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Author's personal copy
Soil Biology & Biochemistry 43 (2011) 462e465
Contents lists available at ScienceDirect
Soil Biology & Biochemistry
journal homepage: www.elsevier.com/locate/soilbio
Short Communication
Positive relationship between herbaceous layer diversity and the performance
of soil biota in a temperate forest
Nico Eisenhauer a, *, Karen Yee b, Edward A. Johnson b, c, Mark Maraun d, Dennis Parkinson b,1,
Daniela Straube e, Stefan Scheu d
a
University of Minnesota, Department of Forest Resources, 1530 Cleveland Ave. N., St. Paul, MN 55108, USA
University of Calgary, Biogeoscience Institute, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada
University of Calgary, Department of Biological Science, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada
d
Georg-August-University Goettingen, J.F. Blumenbach Institute of Zoology and Anthropology, Berliner Str.28, 37073 Goettingen, Germany
e
University of Innsbruck, Institute of Ecology, Technikerstr. 25, 6020 Innsbruck, Austria
b
c
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 10 August 2010
Received in revised form
15 October 2010
Accepted 25 October 2010
Available online 9 November 2010
The current decline in biodiversity is particularly pronounced in the herbaceous layer of forest ecosystems. We explored the relationship between a naturally occurring plant diversity gradient in the
understory vegetation of a deciduous forest and several above-and belowground ecosystem processes.
We show that particularly soil microbial parameters and microarthropod densities are positively
correlated with plant species richness. These results confirm recent findings in grassland ecosystems and
highlight the intimate interconnectance between the diversity and functioning of above-and belowground compartments. We conclude that irrespective of a potential causal relationship between plant
species richness and belowground processes, it is essential to consider the performance of soil biota in
order to understand the relationship between herbaceous layer composition and ecosystem function.
Ó 2010 Elsevier Ltd. All rights reserved.
Keywords:
Above-and belowground interactions
Biodiversity loss
Ecosystem functioning
Litter decomposition
Soil microarthropods
Soil microorganisms
Understory vegetation
Anthropogenic alterations of Earth’s ecosystems and their
functions are substantial and multifaceted (Vitousek et al., 1997).
One major current global change phenomenon is the loss of
biodiversity (Pimm et al., 1995; Sala et al., 2000), being particularly
pronounced in the herbaceous layer of forest ecosystems (Gilliam,
2007). As the functioning of forest ecosystems essentially relies
on the composition and diversity of the herbaceous layer (Gilliam,
2007), the question arises how the latter is linked to soil biota
performance and processes (Wardle et al., 2004; Wardle, 2006;
Eisenhauer et al., 2010a). Most knowledge on the relationship
between plant diversity and the performance of soil biota is based
on manipulative semi-natural grassland experiments (Spehn et al.,
2000; Hedlund et al., 2003; Eisenhauer et al., 2009a). In forest
ecosystems, impacts of tree identity or litter diversity on soil biota
have been studied (Keith et al., 2008; Wardle et al., 2008). Only few
* Corresponding author. Tel.: þ1 612 624 6709; fax: þ1 612 625 5212.
E-mail address: [email protected] (N. Eisenhauer).
1
Deceased author.
0038-0717/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.soilbio.2010.10.018
studies considered the effects of plant diversity of the herbaceous
layer on soil microbial communities (Carney and Matson, 2005;
Royer-Tardif et al., 2010; Gilliam et al., 2010). Here, we explore
the naturally occurring gradient in herbaceous layer plant species
richness (PSR) and the linkage to above- and belowground
processes and organisms.
This study was conducted in a deciduous forest in southwest
Alberta (5120 N, 115 40 W). The dominating tree species in the
investigated forest was trembling aspen (Populus tremuloides)
interspersed with some balsam poplar (Populus balsamifera). The
herbaceous layer was dense and mainly consisted of herbs (e.g.
