Download Traits explain community disassembly and trophic contraction

Global Change Biology (2012) 18, 2448–2457, doi: 10.1111/j.1365-2486.2012.02725.x
Traits explain community disassembly and trophic
contraction following experimental environmental change
Z O Ë L I N D O * , J O N A T H A N W H I T E L E Y * and A N D R E W G O N Z A L E Z *
*Department of Biology, McGill University, 1205 Dr. Penfield Avenue, Montréal, Québec, H3A 1B1, Canada
Abstract
Many ecosystems are currently undergoing dramatic changes in biodiversity due to habitat loss and climate change.
Responses to global change at the community level are poorly understood, as are the impacts of community
disassembly on ecosystem-level processes. Uncertainties remain regarding the patterns of extirpation and persistence
under single vs. multiple forms of environmental change. Here, we use a trait-based and food web approach to
examine the effects of experimentally changing moisture, temperature and habitat ‘openness’ on a functionally
important group of microarthropods associated with a boreal forest floor bryosphere (detrital moss) system. Overall,
the outcome of community disassembly was mediated by the correlation between our environmental factors and
species traits, particularly body size. Minor increases in summer temperatures maintained greater species richness,
whereas drought stress had a significant negative effect on community-level abundance and richness. These effects
were reflected in modifications to the community-wide body-size spectra. Habitat openness alleviated biodiversity
loss in the larger-bodied species of the most abundant taxonomic group, but did not fully mitigate the effects of
drought. The most striking result of this experiment was an overall contraction of the food web among persistent
species under drought stress (i.e. those not extirpated by environmental change). These results suggest that major
changes in boreal microarthropod community structure are likely to occur in response to common forms of global
change. Moreover, the contraction in trophic structure even amongst tolerant species suggests that ecosystem
function within the bryosphere can be altered by environmental change.
Keywords: biodiversity loss, body size spectra, climate change, community disassembly, habitat fragmentation, natural
abundance stable isotopes, traits, trophic space
Received 20 December 2011; revised version received 5 March 2012 and accepted 17 April 2012
Introduction
Habitat fragmentation and climate change jointly affect
biodiversity directly and indirectly, by modifying
interactions between persistent species (Gonzalez et al.,
2011). Anthropogenic change, such as habitat loss and
fragmentation, has been shown to induce nonrandom
extinction (Didham et al., 1998; Holt et al., 1999;
Holyoak, 2000; Duffy, 2003; Staddon et al., 2010) and
the attrition of species interactions (Borrvall & Ebenman,
2006): a process termed community disassembly.
Recently changes in climate variables, such as temperature and moisture, have been identified as key factors
exacerbating the negative effects of habitat loss on
biodiversity (Mantyka-Pringle et al., 2012). It is now
recognized that interactions between multiple stressors
may lead to nonadditive outcomes (Vinebrooke et al.,
Present address: Zoë Lindo, Department of Biology, University of
Western Ontario, Biological and Geological Sciences Building,
London, Ontario, N6A 5B7, Canada.
Correspondence: Zoë Lindo, tel. + 519 661 2111 ext 82284,
Fax + 519 661 3935, e-mail: [email protected]
2448
2004; Brook et al., 2008; Darling & Côté, 2008), yet the
rate and scale of biodiversity loss due to the effects of
climate change and habitat fragmentation are not well
understood. There is therefore a clear need to understand how communities and ecosystems will respond
to rapid cumulative environmental change of different
types.
It has been suggested that species loss during community disassembly is trait-mediated (Zavaleta et al.,
2009), and may be predictable if knowledge of the functional traits involved in the response to environmental
change is available. Trait-based approaches can predict
patterns of extinction and persistence, because the
distribution of trait values can affect the potential of a
population to persist or perish under a set of environmental conditions (Norberg et al., 2001; Webb et al.,
2002). For example, extinction risk under habitat loss
and fragmentation is associated with traits such as high
trophic position, large body size and poor dispersal
ability (Didham et al., 1998; Gonzalez & Chaneton,
2002; Cardillo, 2003). However, traits involved in the
response of a species to one environmental stressor
may not be relevant in responding to others: e.g.
