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Environmental Management
ISSN 0364-152X
Volume 48
Number 5
Environmental Management (2011)
48:1000-1012
DOI 10.1007/s00267-011-9750-0
Taxonomic and Functional Responses
to Fire and Post-Fire Management of a
Mediterranean Hymenoptera Community
Eduardo Mateos, Xavier Santos & Juli
Pujade-Villar
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Taxonomic and Functional Responses to Fire and Post-Fire
Management of a Mediterranean Hymenoptera Community
Eduardo Mateos •Xavier Santos •Juli Pujade-Villar
Received: 13 April 2011 / Accepted: 29 August 2011 / Published online: 24 September 2011
ÓSpringer Science+Business Media, LLC 2011
Abstract Fire is one of the commonest disturbances
worldwide, transforming habitat structure and affecting
ecosystem functioning. Understanding how species respond
to such environmental disturbances is a major conservation
goal that should be monitored using functionally and taxo-
nomically diverse groups such as Hymenoptera. In this
respect, we have analyzed the taxonomic and functional
response to fire and post-fire management of a Hymenoptera
community from a Mediterranean protected area. Thus,
Hymenoptera were sampled at fifteen sites located in three
burnt areas submitted to different post-fire practices, as well
as at five sites located in peripheral unburnt pine forest. A
total of 4882 specimens belonging to 33 families, which were
classified into six feeding groups according to their dietary
preferences, were collected. ANOVA and Redundancy
Analyses showed a taxonomic and functional response to fire
as all burnt areas had more Hymenoptera families, different
community composition and higher numbers of parasitoids
than the unburnt area. Taxonomic differences were also
found between burnt areas in terms of the response of
Hymenoptera to post-fire management. In general the num-
ber of parasitoids was positively correlated to the number of
potential host arthropods. Parasitoids are recognized to be
sensitive to habitat changes, thus highlighting their value for
monitoring the functional responses of organisms to habitat
disturbance. The taxonomic and functional responses of
Hymenoptera suggest that some pine-forest fires can
enhance habitat heterogeneity and arthropod diversity, hence
increasing interspecific interactions such as those estab-
lished by parasitoids and their hosts.
Keywords Biodiversity conservation Disturbance
Iberian Peninsula Parasitoids Arthropods
Introduction
Understanding the response of species to environmental
changes is vital in order to predict their effects on biodi-
versity through complex ecological processes and species
interactions (Bengtsson and others 2000). Both global
environmental changes and local disturbances exert strong
impacts that can result in loss of diversity and changes in
dominant species (Thomas and others 2004; Wood and
others 2000). These effects can be of concern for conser-
vation when threatened species are involved in these
changes. Wildfires are considered to be amongst the dis-
turbances that cause the greatest impact on ecosystem
functioning and species composition in many areas of the
world (Bond and others 2005; Blondel and others 2010).
As a result, the response to fire has been examined in many
taxonomic groups as a means of quantifying post-fire
species losses and gains (e.g., Moretti and others 2004) and
changes in dominant species such as adaptation to shifts in
environmental conditions (e.g., from woodlands to open
areas; Herrando and others 2003; Brotons and others 2005;
Apigian and others 2006; Santos and others 2009). How-
ever, a more recent approach has proposed analyzing the
response of organisms to disturbances such as fire by
assessing changes in the functional trait composition of
biotic communities (Moretti and others 2009). Analyzing
the variation in functional and taxonomic composition in
tandem has proven to be an excellent approach to under-
standing the mechanisms of community responses to
environmental changes (Moretti and others 2009).
E. Mateos (&)X. Santos J. Pujade-Villar
Departament de Biologia Animal, Universitat de Barcelona,
Avinguda Diagonal 645, Barcelona E-08028, Spain
e-mail: emateos@ub.edu
123
Environmental Management (2011) 48:1000–1012
DOI 10.1007/s00267-011-9750-0
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Arthropods make up the largest proportion of species
richness at any spatial scale (Hammond 1992), play a
major role in ecosystem services and are potentially an
excellent candidate group for assessing the response of
organisms to disturbances (Losey and Vaughan 2006).
Unfortunately, arthropods have tended to be underused in
large monitoring projects as specialists with experience in
the identification of many taxa are scarce or nonexistent
(Noss 1996, Whitehead 1990). However, the functional
approach to assessing the response of organisms to envi-
ronmental changes allows the use of some arthropods
groups for which taxonomic classification at a species level
is not possible but functional classification is (Petchey and
Gaston 2002,2006). Indeed, some authors have suggested
that in order to understand the relationships between eco-
system characteristics and arthropods, it is more consistent
to work with functional groups than with taxonomic groups
(Perner and others 2003; Voigt and others 2007).
