. II. The interaction of light environment and soil fertility on seedling physiology. Physiologia Plantarum 101, 124–134. Kavvadias, V.A., Alifragis, D., Tsiontsis, A., Brofas, G., Stematelos, G., 2001. Litterfall, litter accumulation and litter decomposition rates in four forest ecosystems in northern Greece. Forest Ecology and Management 144, 113–127. Liang, K.Y., Zeger, S.L., 1986. Longitudinal data analysis using generalised linear models. Biometrika 73, 13–22. Nelder, J.A., Wedderburn, R.W.M., 1972. Generalised linear models. Journal of the Royal Statistical Society A 135, 370–384. Parmelee, R.W., Beare, M.H., Blair, J.M., 1989. Decomposition and nitrogen dynamics of surface weed residues in no-tillage agroecosystems under drought conditions: influence of resource quality on the decomposer community. Soil Biology & Biochemistry 21, 97–103. Pedersen, L.B., Bille-Hansen, J., 1999. A comparison of litterfall and element fluxes in even aged Norway spruce, sitka spruce and beech stands in Denmark. Forest Ecology and Management 114, 55–70. Porazinska, D.L., Bardgett, R.D., Blaauw, M.B., Hunt, W., Parsons, A.N., Seastedt, T.R., Wall, D., 2003. Relationships at the aboveground– belowground interface: plants, soil biota, and soil processes. Ecological Monographs 73, 377–395. Priha, O., Hallantie, T., Smolander, A., 1999. Comparing microbial biomass, denitrification enzyme activity, and numbers of nitrifiers in the rhizosphere of Pinus sylvestris, Picea abies and Betula pendula seedlings by microscale methods. Biology and Fertility of Soils 30, 14–19. Raymond, B., Vanbergen, A., Pearce, I., Hartley, S.E., Cory, J.S., Hails, R.S., 2002. Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus. Oecologia 131, 533–541. Sariyildiz, T., Anderson, J.M., 2003. Decomposition of sun and shade leaves from three deciduous tree species, as affected by their chemical composition. Biology and Fertility of Soils 37, 137–146. SAS Institute, 1990., fourth ed.Anon, 1990. SAS/STAT(R) User’s Guide, Version 6, vols. 1–2. Cary, North Carolina. Seastedt, T.R., 1984. The role of arthropods in decomposition and mineralisation processes. Annual Review of Entomology 29, 25–46. Swift, M.J., Heal, O.M., Anderson, J.M., 1979. Decomposition in Terrestrial Ecosystems. University of California Press, Berkeley, CA. 372 pp. Wardle, D.A., 2002. Communities and Ecosystems: Linking the Aboveground and Belowground Components. Princeton University Press, Princeton, NJ. 392 pp. Zeller, B., Colin-Belgrand, M., Dambrine, E., Martin, F., Bottner, P., 2000. Decomposition of 15N-labelled beech litter and the fate of nitrogen derived from litter in a beech forest. Oecologia 123, 550–559.
Short communication
Do plant species encourage soil biota that specialise in the rapid decomposition of their litter? Edward Ayres*, Karsten M. Dromph1, Richard D. Bardgett Department of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK Received 19 November 2004; received in revised form 18 April 2005; accepted 19 April 2005
Abstract Plants are often nutrient limited and soil organisms are important in mediating nutrient availability to plants. Thus, there may be a selective advantage to plants that alter the soil community in ways that enhance the decomposition of their litter and, hence, their ability to access nutrients. We incubated litter from three tree species (Fagus sylvatica, Acer pseudoplatanus and Picea sitchensis) in the presence of biota extracted from soil beneath a stand of each species to test the hypothesis that litter decomposes fastest in the presence of biota derived from soil where that species is locally abundant. We found that respiration rate, a measure of decomposer activity and carbon mineralisation, was affected by litter type and source of soil biota, whereas, mass loss was only affected by litter type. However, litter from each tree species did not decompose faster in the presence of indigenous soil biota. These findings, therefore, provide no support for the notion that woodland plants encourage the development of soil communities that rapidly decompose their litter. q 2005 Elsevier Ltd. All rights reserved. Keywords: Leaf litter; Decomposition; Mass loss; Soil biota; Flora; Fauna; Community structure; Respiration; Nutrient cycling; Local adaptation
Soil nutrient availability often limits plant productivity; therefore, plants that alter their environment in ways that enhance their ability to access nutrients may have a selective advantage. Litter decomposition is critical in determining soil nutrient cycling rates (Swift et al., 1979) and it has been hypothesised that some plants may encourage the development of a soil community suited to the rapid decomposition of their litter (Wardle, 2002), since this would increase nutrient availability to the plant and hence its competitive status within the plant community. Whilst this idea has not been explicitly tested, there is evidence from the literature to suggest that it could occur. First, it is well established that litter differs in chemical composition between plant species, influencing its rate of decomposition, and that individual plant species can affect the biomass and community * Corresponding author. Present address: Natural Resource and Ecology Laboratory, Colorado State University, Fort Collins, CO 80521, USA. Tel.: C1 970 491 1984; fax: C1 970 491 1965. E-mail address: [email protected] (E. Ayres). 1 Present address: Department of Ecology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark.