© 2012 Blackwell Publishing Ltd
S P E C I E S T R A I T S E X P L A I N C O M M U N I T Y D I S A S S E M B L Y 2449
dispersal traits in fragmented landscapes vs. drought
tolerance in the response to climate change. Furthermore, when selective extinctions occur during community disassembly, changes in species abundances,
composition and the nature of interspecific interactions
are expected to impact ecosystem processes through
changes in community trophic structure, biomass and
nutrient assimilation rates (Larsen et al., 2005). Species
that persist following community disassembly may
have significantly altered ecological roles (Layman
et al., 2007b). Body size as a general morphological trait
can predict species loss and be related to trophic transfer efficiency, as it is often correlated with many other
functional traits and demographic processes (Woodward et al., 2005). The body size spectrum (BSS), which
represents the relationship between body size and
abundance (or biomass), has been suggested as an integrative measure of community structure (Woodward
et al., 2005) and a good indicator of ecological change
(Petchey & Belgrano, 2010).
Few experiments have sought to identify the traits
associated with species extinctions and persistence, or
examined the subsequent effects on community trophic
structure. Here, we use a bryophyte-microarthropod
detrital system (the bryosphere sensu Lindo & Gonzalez,
2010) as a natural model system to experimentally test
the effects of combined global change factors on biological communities. The bryosphere is a species-rich
system with a detrital food web spanning multiple
trophic levels, and is easy to manipulate in the field. In
addition, shifts in bryosphere microarthropod communities have direct effects on the microbial components
of detrital systems which perform carbon and nitrogen
cycling, and have resolute and long-term consequences
for ecosystem functioning in boreal and temperate
forests. We examine the effects of increased temperature, drought stress and habitat ‘openness’ on soil
microarthropod traits and community disassembly.
Following 2 years of treatment we: 1) assessed the
biodiversity (species abundance, richness); 2) correlated
species-specific traits with temperature, drought and
openness treatments to describe the process of
community disassembly; and 3) described changes in
community-level patterns of persistent species trophic
functioning. We predicted communities under drought
stress would experience species loss (extirpation)
associated with specific traits related to drought
tolerance, but that increased ‘openness’ would mitigate
species loss through immigration from the external
habitat matrix. At the community-level, we expected
shifts in body size spectra and changes in the
trophic space of persistent species associated with
changes in resources and species interactions following
community disassembly.
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
Materials and methods
Study system
Our experimental field site was located in the subarctic-boreal
forest region near the town of Schefferville, in northern Québec, Canada (54°48′ N, 66°49′ W). This area is characterized by
short, cool summers and long, cold winters with mean
monthly temperatures ranging from 24 °C in January to 12 °C
in July (Environment Canada, 2011). The growing season at
Schefferville is short (100–120 days), with frequent cloud
cover (Lechowicz & Adams, 1978). The mean annual precipitation is 823 mm with 408 mm in the form of rain (Environment Canada, 2011). The area is a transitional zone between
boreal forest and tundra with typically well-drained, nutrientpoor podzolic (Brunisols) soils (Moore, 1980). The dominant
tree species is black spruce [Picea mariana (Mill.) B.S.P.] with
patches of white spruce [Picea glauca (Moench) Voss] and tamarack [Larix laricina (Du Roj) Koch]. The understory is patchy
and contains dwarf birch (Betula glandulosa Michx.) and Labrador tea (Ledum groenlandicum Oeder.). The ground cover is
nearly continuous with the feathermoss Pleurozium schreberi
[(Brid.) Mitt.]; infrequently, the moss species Ptilium cristacastrensis (Hedw.) and Hylocomium splendens (Hedw.) occur.
Patches of Reindeer lichen [Cladonia alpestris (L.) Rabh.] are
common in nearby areas.
The experimental area was composed of eight replicate
sites (blocks) within a 2.4 hectare area. Our site development
and sampling occurred in contiguous areas of P. schreberi.
Within each site, replicate plots were created on the forest
floor in 2007 for destructive sampling in 2008 and 2009. Plots
consisted of individual patches of P. schreberi moss that were
either contained within 115 cm wide hexagonal open-topped
chambers (OTC) or left under ambient conditions. Within the
chamber treatments, the OTCs created a strong moisture
gradient by acting as a rain shadow at the periphery of the
chamber (effectively 25 cm wide) while the area in the
middle of the OTC received precipitation similar to ambient
conditions. The effect of the OTC increased the temperature
at the soil surface by an average of 0.5 °C over the year,
driven mainly by a 2 °C increase in daily maxima during the
summer months.
