Oikos 120: 1366–1370, 2011

doi: 10.1111/j.1600-0706.2010.19418.x
© 2011 The Authors. Oikos © 2011 Nordic Society Oikos
Subject Editor: Wim van der Putten. Accepted 21 December 2010

All size classes of soil fauna and litter quality control the
acceleration of litter decay in its home environment

Alexandru Milcu and Pete Manning

A. Milcu (a.milcu@imperial.ac.uk) and P. Manning, NERC Centre for Population Biology, Division of Biology, Imperial College London,
Silwood Park, Ascot, SL5 7PY, UK. PM also at: School of Agriculture, Food and Rural Development, Newcastle Univ., Newcastle upon Tyne,
Tyne and Wear, NE1 7RU, UK.

There is increasing evidence that litter decomposition is faster beneath the plant species it was derived from, an effect called
home-field advantage (HFA). Adaptation of soil biota to decompose the litter that they encounter most often has been
proposed as the main mechanism to explain HFA. However, there is little direct evidence supporting this assumption and
the contribution of different decomposer groups to the HFA is unknown. Furthermore, the large observed variation in
the strength of the HFA may be linked to litter quality, with increasing HFA for more recalcitrant substrates. To test the
relationship between HFA, litter quality and soil fauna, we performed a field litter bag experiment, with different mesh sizes
and reciprocal litter transplants, across a successional gradient varying in litter quality inputs and soil fauna composition.
The results show that the HFA was stronger in sites dominated by more recalcitrant litter inputs and provide evidence that
a range of soil fauna size classes contribute to this effect. Our findings help explain the lack of HFA in ecosystems with
simple litters and in studies where experimental artefacts (e.g. fine mesh sizes) affect the contribution from certain classes
of soil fauna.

Litter decomposition plays a key role in ecosystem service
provision by converting plant material into easily accessible
inorganic components that are used by soil heterotrophs
and plants (Cebrian 1999, Wilkinson 2006). By producing
litters of differing chemical composition plants influence
the activity and composition of the organisms involved in
decomposition (Wardle 2002, van der Putten et al. 2009).
Correspondingly, decomposers differ in their feeding pref-
erences and physiological traits (e.g. enzyme production)
and so differ in their capacity to consume and decompose
various litters (Couteaux et al. 1995, Hättenschwiler et al.
2005). This is especially apparent during vegetation suc-
cession where temporal changes in the functioning of the
belowground compartment are ultimately determined by
changes in the traits of the dominant plant species (Wardle
2002). This interaction between litter chemical composition
and decomposers is likely to be responsible for the tendency
of litter to decompose faster beneath the plant species it
originated from than beneath other species, an effect that
has been called ‘home-field advantage’ (HFA) (Gholz et al.
2000, Vivanco and Austin 2008, Ayres et al. 2009a).
On average the HFA accelerates litter mass loss by ∼8%,
although a large amount of variation has been found (from
9% slower to 20% faster at home than away) (Ayres et al.
2009b). It has been suggested that differences in the quality
of the dominant litter in different ecosystems might explain
some of this variation. High quality litter, which is com-
posed of easily degradable compounds might be expected to
have lower HFA as most decomposers are able to consume
it. In contrast, for low-quality litter, which contains recalci-
trant and toxic secondary compounds, the HFA is expected
to be larger since only specialized decomposer communities
are able to degrade these compounds rapidly (Ayres et al.
2009b, Strickland et al. 2009). This led to the hypothesis
that the HFA results from local adaptation of the soil com-
munity to decompose litter from the plant species above
them (Wardle 2002, Bardget and Walker 2004, Ayres et al.
2009a), be it by alteration of physiological activities, shifts
in community composition, evolution, or a combination
of these processes. Whilst there is some evidence to suggest
that this occurs, few studies have specifically investigated the
role of soil communities in the HFA (Ayres et al. 2009b,
Strickland et al. 2009). There are also concerns associated
with the methodology used; short-term lab incubations
containing simplified decomposer communities and small
mesh sizes which prevent meso- and macrofaunal access,
could potentially underestimate the HFA (Ayres et al. 2006,
Chapman and Koch 2007). The exclusion of specific fauna
size classes from litterbags by using different mesh sizes
has been shown to strongly influence decomposition rates
(Setälä et al.1996, Bradford et al. 2002) and although there
are experimental caveats associated with this approach, e.g.
that microclimate is also affected, studies combing both
different mesh sizes with direct exclusions have proven the
method to be largely effective (Setälä et al. 1996, Bradford
et al. 2002).