0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2005.04.018
structure of the microbial community (Bradley and Fyles, 1995; Groffman et al., 1996; Grayston et al., 1998; Bardgett et al., 1999; Priha et al., 1999; Porazinska et al., 2003; Bardgett and Walker, 2004), as well as the abundance of animals that feed on them (Parmelee et al., 1989; Blair et al., 1990; Griffiths et al., 1992; Hansen, 1999). Second, soil microbes are directly responsible for most decomposition, and soil animals, such as microarthropods (Seastedt, 1984), isopods (Ha¨ttenschwiler and Bretscher, 2001), and earthworms (Cortez and Bouche´, 2001) can stimulate decomposition via litter fragmentation and defecating into the soil, and through altering the activity and composition of the microbial community (Wardle, 2002). There is limited experimental evidence that soil biota beneath a plant species decomposes litter from that species faster than litter from other species, however, the pattern appears inconsistent. Triticum aestivum residue decomposed faster in soil incorporated with T. aestivum residue, than in ‘residue-removed’ soil, whereas, decomposition of residue from two other species did not differ between the soils (Cookson et al., 1998). In a 2-year litter addition study, Hansen (1999) found that Quercus rubra litter decomposed faster in the second year, while litter decomposition from two other species did not differ. Increased decomposition
184
E. Ayres et al. / Soil Biology & Biochemistry 38 (2006) 183–186
coincided with changes in the mite community, suggesting Q. rubra litter encouraged soil biota that increased its decomposition rate (Hansen, 1999). Evidence of an ecosystem-level enhancement of litter decomposition is more compelling. Litter from a dominant tree species decomposed faster in forest soil than in prairie or meadow soil, however, decomposition of litter from a dominant prairie or meadow species did not differ between ecosystems (Hunt et al., 1988). Similarly, litter from a broadleaf tree decomposed faster in ‘broadleaf habitats’ than in ‘coniferous habitats’, however, habitat had no effect on conifer litter decomposition (Gholz et al., 2000). We tested the hypothesis that a plant species’ litter decomposes faster in the presence of biota derived from the soil of that plant species, than in the presence of biota from soils of other species. This was conducted under laboratory conditions by incubating litter from three tree species with biota extracted from soil beneath pure stands of each species and quantifying respiration and litter mass loss. Naturally senesced leaf litter and soil were collected from pure stands of beech (Fagus sylvatica), sycamore (Acer pseudoplatanus) and sitka spruce (Picea sitchensis) surrounding Lancaster University, in north-west England. The stands were separated by less than 500 m, therefore, environmental influences were considered comparable. Five soil cores (8 cm diameter, 5 cm deep) and five samples of litter (50 g) were collected from each stand. The litter was sterilised (autoclaved: 121 8C for 20 min), dried (70 8C), and broadleaf litter was cut into 1.5 cm squares; needles were not cut. One of the five litter samples for each tree species was allocated to one of five blocks and used exclusively for that block. Forty-five McCartney bottles (29 ml) were filled with 0.5 g litter from one of the three species. As with the litter, one of the five soil cores for each tree species was allocated to one of five blocks. Each soil core was mixed with 500 ml distilled water and filtered (Whatman No. 1) to create an inoculum. The inoculum probably contained bacteria, fungi and protozoa, and possibly smaller nematodes. However, larger nematodes, enchytraeid worms, mites, collembolans, earthworms and other macrofauna were excluded. If larger soil fauna been included in the inoculum it is possible that the results would have differed from those reported here. However, it should be noted that whilst larger animals play an important role in litter fragmentation, and, hence, its mass loss, soil microbes are directly responsible for the majority of decomposition (Bardgett, 2005). Inoculum (2 ml) from each soil core was added to three bottles (one per tree species), resulting in nine treatments with five replicates. The litter was incubated without soil so that soil respiration would not mask changes in respiration derived from litter. However, we note that this simplification is likely to have altered its decomposition rate and probably does not truly reflect what occurs in the field. The bottles were arranged in a randomised block design and incubated at 10 8C.