Moss patches (12.5 cm diameter 9 9 cm deep) were cut
from the surrounding matrix, placed in plastic plant pots, then
exposed to one of four treatments: 1) outside of the OTC under
ambient conditions (ambient), 2) within the inner area of the
OTC (inner), 3) at the outer periphery of the OTC (outer), or 4)
at the outer periphery of the OTC but open to the surrounding
moss habitat by two, 3 cm wide openings on each side (corridors). We use the ambient moss patches as a control to explore
the effects of temperature, moisture and ‘openness’ on community disassembly: differences between ambient and innerchamber patches test the effect of temperature (contrast 1),
differences between inner-chamber patches and outer-chamber
patches test the effect of drought (contrast 2) and differences
between outer-chamber patches with and without corridors test
the effect of openness in the presence of drought (contrast 3).
Moss patches were collected during the peak dry period
(August) following 1 and 2 years in the field. Microarthropods
2450 Z . L I N D O et al.
were extracted from the moss using Tullgren funnels over
48 h into 75% EtOH, then identified and enumerated. Moss
samples were weighed prior to and immediately following
extraction to gravimetrically calculate the moisture content of
individual patches (moisture content % = ([wet weight
(g)
dry weight (g)]/dry weight (g))*100). Microarthropod
abundance and species richness were standardized by dry
weight (dwt) of substrate sampled, and are expressed as the
number of individuals or number of species per gram dry
weight respectively. Body mass of each species was estimated
using average length and width measurements from representative types of adults and immatures converted to mass (lg)
using Caruso & Migliorini (2009).
We characterized the species in our samples according to
26 trait states related to life history and morphological
characteristics. Traits hypothesized to be relevant in coping
with environmental change were considered a priori (Supporting Information Table S1). Body size was measured from
body mass calculations; desiccation tolerance was categorized from Spearman rank coefficient (r) of the correlation
between species abundance and moisture content at the
patch level. Sclerotization (or mineralization) of the cuticle
was categorized based on body colour and hardness. Species
were grouped into seven feeding guilds (algivores, fungivores, detritivores, lichenivores, herbivores, omnivores and
predators), two reproductive modes (asexual-parthenogenetic, sexual) and three levels of taxonomic uniqueness.
Taxonomic uniqueness was binned as three categories
dependent on the number of known species in a family: low
diversity (<3), moderate (3–15) and high diversity (>15). Life
history traits were assigned at the genus and species level
for oribatid mites and at the family level elsewhere based on
the literature and personal communication with taxonomic
experts.
A subset of ten species from 2009 ambient and outer-chamber samples were analysed for natural abundance 15N/14N
and 13C/12C stable isotopes. Species were selected on the
basis of being consistently present in both ambient and outer
patches with a biomass that allowed accurate stable isotopic
analysis. Individuals were handpicked from ethanol into tin
capsules and dried at 60 °C for 24 h. Samples were weighed
and stored in a desiccator until analysed. Each sample consisted of 1–450 individuals pooled from each patch to obtain
sufficient biomass for analyses. The same ten species from
replicate ambient and outer patches were analysed. Samples
were shipped to the UC Davis Stable Isotope Facility for analysis of 13C and 15N isotopes using a PDZ Europa ANCA-GSL
elemental analyser interfaced to a PDZ Europa 20-20 isotope
ratio mass spectrometer (Sercon Ltd., Cheshire, UK). The
final delta values are expressed relative to international standards V-PDB (Vienna PeeDee Belemnite) and Air for carbon
and nitrogen respectively. The stable isotopes of ten species
were compared between ambient and outer treatments, using
six metrics (Layman et al., 2007a): d15N range (NR), d13C
range (CR), total area (TA), mean distance to centroid (CD),
mean nearest neighbour distance (NND) and standard deviation of nearest neighbour distance (SD NND). All metrics
were calculated in R version 2.14.1 (R Development Core
Team, 2011).
Statistical analyses
Moisture content was analysed using a two-way analysis of
variance (ANOVA) with treatments crossed by year. A two-way
multivariate analysis of variance (MANOVA) was used to compare the species richness and abundance of taxonomic groups
among treatments and years (overall Wilk’s k and univariate
F values given) in STATISTICA 7.0 (StatSoft, Inc., 2004). Standardized microarthropod abundances, per g dry weight of substrate, were log transformed (x + 1) prior to analyses. We
focused on overall effects of temperature, drought and openness on abundance and richness using a planned contrast that
reflected our experimental design: (1) differences between
ambient and inner-chamber patches (temperature), (2) differences between inner-chamber patches and outer-chamber
patches (drought) and (3) differences between outer-chamber
patches with and without corridors (openness).