Hymenoptera has been described as a hyperdiverse taxon
with approximately 145,000 described species (Huber
2009). Indeed, this order is represented in almost all the
planet’s ecosystems, including aquatic and cave environ-
ments. Hymenoptera as a group have profound and often
highly specialized interactions with other animals and
plants; for this reason they are recognized as playing a major
role in maintaining global diversity (LaSalle and Gauld
1993a). The importance of Hymenoptera in the ecosystem is
crucial as they control other arthropod populations by
predation and parasitism, and are actively involved in the
process of pollination (Gauld and others 1990; Day 1991;
LaSalle and Gauld 1993b). Parasitoid Hymenoptera tend
to be involved in extremely complex interactions at a
community level (see Shaw and Hochberg 2001 and
references therein), and can be promoters of diversity and
stability within insect communities at a second trophic level
(Freeland and Boulton 1992; LaSalle and Gauld 1992,
1993b). For this reason, Hymenoptera have been used to
monitor the effects of fire (Lockwood and others 1996) and
several silvicultural practices (Lewis and Whitfield 1999).
Hymenoptera are very sensitive to habitat transformations
(Hughes and others 2000). The taxonomic response to fire
was not matched by functional replacement in the Mediter-
ranean bee community. In light of this study, we predicted a
strong taxonomic response, and a functional replacement, of
Hymenoptera to fire in the Mediterranean region.
Materials and Methods
Study Area and Fire History
The field work was conducted in the Sant Llorenc¸ del Munt
i l’Obac Natural Park (Barcelona province, NE Spain)
(Fig. 1). This reserve is located in the Catalan Pre-coastal
Mountain Range. The landscape of the park is rugged, with
craggy outcrops, and the climate is sub-humid Mediterra-
nean with an annual rainfall of around 600 mm. The park’s
typical forest tree is Holm oak (Quercus ilex). In peripheral
lowland areas of the park, however, Holm oak was partially
replaced by vineyards (Vitis vinifera) around the beginning
of the 20th century, although the fields were abandoned
after the devastating Phylloxera plague and naturally
replaced by Pinus halepensis and Pinus nigra plantations.
The pine forests have Holm oak underbrush.
Rainfall is higher in spring and autumn than in summer,
thus meaning that the area is prone to fast-spreading fires
during hot, dry summers. The eastern border of the park
burnt on 10th August, 2003, during a summer fire that
affected 4,443 ha, with 1,778 ha of this lying inside the
park. The weather conditions at the starting time of the fire
(16.00 PM) were 34.8°C, 20% humidity and 37 km / hour
wind speed. Driven by the wind, the fire advanced rapidly
and all the area burnt in just one day (estimated speed of
the fire front was 20–25 m/min). The rest of the area had
been unburnt since the pine regeneration during the mid-
20th century.
Post-Fire Management and Site Selection
Timber extraction began soon after the fire in August 2003
and two years later most of the area had been completely
logged, with no or very few standing snags remaining.
Logging in the study area did not include elimination of
branches, and woody debris remained in the ground. After
logging, a sub-area was also subsoiled to plant mainly
coniferous stands. Subsoiling was done at a soil depth of
60 cm. Subsoils were done both on the side of the slope
and also perpendicular to the slope.The area previously
burnt in 1970 was also logged after the old fire and later
grazed by herds of goats and sheep. Grazing after the 1970
fire presumably precluded pine regeneration to the pre-fire
forest and, 33 years later, prior to the fire in August 2003,
the area was dominated by a scrubland landscape, which is
why this area was not logged after the 2003 fire. In sum-
mary, the study area was a heterogeneous landscape mosaic
both in terms of pre-fire landscape structure (grazing after
fire in 1970) and post-fire management, which included
logging combined with subsoiling in some areas.
We defined three different areas on the basis of the post-
fire management, and selected five replicate sites per area
(Figs. 1,2). Thus, ‘‘LOGGING’’ was the area burnt only in
2003 with subsequent logging (with partial elimination of
branches and snags), ‘‘SUBSOILING’’ the area burnt only
in 2003 with subsequent logging and subsoiling, and
‘‘RE-BURNT’’ was the area burnt in 1970, then logged and
grazed, and burnt again in 2003. Additionally, we establ ished
Environmental Management (2011) 48:1000–1012 1001
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one reference area containing five unburnt control repli-
cates (‘‘UN-BURNT’’) in a pine forest near the fire edge
with the same dominant tree species as the area burnt
before the fire. Thus, the entire study was comparing the
Hymenoptera assemblages among various habitats affec-
ted by a single fire in 2003 and later submitted to dif-
ferent post-fire activities, and then comparing these to an
unburnt area.