Respiration, a measure of the metabolic activity of the decomposer community and carbon mineralisation, was determined by sealing the bottles for 50 min using No. 37 subaseals and measuring the CO2 concentration in headspace gas using an infra-red gas analyser (IRGA) (Analytical Development, Hoddesdon, UK). After 103 days, the litter was removed, dried (70 8C) and litter mass loss was measured. Data were analysed using generalised linear models (GLM) (Nelder and Wedderburn, 1972) with the GENMOD procedure in SAS 8.0 (SAS Institute, 1990). Date was included as a repeated measure (Liang and Zeger, 1986). Both date and litter type affected respiration rate and accounted for most of the variation in this measure (Table 1; Fig. 1a). Initially, respiration rate decreased over time, however, it stabilised after day 70. Respiration rate and mass loss from A. pseudoplatanus litter were greater than from the other species (Tables 2 and 3; Figs. 1a and 2), suggesting it is of superior quality. In agreement with this, Ha¨ttenschwiler and Bretscher (2001) showed A. pseudoplatanus litter had a greater nitrogen (N) content than F. sylvatica litter, and was consumed more rapidly, and preferentially, by an isopod. Respiration rate was greater from P. sitchensis litter than from F. sylvatica litter until day 55, after which CO2 evolution was slightly greater from F. sylvatica litter (Fig. 1a). There was no difference in mass remaining between these two species (Table 3; Fig. 2). In contrast, in a 7-day experiment, Dursun et al. (1993) observed respiration rates that were three times greater from F. sylvatica litter than from P. sitchensis litter. Both species have similar concentrations of nutrients that correlate with litter decomposition rate: litter concentrations of N ranging from 9.2 to 16.6 mg gK1 (Pedersen and Bille-Hansen, 1999; Zeller et al., 2000; Kavvadias et al., 2001; Sariyildiz and Anderson, 2003) and phosphorus (P) from 0.5 to 0.9 mg gK1 (Pedersen and Bille-Hansen, 1999) have been reported for F. sylvatica, and concentrations of N from 12.5 to 14.1 mg gK1 (Pedersen and Bille-Hansen, 1999) and P from 0.5 to 0.8 mg gK1 (Pedersen and Bille-Hansen, 1999) have been reported for P. sitchensis. Furthermore, reported phenolic concentrations in F. sylvatica and P. sitchensis leaves are 35–100 mg g K1 (Johnson et al., 1997) Table 1 Output from a repeated measures GLM on the effect of date, litter type and source of soil biota on respiration rate from litter
Date Litter Soil biota Date!litter Date!soil biota Litter!soil biota Date!litter!soil biota
df
F
P
1 2 2 2 2 4 4
288.2 69.8 6.1 20.1 0.6 1.5 2.6
!0.0001 !0.0001 0.0025 !0.0001 NS NS 0.0344
NS, not significant (PO0.05); df, degrees of freedom.
E. Ayres et al. / Soil Biology & Biochemistry 38 (2006) 183–186 Table 3 Mass remaining from each litter type after 103 days Species
Mass remaining (%)
F. sylvatica A. pseudoplatanus P. sitchensis
93.1 (1.0) 87.5 (1.4) 93.3 (0.9)
60
Litter
40
Values are means (SE) (nZ5).
20
0 0
20
40
60
80
100
120
80
100
120
Day
(b) 80
60
40
20
0 0
20
40
60
Day
Fig. 1. Respiration rate from (a) litter of each tree species (averaged across source of soil biota) and (b) soil biota derived from a stand of each tree species (averaged across litter type). Dotted, F. sylvatica; solid, A. pseudoplatanus; broken, P. sitchensis. Values are meansGSE.
and 52 mg gK1 (Raymond et al., 2002), respectively. Our results, combined with the literature, suggest F. sylvatica and P. sitchensis litter decompose at similar rates during the initial stage of decomposition. The source of soil biota also affected respiration rate, but accounted for less variation than date and litter type (Table 1; Fig. 1b). This provides some evidence that tree species can modify the soil community to influence litter decomposition. However, contrary to our hypothesis, indigenous soil biota did not result in enhanced respiration (Table 1) or mass loss (Table 2; Fig. 2). There was a significant three-way interaction on respiration (Table 1); Table 2 Output from a GLM on the effect of litter type and source of soil biota on litter mass remaining after 103 days
Litter Soil biota Litter!soil biota
df
F
P
2 2 4
10.5 0.4 0.6
0.0012 NS NS
NS, not significant (PO0.05); df, degrees of freedom.