We use the body size spectra (BSS) as an integrative measure of the microarthropod community structure (Woodward
et al., 2005) due to the metabolic underpinnings of the body
size scaling, and the relationship between body size and
numerous species traits (Woodward et al., 2005). The log-log
relationship between average standardized abundance of each
species and their body size was analysed by quantile regression using the package ‘quantreg’ (Koenker, 2005) in R version
2.14.1 (R Development Core Team, 2011). The 75th quantile
was used for the regression as it eliminated spurious results
due to nonabundant species being present or absent, thus
examines the BSS relationship in the most abundant species.
We tested a null hypothesis of equal slopes across all treatments by comparing a series of nested models using a Wald
test (Bassett & Koenker, 1982): a full model that allows slopes
and intercepts to vary across treatments, a model with a single
slope (equal across treatments) and different intercepts for
each treatment and a simple model with a single slope and
intercept (no treatment effect). Nested models are compared
with the full model, such that a rejection of the null hypothesis
(P < 0.05) indicates that the extra terms in the full model not
included in the nested model are not equal, and therefore
represent the data more accurately.
We use two methods to link the traits of the bryofaunal species to our environmental treatment variables: RLQ analysis
(Dolédec et al., 1996) and fourth-corner analysis (Legendre
et al., 1997; Dray & Legendre, 2008). The RLQ analysis consists
of a multivariate ordination of species abundance data (L) constrained by species trait data (Q) and environmental data (R),
whereas fourth-corner analysis quantifies and tests the correlation between the variables in Q and R. A total of 32 patches
and 25781 individuals belonging to 110 species were included
in the analysis (Table S1). Three separate ordinations of the R,
L and Q tables were performed prior to the RLQ analysis. The
species abundance matrix L (J 9 I) containing the number of
individuals in each species (J) occurring in each sample (I)
was analysed by correspondence analysis (CA). The environmental variables (table R) and species traits (table Q) were
analysed using principal component analysis (PCA), with row
weights and column weights of table L respectively. The sites
and species scores (or coordinates) from the species CA are
used to link the R and Q tables, as sites are shared by R and L,
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
S P E C I E S T R A I T S E X P L A I N C O M M U N I T Y D I S A S S E M B L Y 2451
and species are shared by Q and L. Moisture content was binned into five moisture categories while dummy variables were
used for other environmental treatment variables; all species
trait states were expressed as dummy variables. A single inertia analysis (RLQ analysis) was conducted on the cross-matrix
of tables R, L and Q. The statistical significance of the relationship between the environmental attributes (R) and species
traits (Q) was assessed by comparing 999 Monte Carlo permutations of the rows of tables R and Q with the total inertia in
the RLQ analysis (Dolédec et al., 1996). Fourth-corner analysis
(Legendre et al., 1997; Dray & Legendre, 2008) was used to
quantify and test the relationship between environmental variables and species trait states. The fourth-corner statistic corresponds to a Pearson product-moment correlation measuring
the link between species abundances, environmental treatment variables and species traits. The RLQ and fourth-corner
analyses were conducted using the ade4 package (Chessel
et al., 2004) in R version 2.14.1 (R Development Core Team,
2011).
(a)
(b)
Results
As expected, moisture content of the moss patches was
significantly different among the environmental climate
treatments (F3,24 = 35.10, P < 0.001), with significantly
greater moisture occurring in the ambient and innerchamber patches compared with the outer-chamber
patches with or without corridors (contrast 2: t = 7.44,
P < 0.001) (Fig. 1a); there was no difference in moisture
between the 2 years of sampling (F1,24 < 0.01, P = 0.990).
Moisture content had an overwhelming effect on species abundance and richness. Overall bryofaunal abundance was significantly greater in wetter (ambient and
inner-chamber) patches (Wilks k = 0.223, F18,54.2 = 2.11,
P = 0.018) than dry outer and corridor patches (Fig. 1b);
univariate statistical results for treatment effects on
abundance are summarized in Table 1. Overall species
richness at the individual patch level was significantly
affected by both year (Wilks k = 0.522, F6,54.2 = 2.90,
P = 0.035) and environmental treatment (Wilks
k = 0.128, F18,54.2 = 3.23, P < 0.001). Species richness
results differ qualitatively from patterns observed in
species abundances, whereby the inner-chamber
patches had significantly greater species richness than
the two dry outer-chamber patch treatments (outer,
corridors), but the ambient treatment patches were not
significantly different from either set of treatments and
had intermediate overall species richness (Fig. 1c). At
the individual taxonomic group level, all groups had
significantly greater richness under inner-chamber vs.
ambient (contrast 1) and outer drought conditions (contrast 2), whereas the dominant taxonomic group, the
oribatid mites, also demonstrated significantly greater
species richness within dry corridor patches compared
with the dry, but isolated, outer patches (contrast 3)
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
(c)
Fig. 1 (a) Moisture content (% of dry weight) of moss substrate
collected from experimental landscapes 1 year (2008) and
2 years (2009) following induced environmental change. (b)
Species abundances (# individuals/g dwt) of microarthropod
groups within climate change experiment. (c) Species richness
(# species/g dwt) of microarthropod groups within climate
change experiment. Error bars are standard deviations.