Aster conspicuus, Epilobium angustifolium, Delphinium glaucum,
Heracleum lanatum), roses (Rosa acicularis, Rosa woodsii) and
grasses (e.g. Bromus sp., Danthonia sp., Agropyron sp.) (Fig. 1; see
Eisenhauer et al., 2009b for plant species list). The soil was
classified as orthic grey luvisol (Karkanis, 1972). Mean annual
precipitation at the study site is 625 mm and mean annual
temperature in the organic layer 3.8 C (Mitchell, 1974).
In August 2004 and 2007, we randomly selected 10 locations per
sampling campaign, spaced >20 m apart, where we investigated
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N. Eisenhauer et al. / Soil Biology & Biochemistry 43 (2011) 462e465
463
Table 1
Table of R2- and P-values of the regressions between plant species richness of the
herbaceous layer vegetation and plant performance parameters, litter biomass, soil
microbial parameters, and the density and diversity of soil microarthropods in 2004
and 2007 (dominant taxa; see Eisenhauer et al., 2007 and Straube et al., 2009 for
details).
2004
Fig. 1. Photograph of the studied aspen forest in southwest Alberta (Canada) in 2004
showing the dense herbaceous understory vegetation, one exemplary plot, and N.
Eisenhauer assessing plant community traits (Photo by K. Yee).
plots of 0.5 0.5 m (Fig. 1). Plots studied in 2007 were >5 m from
the plots sampled in 2004, and plots were generally >20 m from
the forest edge. We determined PSR of the herbaceous layer, plant
species-specific coverage (% coverage, modified after Daubenmire,
1959), as well as plant density by counting plant tillers. Forbs
were identified to species level, whereas grasses were grouped
together. Nevertheless, we will use the term PSR in the following,
since forbs made up 72 and 75% of the plant biomass in 2004 and
2007, respectively. PSR in the plots varied between 9 and 14 species
in 2004, and between 6 and 12 species in 2007. We harvested
aboveground plant biomass by cutting the vegetation <10 mm
above the soil surface level. We then removed plant litter materials,
and both plant and litter materials were dried to constant weight
(80 C, 48 h).
Adjacent to each of the plots of the vegetation survey, we took
two soil cores using a metal corer (diameter 5 cm) to a depth of
15 cm. One of the cores was used to determine soil microbial
parameters, and the second to extract soil microarthropods by heat
(Macfadyen, 1961). Extracted soil microarthropods were stored in
70% ethanol and identified as far as possible (species to family
level). Microbial respiration and biomass were measured using an
O2 microcompensation apparatus (Scheu, 1992). Basal respiration
was determined without addition of substrate; microbial biomass
was calculated from the respiratory response to D-glucose
(Anderson and Domsch, 1978; see Eisenhauer et al., 2007 for
details).
Data were log-transformed to meet the requirements of
regressions, if necessary (plant density in 2007). Regressions were
performed between PSR and plant, microbial and microarthropod
performance parameters listed in Table 1 using STATISTICA 7
(StatSoft, Tulsa, USA). In order to illustrate results of both years in
a comparable way in the figures, variables were standardized, i.e.
minimum values ascribed “0” and maximum values “1”. According
to largely consistent relationships, we also discuss marginally
significant regressions (Table 1).
Aboveground plant biomass was not correlated with PSR
(Table 1). There was a negative relationship between PSR and plant
coverage in 2004 but not in 2007. Plant density was positively
correlated with PSR in both years (Fig. 2A). In 2007 there was
a negative correlation between PSR and litter biomass (Fig. 2B).