however, the effect was inconsistent (data not shown). Our results do not support the findings of Cookson et al. (1998) or Hansen (1999), who suggested plant species encourage soil biota that specialise in the rapid decomposition of their litter. However, the experiment conducted by Hansen (1999) was not designed to explicitly test this hypothesis and Cookson et al. (1998) used plant residues, not naturally senesced litter, which differs markedly in chemical composition (Chapin and Kedrowski, 1983; Aerts, 1996). Litter from different habitats may decompose faster in soils from their own habitat type than in soils from other habitats (Hunt et al., 1988; Gholz et al., 2000), however, the results from our study suggest that at the species level, plants species do not encourage the development of a soil microbial community that specialises in decomposing their litter rapidly, at least during the early phase of decomposition. It is possible that the role of soil biota in decomposition may increase as labile substances are lost and decomposition rate declines, but it is not possible to infer this from the results presented here. This study investigated the hypothesis that plants engineer the soil community to enhance the decomposition rate of their litter. However, its design has certain limitations, notably the exclusion of larger soil fauna and its relatively short duration. Therefore, this hypothesis requires further examination under both laboratory and field conditions, with a broader selection of the soil biota and over time scales that encompass later stages of decomposition. Nonetheless, since soil microbes are directly responsible for the majority of litter decomposition, 100
Mass remaining (%)
Respiration rate (µl CO2 h–1)
(a) 80
Respiration rate (µl CO2 h–1)
185
95
90
85
80
F. sylvatica
A. pseudoplatanus
P. sitchensis
Litter type Fig. 2. Litter mass remaining from each combination of litter type and source of soil biota. Dark grey, light grey, and white bars represent soil biota from F. sylvatica, A. pseudoplatanus and P. sitchensis stands, respectively. Values are meansGSE.
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and their abundance and community structure can be modified by plant species (Bradley and Fyles, 1995; Groffman et al., 1996; Grayston et al., 1998; Bardgett et al., 1999; Priha et al., 1999; Porazinska et al., 2003; Bardgett and Walker, 2004), it seems likely that an enhancement of litter decomposition rate in the presence of indigenous soil biota would be detectable in the presence of soil micro-flora and -fauna. This study does not support the notion that plant species encourage soil organisms that specialise in rapidly decomposing their litter, at least during the initial stage of decomposition. However, it does not preclude the possibility that plants encourage soil biota that promotes the rapid release of nutrients from their litter. Litter decomposition and nutrient release from litter are related, but not the same. Therefore, experiments that investigate the fate of nutrients (e.g. using 15N or 32P) derived from litter of various plant species decomposing in soils planted exclusively with each of those species are required. Acknowledgements The authors are grateful for the comments of two anonymous reviewers, which greatly improved the manuscript. Funding for this study was provided by the award of a studentship to EA by the Natural Environment Research Council (NERC). References Aerts, R., 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608. Bardgett, R.D., 2005. The Biology of Soil: A Community and Ecosystem Approach. Oxford University Press, Oxford, UK. 256 pp. Bardgett, R.D., Walker, L.R., 2004. Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biology & Biochemistry 36, 555–559. Bardgett, R.D., Mawdsley, J.L., Edwards, S., Hobbs, P.J., Davies, W.J., 1999. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Functional Ecology 13, 650–660. Blair, J.M., Parmelee, R.W., Beare, M.H., 1990. Decay rates, nitrogen fluxes and decomposer communities in single and mixed species foliar litter. Ecology 71, 1976–1985. Bradley, R.L., Fyles, J.W., 1995. Growth of paper birch (Betula papyrifera) seedlings increases soil available C and microbial acquisition of soil nutrients. Soil Biology & Biochemistry 27, 1565–1571. Chapin III., F.S., Kedrowski, R.A., 1983. Seasonal changes in nitrogen and phosphorous fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64, 376–391. Cookson, W.R., Beare, M.H., Wilson, P.E., 1998. Effects of prior crop residue management on microbial properties and crop residue decomposition. Applied Soil Ecology 7, 179–188. Cortez, J., Bouche´, M., 2001. Decomposition of Mediterranean leaf litters by Nicodrilus meridionalis (Lumbricidae) in laboratory and field experiments. Soil Biology & Biochemistry 33, 2023–2035. Dursun, S., Ineson, P., Frankland, J.C., Boddy, L., 1993. Sulphite and pH effects on CO2 evolution from decomposing angiospermous and coniferous tree leaf litter. Soil Biology & Biochemistry 25, 1513–1525. Gholz, H.L., Wedin, D.A., Smitherman, S.M., Harmon, M.E., Parton, W.J., 2000. Long-term dynamics of pine and litter decomposition in
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