(Table 1). The year effect was driven by a significant
reduction in the number of collembolan species
collected per patch in 2009 (F1,24 = 10.88, P = 0.003).
Quantile regression on the body size spectra (BSS)
revealed that species abundances declined significantly
with body size (overall regression equation: log
2452 Z . L I N D O et al.
Table 1 Univariate results of MANOVA test for standardized taxonomic group abundance and species richness. A priori contrast
results are given demonstrating a significant individual effect of increased temperature (contrast 1: ambient vs. inner), drought stress
(contrast 2: inner vs. outer), or habitat openness (contrast 3: outer vs. corridor); nonsignificant results not shown
Univariate results
Significant contrasts
F (3, 24)
P
Temperature (1)
Drought (2)
Abundance
Oribatida
Prostigmata
Collembola
Mesostigmata
Astigmata
Others
12.17
5.95
9.08
13.19
9.5
4.22
<0.001
0.003
<0.001
<0.001
<0.001
0.016
–
–
–
–
–
–
t
t
t
t
t
t
=
=
=
=
=
=
5.18, P
3.72, P
3.85, P
4.99, P
4.06, P
3.51, P
<
=
<
<
<
=
0.001
0.001
0.001
0.001
0.001
0.002
–
–
–
–
–
–
Species richness
Oribatida
Prostigmata
Collembola
Mesostigmata
Astigmata
Others
9.01
6.73
13.63
11.16
5.57
9.97
<0.001
0.002
<0.001
<0.001
0.004
<0.001
t
t
t
t
t
t
t
t
t
t
t
t
=
=
=
=
=
=
5.19, P
4.15, P
5.19, P
5.13, P
4.05, P
4.99, P
<
<
<
<
<
<
0.001
0.001
0.001
0.001
0.001
0.001
t=
–
–
–
–
–
=
=
=
=
=
=
2.80, P
2.47, P
2.17, P
2.35, P
2.44, P
2.58, P
Fig. 2 The relationship between the average standardized
abundance of each microarthropod species with body size (loglog scale) for all species within ambient, inner (temperature),
outer (drought) and corridor (openness) treatments. Lines show
the 75% quantile regression for each treatment.
(abundance) = 1.60–0.30
log
(mass);
(intercept:
P < 0.001, slope: P = 0.001)) (Fig. 2). Although dry outer
patches demonstrated a steeper slope (-0.46) than other
treatments (ambient = 0.34; inner = 0.31, corridor =
0.31), this relationship was not significantly different
among treatments (F3, 432 = 0.22, P = 0.883). Similar to
results of manova for the overall abundances, abundance values represented by the intercept of the BSS
relationships (log-log scale) were significantly different
=
=
=
=
=
=
0.010
0.021
0.040
0.028
0.022
0.016
Openness (3)
2.53, P = 0.018
among wet (ambient = 1.91, inner = 2.06) and dry
(outer = 1.36, corridor = 1.38) treatments (F6,432 = 5.63,
P < 0.001); abundance was slightly, although nonsignificantly, increased under warming (inner) conditions
compared with ambient (Fig. 2).