Microbial biomass (Fig. 2C) and basal respiration (Fig. 2D) were
R2
P
2007
R2
P
Plants
Plant biomass
Plant coverage
Plant density
Litter biomass
e
e
þ
þ
0.08
0.33
0.30
0.07
0.4185
0.0853
0.0929
0.4469
Y
[
e
þ
þ
e
0.00
0.06
0.65
0.67
0.9492
0.4962
0.0047
0.0036
[
Y
Microorganisms
Basal respiration
Microbial biomass
þ
þ
0.40
0.30
0.0508
0.0983
[
[
þ
þ
0.65
0.36
0.0050
0.0689
[
[
Mesofauna
Collembola (total)
Isotomidae
Onychiuridae
Oribatida (total)
Oppiidae
Brachythoniidae
Total density
Total diversity
þ
þ
þ
þ
þ
þ
þ
þ
0.36
0.28
0.31
0.21
0.19
0.19
0.24
0.52
0.0674
0.1143
0.0940
0.1887
0.2029
0.2121
0.1482
0.0184
[
e
e
þ
þ
þ
þ
þ
e
0.23
0.19
0.11
0.33
0.41
0.13
0.14
0.10
0.1653
0.2122
0.3536
0.0850
0.0451
0.4318
0.2829
0.3730
[
[
[
[
Significant (P < 0.05) and marginally significant (P < 0.1) effects are given in bold.
N ¼ 10, [ ¼ increase with increasing plant species richness, Y ¼ decrease, þ/
indicate the tendency of the relationships (according to positive or negative
correlation coefficients).
positively correlated with PSR. Collembola density and PSR were
positively correlated in 2004 (Fig. 2E), primarily due to high density
of Onychiuridae, but not significantly correlated in 2007. In 2007
there was a positive correlation between PSR and Oribatida density
(Fig. 2F), which was mostly due to a positive correlation between
PSR and the density of Oppiidae. While there was no correlation
between PSR and total density of soil microarthropods, total
diversity of microarthropods was positively correlated with PSR in
2004.
Forest biodiversity is largely a function of the herbaceous layer
vegetation (Gilliam, 2007). The results of the present study suggest
a positive relationship between herbaceous PSR and plant density,
soil biota performance and functions. The positive correlation of
PSR with microbial biomass, basal respiration and -in some yearspositive relationships between the density of Collembola and Oribatida and a negative correlation between litter biomass suggests
that litter diversity stimulated decomposer activity and thereby
decomposition processes. Of course, correlations do not necessarily
reflect causal relationships, and above- and belowground parameters may be driven by other abiotic or biotic conditions (Rusek,
2000; Hooper et al., 2000). However, we found no significant
relationships when we tested PSR against distance to forest edge,
tree and shrub coverage and soil water content (data not shown;
see Eisenhauer et al., 2007).
Recent findings in temperate grassland point to an intimate
relationship between the diversity and functioning of above- and
belowground compartments of terrestrial ecosystems. While soil
biota essentially rely on the quality of plant derived resources
(Wardle et al., 2004), plant performance is driven by the activity
and diversity of decomposers (Eisenhauer et al., 2009c, 2010b,
2010c). Results of the present study suggest a similar abovee
belowground interconnectance in forest ecosystems, reinforcing
previous studies on soil microbes (Carney and Matson, 2005;
Royer-Tardif et al., 2010; Gilliam et al., 2010). We conclude that,
irrespective of a potential causal relationship between PSR and
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N. Eisenhauer et al. / Soil Biology & Biochemistry 43 (2011) 462e465
Fig. 2. Regressions between plant species richness of the herbaceous layer [number of species plot1; standardized values between 0 and 1] and (A) plant density [number of tillers
plot1], (B) litter biomass [g plot1], (C) microbial biomass [mg Cmic g1 soil dry weight], (D) basal respiration [ml O2 h1 g1 soil dry weight], (E) Collembola density
[individuals m2], and (F) Oribatida density [individuals m2] (all standardized values). Black circles and solid lines indicate regressions in 2004, white circles and dashed lines
indicate regressions in 2007. Only lines of significant (P < 0.05) and marginally significant (P < 0.1) regressions are given.
belowground processes, it is essential to consider the performance
of soil biota in order to understand the relationship between the
composition of the herbaceous layer and ecosystem functions.
scholarship in 2004 and for a postdoctoral scholarship by the DFG
(German Science Foundation; Ei 862/1-1).
References
Acknowledgements
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work and laboratory analyses. Comments of Frank S. Gilliam and
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