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 To test the validity of the HFA hypothesis, the importance
of litter quality and the contribution of faunal size classes we
conducted a field litter decomposition with litters varying
in quality (lignin content) from the dominant species of a
secondary succession (Raphanus raphanistrum, Dactylis glom-
erata and Quercus petrea representing the early, mid and late
successional stage, respectively). These litters were placed in
litterbags of three different mesh sizes allowing litter access
by: 1) microflora (fungi and bacteria) and microfauna (Pro-
tozoa and Nematoda) only, 2) microflora and micro- and
mesofauna (primarily Collembola, Acari and enchytraeid
worms) and 3) microflora and all fauna size groups including
macrofauna invertebrates (such as Lumbricidae earthworms)
to access the litter. We hypothesised that the strength of the
HFA increases with successional stage and decreases with
increasing litter quality because specialist decomposers are
required to break down complex and recalcitrant litter.
Methods
Experimental setup
The study area was located at Silwood Park, southeast
England, (0°35´W, 51°25´N) at an elevation of 68 m. The
three successional sites are found within 200 m of each other
and all lie on sandy deposits, the Bagshot Sands. They con-
sist of a regularly tilled site left fallow for one year (the early
successional site), mature grassland (mid successional site)
and a deciduous forest (late successional site) (Table 1). The
early succession site was continuously cultivated since 1947
and left fallow in autumn 2006. The vegetation consists of a
mixture of ruderal herbs (R. raphanistrum, Plantago lanceo-
lata) and early successional grassland species (Poa spp., Vicia
hirsuta). The mid successional site has been grassland since
1947 and is covered by typical grassland vegetation domi-
nated by the perennial grass Dactylis glomerata. The late suc-
cessional site was also cultivated until 1947 then left fallow.
A myxoma virus outbreak in the 1960s resulted in low graz-
ing pressure by rabbits and tree recruitment. Quercus petraea
and Betula pendula are the dominant species. Details of the
Table 1. Chemical soil characteristics in the early (recently culti-
vated field), mid (grassland) and late (60-year-old deciduous wood-
land) successional sites. The pH was measured using a standard soil
water extraction. C% and N% were measured using a CNS elemen-
tal analyser. Nitrate and ammonium N were extracted from the soil
with potassium chloride solution. The nitrate is measured by cad-
mium reduction to nitrite, which is determined spectrophotometri-
cally after formation of a diazo compound between nitrite and
sulphanilamide. Ammonium is determined by formation of indo-
phenol blue by reaction with hypochlorite and phenol. Organic N
was converted to inorganic N by persulphate oxidation and the
resulting nitrate was measured as above. Available P was estimated
using the Olsen method. Data shown is an average of three repli-
cates per site, as measured at the onset of the experiment in 2006.
Characteristics/site Early Mid Late
Soil pH 5.5 5.3 4.3
C% (C-to-N ratio) 1.91% (12.1) 3.2% (12.0) 7.4% (13.3)
DIN (mg kg⫺1) 3.6 3.6 1.6
DON (mg kg⫺1) 30.4 22.2 7.4
P% (N-to-P ratio) 0.03% (13.4) 0.09% (3.0) 0.03% (5.2)
Available P (mg l⫺1) 13.3 83.3 10.0
soil chemical characteristics for the three sites as measured
in 2006 are given in Table 1. In each successional stage two
plots (Plot) of ∼ 5.5 ⫻ 3.5 m were fenced in order to pre-
vent access by rabbits and deer. Within each plot (i.e. nested
within the successional sites) the mesh sizes and litter treat-
ments where established, with four replicates per treatment
resulting in a total of 216 litter bags (three successional
stages ⫻ two plots/succession ⫻ three mesh sizes ⫻ three lit-
ter species ⫻ four replicates). The mesh size treatment com-
prised litter bags with three mesh sizes: 100 μm diameter,
allowing access to only microflora and microfauna; 1 mm
diameter, which also allows mesofauna; and 3 mm diameter
allowing also macrofauna invertebrates (see above for details
of which groups were able to access each). Senescent litters
of the three plant species were collected in autumn 2006 and
dried for three days at 50°C. Leaves and shoots were used for
Raphanus (43.9% C, 7.7% lignin, C:N ⫽ 30.8) and Dactylis
(45.6% C, 9.2% lignin, C:N ⫽ 34.9) and only leaves for
Quercus (48.4% C, 23.7% lignin, C:N ⫽ 42.0), thus simu-
lating the typical form of annual inputs. The litter bags, each
containing 3 g dry weight of plant material were placed in
the field in October 2006 by securing them with a peg on
the soil surface.
After one year of field exposure the remaining litter was
collected, dried at 50°C for 3 days and weighed. Earthworm
and mesofauna densities were assessed in spring 2007 by
sampling adjacent to the decomposition plots. Earthworms
were collected by digging and hand sorting three subplots
of 0.28 m2 (down to 60 cm depth) in each successional site.
The earthworms were counted and sorted in three func-
tional groups: epigeic (litter feeding and dwelling species),
endogeic (geophagus soil dwelling species) and anecic (lit-
ter feeding with permanent vertical burrows) (Edwards and
Bohlen 1996). Mesofauna was sampled using three soil cores
of 4 cm depth and 5 cm diameter from each successional site
followed by a 7 day Tullgren extraction.
Statistics
R Statistical package (aov function, R ver. 2.10.1) was used
to test the effect of site, litter mesh-size and their interac-
tions on arcsine transformed percentages of litter mass
loss using an ANOVA, with a mesh size within plot error
structure to account for the nested design (Crawley 2007).
ANOVA was also used to test for differences in mesofauna
abundances between the sites, whilst a multivariate approach
(MANOVA) was used to test whether there are significant
differences in the abundance of different earthworm func-
tional groups between the sites.
The HFA was calculated from the percentage litter mass
loss for the three litter species in each of the three successional
stages using a method originally introduced to calculate
HFA in sports (Clarke and Norman 1995) and subsequently
used for decomposition data by Ayres et al. (2009b). This
method allows for the HFA to be disentangled from site and