The first two axes of the RLQ analysis explained
68.9% and 19.0% of the total variance of the cross-matrix
of the species traits and environmental variables respectively. Random permutations of the rows of the R and
Q tables indicated a significant (P = 0.003) association
of the co-structure between species traits and environmental variables. The proportion of variance accounted
for by the RLQ analysis was compared with that resulting from the separate analyses of the individual matrices. The RLQ axis 1 accounted for 63% and 81% of the
potential variability of the first axis in the separate analyses of the species traits and environmental variables:
i.e. the ratio between the variance of the environmental/trait characteristics in RLQ and the variance of the
environmental/trait characteristics in the separate analysis. Because the RLQ analysis maximizes the covariance between the species traits and the environmental
variables, species abundance explains less variance in
the first axis (48%) (Table 2). This first axis represents
the majority of the variance among the environmental
dataset and corresponds to inner-chamber patches that
were wet or had high moisture content vs. outer patches
with and without corridors; the second axis represents
patches that were strongly dry vs. those with moderate
moisture conditions (Fig. 3a). For the species trait dataset this first axis divided species among reproductive
strategy (sexual, asexual) and taxonomic uniqueness
(Fig. 3b). The second axis, while contributing only 19%
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
S P E C I E S T R A I T S E X P L A I N C O M M U N I T Y D I S A S S E M B L Y 2453
Table 2 Comparison of variation explained (%) by RLQ analyses with variation explained in the separate analyses of three
matrices (R matrix: environment 9 site; L matrix: species 9 site; Q matrix: species 9 trait). In the separate analysis,
the environmental variables and species traits were analysed
using principal component analysis (PCA); the species
abundances were analysed by correspondence analysis (CA)
(a)
Separate analyses
% variance
explained by axis 1
R/PCA
14.3
L/CA
37.7
Q/PCA
19.6
RLQ analysis
R/RLQ
L/RLQ
Q/RLQ
% variance
explained by axis 2
13.4
30.0
12.8
% variance
explained by axis 1
% variance
explained by axis 2
63.1
47.7
81.0
57.6
54.5
83.1
of the variation in the RLQ analysis of the trait data
reveals an interesting subset of species that are highly
desiccation tolerant despite being small-bodied (0-5 lg)
and not sclerotized. The fauna associated with this
group comprised five species of small prostigmatid
mites in the families Tydeidae and Eupodidae. Permutation tests reveal numerous correlations between environmental variables and species trait states that were
significantly different from random (Fig. 3c). None of
the species traits correlated with ambient vs. chamber
treatments per se at the plot level; however, many traits
were significantly positively or negatively correlated
with the effects of the OTC, in particular moisture content of the patches as dictated by patch arrangement
within the chambers (Fig. 3c). The highest correlation
(R = 0.45, P < 0.001) was between highly desiccationtolerant species and dry habitat patches.
The trophic space of persistent species within outerchamber treatments demonstrated a distinct vertical
contraction of the diet (d15N range) compared to trophic
space of the same species under ambient conditions
(Fig. 4). Community trophic metrics d15N range, total
area, average distance to nearest neighbour and the
standard deviation of nearest neighbour distances, all
decreased in outer-chamber treatments compared with
ambient conditions, whereas d13C and distance-tocentroid values increased (Table 3).
(b)
(c)
Fig. 3 The results of RLQ analysis indicating associations along
the first two axes between (a) environmental descriptors and (b)
microarthropod species traits. (c) Fourth-corner correlations
between species trait states (rows) and environmental variables
(columns) at the patch level. White boxes indicate no significant
correlation, grey boxes indicate significant negative relationship,
black boxes indicate significant positive relationship.
Discussion
Nonrandom community disassembly has been shown
in response to habitat fragmentation (Gonzalez et al.,
1998; Staddon et al., 2010), where extinction risk is often
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
associated with higher trophic position, larger body
size and smaller local population densities. Our data
suggest that specific correlates of extinction associated
2454 Z . L I N D O et al.
gradients. The strong negative effect of drought was
also evident in our measures of species richness; yet
habitat openness to the surrounding matrix partially
mitigated this effect, at least in the dominant taxa.
Habitat connectivity has been shown to increase the
ability of communities to recover from perturbation
through recolonization events (Gonzalez et al., 1998;
Starzomski & Srivastava, 2007), and even mitigate the
negative ecosystem-level effects of fragmentation (Staddon
et al., 2010). Dispersal from surrounding habitats may
become increasingly important as the overall habitat
quality decreases, such as under drought stress. Immigration from adjacent high-quality (moist) areas may
have boosted species richness and increased long-term
survival of metapopulations (Gonzalez & Chaneton,
2002; Binzenhoefer et al., 2008), although no effect of
the corridor treatment was observed for patterns of
abundance. Chisholm et al. (2011) found that despite
extreme drought conditions in an experimental bryosphere system, poor-quality drought patches adjacent
to high-quality wet patches maintained species richness
through mass effects driven by dispersal. While corridor
patches were within the drought-stress peripheral zone
of the OTC, as was the moss matrix immediately surrounding the corridor patches, good-quality moist habitat conditions existed within 10 cm, allowing colonists
with the ability to disperse to access the corridor
patches.
Abundance generally declines with increasing body
size and an efficient transfer of energy is characterized
by a shallow negative slope in body size spectra (BSS).