litter effects and was calculated for the three litter species
using the following four equations (modified after Ayres
et al. 2009b):
HFAi ⫽ HDDi – ADDi – H (1)
HDDi ⫽ (DiI – DjI) ⫹ (DiI – DkI) (2)
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ADDi ⫽ (DiJ – DjJ) ⫹ (DiK – DkK)
H ⫽ (HDDi – HDDj – HDDk)/(n –1)
where HFAi represents the additional decomposition at
home for species i; I, J and K are the home environments
for species i, j and k, respectively; D is a measure of decom-
position (here % litter mass loss); HDD and ADD represent
home decomposition difference and away decomposition
difference, respectively; H represents the total HFA for all
species combined; and n represents the number of species.
Results and discussion
Results were consistent with literature reports (Melillo et al.
1982, Taylor et al. 1989) in showing significant effects of
litter quality on decomposition rates, with the highest mass
loss in R. raphanistrum (62.2%), followed by D. glomerata
(52.1%) and Q. rubra (45.8%) (Table 2). Importantly, litter
type and successional stage had a significant interactive effect
on the percentage litter remaining (Table 2), showing higher
decomposition rates for litter originating in late and early
successional stages when decomposing in their own environ-
ment, but not for litter originating in the early successional
stage (Fig. 1). HFA increase from –5.4% in the early suc-
cessional stage (for R. raphanistrum) to ⫹ 6.6% in the mid
successional stage (for D. glomerata) and 19.5% in the late
successional stage (for Q. rubra). Furthermore, the three-way
interaction between succession stage, mesh size and litter
type (Table 2) shows that the HFA was differentially affected
by faunal size classes (Fig. 2). Closer examination using
Tukey’s pairwise comparison test shows that the decomposi-
tion of D. glomerata in its home environment (mid succes-
sional stage) was significantly increased by mesofauna. The
decomposition of Q. petraea, when in its own environment
(the late succession site), was stimulated by all faunal classes,
since each mesh size increase saw a significant acceleration
in Quercus decomposition at the late site but not at the
early and late succession stages (Tukey’s HSD p ⬎ 0.05). In
contrast, there was no HFA for the high quality litter of
R. raphanistrum; it decomposed just as rapidly in the mid
and late sites as at the early site (Fig. 2).
The results are consistent with the hypothesis that HFA
increases with decreasing litter quality (Ayres et al. 2009a).
Furthermore, the results emphasize that the contribution of
different faunal-sizes to the HFA varies with successional
stage. In this study the HFA effect in the late successional
stage took place through accelerated decomposition caused
Table 2. ANOVA table output on the effect of succession, mesh
size, litter type and their interactions on the litter mass loss after
one year.
Source DF F p
Succession 2,3 4.56 0.1231
Mesh 2,186 35.60 ⬍0.0001
Litter 2,186 38.63 ⬍0.0001
Succession ⫻ Mesh 4,186 2.60 0.0371
Succession ⫻ Litter 4,186 9.07 ⬍0.0001
Mesh ⫻ Litter 4,186 3.91 0.0044
Succession ⫻ Mesh ⫻ Litter 8,186 2.25 0.0256
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(3)
(4)
Figure 1. Percentage litter remaining after one year of field exposure
as affected by litter type, successional stage and their interaction.
Letter H denotes the litter species decomposing in its home envi-
ronment/ecosystem. Error bars represent ⫾ SE.
by all faunal classes, whilst in the mid successional stage this
mainly took place through mesofauna. The results correlate
well with observed differences in on macrofauna (particularly
earthworms) and mesofauna community composition in the
experimental sites. A multivariate analysis testing the effect of
successional stage on the abundance of earthworms belonging
to different functional groups (anecic, endogeic and epigeic)
found significant differences between the three sites (Pillai–
Bartlett, F2,6 ⫽ 22.9, p ⬍ 0.001). The late successional site
was dominated by the epigeic (litter feeding) woodland spe-
cies Dendrodrilus rubidus and Lumbricus castaneus (63 ind.
m⫺2) whilst the mid- and early successional site dominated
by the geophagus endogeic (soil dwelling) Aporectodea genus
(A. caliginosa, A.longa and A. rosea), with densities of 13 and
48 ind. m⫺2 for the early and mid successional sites respec-
tively. Moreover, we found significant differences between
the mesofauna densities of the sites (the summed abundance
of Collembola and Acarina; F1,6 ⫽ 20.3, p ⫽ 0.002), with
the highest at the mid (∼57 thousand ind. m⫺2), lowest at
the early (∼two thousand ind. m⫺2) and intermediate at the
late successional site (∼25 thousand ind. m⫺2). Whilst the
dominance of the woodland litter feeding earthworm species
present in the late successional site is a clear indication that
specialist species break down recalcitrant litter, the low reso-
lution of taxonomical identification for the mesofauna data
does not allow us to infer whether the increased HFA at the
mid successional stage was caused by increased densities or
the presence of more specialised mesofauna species.
There are now several strands of evidence that litter prop-
erties can influence decomposer communities, and that
these changes feedback to affect decomposition rates and
carbon cycling. Strickland et al. (2009) found very similar
results to ours, that microbial communities conditioned
to receive herbaceous (simple) inputs perceived grass litter
as of a higher quality than tree litter, while microbes from
a forest community decomposed both groups similarly.
Negrete-Yankelevich et al. (2008) and Ayres et al. (2009a)
also found that the quality of tree litter inputs could alter
the structure of soil biota communities and that home field
advantage could be observed for some species in the same
Figure 2. Percentage litter remaining after one year of field exposure, as affected by the successional stage, mesh size, litter type (Rapahnus
raphanistrum, Dactylis glomerata and Quercus rubra) and their interaction. Micro, meso and macro refers to the litter bag treatments, which
allow access to microflora and fauna, micro- ⫹ mesofauna and micro- ⫹ meso- ⫹ macrofauna, respectively. Letter H denotes the litter
species decomposing in its home environment/ecosystem. Error bars represent ⫾ SE.

Figure 3. Simplified conceptual model of decomposition in environments receiving simple (rapidly decomposing) and complex (recalci-
trant) litter substrates, with arrows representing the flow of carbon and energy. In soil environments receiving simple litters, e.g. our early
successional site, the majority of resources do not require specialist decomposers and communities of these do not develop. In those receiv-
ing more complex substrates a greater proportion of the litter inputs can only be consumed by specialist decomposers and so communities
of these thrive. The absence of this community component in soils not receiving this litter type explains the home-field advantage, while
the ubiquity of decomposers able to decompose simple substrates explains its absence in simple litter environments.

1369
system. These findings and our own lead us to propose a
simplified conceptual model of decomposition in environments
receiving simple (rapidly decomposing) and complex (recalci-
trant) litter substrates (Fig. 3). We propose that HFA effects
increase in the later stages of succession where adaptation of
soil community to more chemically complex litters with a
higher content of recalcitrant compounds becomes increas-
ingly important. Whilst the results indicate that HFA effects
increase with successional stage, the level of disturbance at the
early successional site (regular tilled) may have prevented the
soil community from adapting to the litter at that site, since
the primary determinant of soil community composition
presumably was the disturbance associates with tillage. How-
ever, in natural ecosystems disturbance and low litter quality
will often occur together but no attempts to experimentally
decouple the contribution of litter quality and disturbance of
soil biota to an overall weak HFA have been made so far.
Revealing the importance of differential contribution
of faunal size classes to the HFA may also help explain the
weaker HFA in studies performed with simplified soil com-
munities (Ayres et al. 2006) or those using mesh size that
does not allow the contribution of all faunal size classes
(Chapman and Koch 2007). In addition, the results are in
line with the increasing evidence that soil decomposer com-
munities contain little functional redundancy (Setälä et al.
2005) and that a high level of specialism exists (Bezemer
et al. 2010).
In conclusion, these findings provide evidence indicat-
ing that the importance of HFA for litter decomposition
increases with successional stage and decreases with litter
quality, and point to the importance of fauna in explaining
HFA effects. Given that decomposition is essential to nutri-
ent cycling and future plant growth these findings point to a
loose symbiosis between later successional species and their
decomposers. While this relationship has been discussed
previously (Wardle 2002) its evolutionary and ecological
consequences are yet to be fully explored.
Acknowledgements – We thank the NERC Centre for Population
Biology for funding and Angela Heim, Tom Sloan and Dennis
Wildman for helping with the experimental setup and sample anal-
yses. We also thank Eric Allan for providing data on soil mesofauna
abundance.
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