Although the slope of the BSS was nonsignificantly different among treatments, the dry outer habitats demonstrated a steeper negative slope that points to a less
efficient transfer of energy among these food webs
(Sheldon et al., 1972; Petchey & Belgrano, 2010). This
supports the idea that changes in basal resources, possibly alterations in the microbial portion of the food web,
had cascading bottom-up effects on microarthropod
consumers. For example, Mulder & Elser (2009) found
that steeper size spectra slopes were associated with
changes in nutrient status of grassland soils, in
particular decreases in carbon and nitrogen availability.
Furthermore, there is some indication that the steeper
BSS slope under drought stress is mitigated in corridor
Fig. 4 Average (± SE) delta 13C and delta 15N values for the
same ten microarthropod species collected in ambient and outerchamber (drought) treatments. Shown is convex hull area of
community within ambient (dashed line, shaded) and outer-chamber
treatments (black line). Data points outside of the convex hull area
are moss-detrital samples for the two treatments.
with drought are different from those associated with
habitat loss in the moss-microarthropod system. We
found that some of the smallest fauna in our experiment persisted under drought conditions, despite possessing traits not usually associated with drought
tolerance, and that habitat openness mitigated some
species loss under drought conditions. Thus, a combination of species-specific environmental tolerances
combined with differential dispersal abilities of species
appear to have contributed to the nonrandom patterns
of microarthropod community composition in our
experimental habitats.
The OTCs produced a strong moisture gradient
among moss patches associated with their position
within the chambers. Drought stress had an
overwhelming effect on bryofauna communities after 1
and 2 years in the field. Moisture content of the moss
habitat was the biggest explanatory variable in our
measures of bryosphere faunal abundance, where
patterns of abundance in all groups followed moisture
Table 3 Community-wide stable isotope metrics associated with Fig 4. Stable isotopes of ten microarthropod species were
explored using six community-wide metrics: [d15N range, d13C range, total area based on convex hull, mean distance to centroid,
mean nearest neighbour distance (NND) and standard deviation of nearest neighbour distance (SD NND)] as described in Layman
et al. (2007a) for ambient and outer treatments
Ambient
Outer
d15N range
d13C range
Total area
Centroid distance
Mean NND
SD NND
15.43
7.21
4.24
5.13
45.78
28.07
1.98
3.00
1.98
1.51
1.49
0.96
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
S P E C I E S T R A I T S E X P L A I N C O M M U N I T Y D I S A S S E M B L Y 2455
treatments, as increased abundances of larger-bodied
species relative to outer patches resulted in a shallower
BSS slope.
Our trait-based approach explained a significant proportion of the community response. We found that the
bryofaunal assemblage could be roughly divided into
four trait-based groups responding to changes in environmental treatments. First, a group of small, unsclerotized, Prostigmatid mites was tolerant to the drying
effects of the outer-chamber patches; when all other
groups of fauna were extirpated from the drought
patches, these Tydeid and Eupodid mites persisted.
The second group was drought intolerant, asexual,
mainly Oribatid mites (Oppiidae, Suctobelbidae, Tectocepheidae) and the third group was medium-sized
detritivores that demonstrated a unimodal relationship
with moisture. Drought conditions are known to act as
an environmental filter, producing progressively nested
communities composed of species tolerant to dry conditions (Lindo et al., 2008). Although all species had significantly reduced abundances under drought
conditions, a particular subset of the fauna consistently
persisted, albeit in low abundances.
Changes in overall richness and abundance were
positively and significantly associated with moisture
availability within habitat patches (see also Siepel, 1996;
Frampton et al., 2000; Tsiafoulia et al., 2005; Lindo &
Winchester, 2008; Kardol et al., 2011). However, the
fourth trait group, found among the corridor treatments
representing ‘openness’ of the fragmented system
under drought conditions, demonstrated dispersalrelated traits. Habitat openness increased species
richness under drought-stress conditions, due to the
presence of well-sclerotized, sexual species in the highdiversity and derived families of Mycobatidae and
Ceratozetidae (Acari: Oribatida). We have yet to fully
explain this result. The higher level of sclerotization
may have increased these species ability to resist
desiccation, but these species were not present in dry
outer patches that restricted fauna movement.
Nevertheless, the significance of sexual reproductive
mode and high-diversity taxa in association with habitat openness was unanticipated. Lindberg & Bengtsson
(2005) found that sexual microarthropod species were
less impacted by drought stress than asexual species,
but asexual species were able to recover faster than
sexual species. Sexual species are thought to have an
advantage in unstable and limited resource conditions,
whereas asexual species are thought to have greater
colonization and growth rates (Bell, 1982; Norton,
1994). Moreover, sexual species may be more dispersive
on average than asexual species, as sexual species need
to seek mates, or in this case spermatophores. However, there is currently no evidence that sexual and
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2448–2457
asexual bryosphere microarthropods differ in their dispersal capability.
Elevated temperature under nondrought conditions
in the inner patches as compared to the ambient patches
also increased the number of species present. We posit
that changes in the microbial community under wet,
warmed conditions could have elicited this response.
Shifts in microbial community composition under elevated temperature have been reported (Zogg et al.,
1997; Gray et al., 2011) with functional implications for
nutrient dynamics and potential cascading effects
through the detrital food web (Wardle et al., 1999).
Decreases in richness and abundance in the outer treatments may have been further exacerbated by correlations among drought and temperature tolerances
(Siepel, 1996; Blankinship et al., 2011), yet it was difficult to disentangle these effects given the strong effect
of drought stress and lack of drought-without-warming
treatments. The effects of experimental warming and
altered precipitation on soil biota have been equivocal
(Blankinship et al., 2011) and other components of the
bryosphere community are likely more impacted by
drought stress than microarthropods (e.g. enchytraeids;
Maraldo & Holmstrup, 2009). Climate warming and
changes in precipitation regimes are expected to have
direct impacts on soil organisms and consequently ecosystem-level processes such as nutrient and energy
fluxes (Swift et al., 1998; Wardle et al., 1998; Hunt &
Wall, 2002).
Species which persist following environmental
change have altered ecological roles as seen in our measures of trophic space and the community-level contraction in diet. Stable isotopic analysis revealed that
the same species differed in d13C and d15N under ambient conditions vs. following 2 years of summer
drought. At the community level, this lead to a
decrease in the range of d15N indicating that trophic
position was reduced in some species and increased in
others. This trophic contraction suggests a long-term
consequence of community disassembly as stable isotopes are integrative measures of feeding over space
and time. We posit that changes in resource availability
and associated bottom-up responses, as suggested
through the analysis of the body size spectra, explain
both downward and upward shifts in trophic position.
Results such as this further corroborate that it is not
only species loss, but also the functional roles of the
species that persist, which will dictate how ecosystem
function will alter under global environmental change
scenarios.
There is a growing body of scientific literature recognizing and addressing community and ecosystem
responses to multiple, interacting elements of global
change (Travis, 2003; Darling & Côté, 2008), yet the
2456 Z . L I N D O et al.
number of experiments which study multiple stressors
is small compared with single-stressor experiments
(Rustad, 2008). Evidence for interactive effects of climate (drought) and habitat openness in this study was
taxon dependent at the family level, which resulted in
divergent trait-based responses within the Oribatid
mite suborder, and the overall assemblage. In this
study, a trait-based approach has advanced our understanding of how environmental change can alter community structure. We found that harsh environmental
conditions (drought stress) initiate a process of community disassembly that differs from other habitat alterations such as fragmentation or habitat loss, but that the
combination of species-specific environmental tolerances and spatial constraints (dispersal capabilities) of
the landscape ultimately interact to structure community composition. A trait-based approach may help us
form an understanding of the community disassembly
process under different environmental conditions, and
identify previously unknown relationships, such as that
between sexual reproduction, high within-group taxonomic diversity and dispersal/corridor use. The next
step to extend this framework of community disassembly
and biodiversity loss is to link changes in communitylevel frequency trait distributions to ecosystem-level
processes and ecosystem function (Lavorel & Garnier,
2002). As demonstrated by changes in trophic space of
persistent species under drought stress, we predict that
ecosystem-level processes are affected by observed
changes in species trait distribution via community
trophic structure, biomass and nutrient assimilation
rates.
Acknowledgments
We thank the McGill Sub-arctic Field Station support crew
(Oksana Choulik) for support, and Graham Bell for use of his
ultra-microbalance. We acknowledge funding from the Natural
Sciences and Engineering Research Council of Canada, the Canada Research Chair Program, Indian and Northern Affairs Canada and Fonds Quebecois de la Recherche sur la Nature et les
Technologies. The helpful comments of the subject editor and
anonymous reviewers significantly improved this manuscript.
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Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Table S1. Species and trait states for the bryosphere microarthropod community at Schefferville, Quebéc. Species
standardized average abundances (no. individuals per g
dwt moss) are given for each experimental treatment. Standard errors in parentheses.
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