All sites were located over conglomerate lithological
substrate mainly composed of clays and sandstone, with a
similar orientation (all sites were oriented between south
and east) and slope (Kruskall–Wallis test H=5.57,
p=0.13). The soil properties of the sites did not show
significant differences in terms of pH (H=2.29, p=
0.51), electrical conductivity (dS m
-1
)(H=3.86,
p=0.28), %C (H=4.49, p=0.21) and %N (H=0.98,
p=0.81). The sites were located between 491 and 699 m
a.s.l., with significant altitudinal differences (H=14.90,
p=0.002) as the control sites were located an average
109 m below the burnt area. Despite altitudinal differences,
the other variables tested and the habitat structure did not
show differences between the areas.
The unburnt control sites had similar vegetation to that
at the burnt sites prior to the fire, with dominance of pines
and Holm oak underbrush, thus making the unburnt refer-
ence sites reliable. This conclusion has been supported by a
recent study comparing gastropod composition by shells
from dead specimens at the burnt sites and living species in
the unburnt area (Santos and others 2009).
The spatial autocorrelation was checked by performing a
Mantel test with 999 permutations by comparing the dis-
tance matrix between pairs of sites and the hymenoptera-
composition similarity matrix calculated by means of
Euclidean distances (Fortin and Gurevitch 2001). The
distance and similarity matrices, as well as the Mantel test,
were performed with the software Passage 1.1 (Rosenberg
2004).
Site Characteristics
We characterized the habitat structure of the sampling sites
by recording six vegetation and ground-cover variables
along a 50-m transect placed in the center of the site. The
extent of three vegetation types (trees, shrub and grass) and
Fig. 1 Location of the study
area in the western
Mediterranean (a) and exact
position of the 20 sampling sites
(b). The solid line indicates the
edge of the fire and dotted line
the limit of the Sant Llorenc¸ del
Munt Natural Park. Acronyms
of the four areas are UN-
BURNT (U), LOGGING (L),
SUBSOILING (S) and RE-
BURNT (R). The squares were
191 km. The black rectangle
indicates the location of the
nearest village Sant Llorenc¸
Savall (SLS) to the study area
(Lat–Long 41°40047.4200N,
2°03033.4300E, datum WGS84)
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three groundcover variables (litter, bare ground and wood
debris) were recorded at points 0.5 m apart along that
transect. Thus, we recorded 100 points that estimated the
cover percentage of the main vegetation and ground-cover
types at each site.
Sampling Methods
In Mediterranean environments, there is a strong seasonal
pattern in faunal activity, with maximums in spring for epi-
geic and aerial fauna. In the present paper we were interested
in spatial differences between Hymenoptera communities
and not in temporal differences, and consequently, we con-
centrated the sampling effort in late spring. Samples were
undertaken during June and July 2007 using two comple-
mentary methods, namely pitfall traps and sweep netting
(Drake and others 2007), in order to collect both soil and
vegetation Hymenoptera. Pitfall trap sampling is a standard
and efficient method for collecting ground-dwelling arthro-
pods (Dent and Walton 1997, Duelli and others 1999). Five
traps were installed at each sampling point, placed at 10-m
intervals in a straight line. After 15 days, the traps were
removed and samples were preserved in 708alcohol. The
traps consisted of a plastic collector 7.5 cm in diameter and
10 cm deep, placed within a plastic container 10 cm in
diameter and 15 cm deep. A plastic funnel 8 cm in diameter
was inserted over the collector pot. A supersaturated aqueous
salt solution was used as preservative.
Vegetation Hymenoptera were collected by sweeping
five random samples from each sampling point. Each
sample consisted of sweeping (20 sweeps) while walking at
a constant speed along a straight path. The net was
mounted on a pole 1 m long, with a light frame 25 cm in
diameter and 50 cm deep. The five sweeping samples were
carried out close to the five pitfalls on each site (in the
same 15 days period and with fine weather conditions),
therefore data from soil and vegetation sampling (pitfall
and sweep-netting respectively) were pooled.
Hymenoptera Groups
Hymenoptera specimens were classified by taxonomic
category of family according to Gauld and Bolton (1988),
Goulet and Huber (1993), and Pujade-Villar and Ferna
´ndez-
Gayubo (2004). The Hymenoptera families were classified
into several functional dietary traits according to Goulet
and Huber (1993) and Hanson and Gauld (2006), and with
respect to the following criteria: (1) Formicidae were
identified to species and then separated according to
feeding strategies (Bernard 1968); (2) Hymenoptera have a
life cycle that includes larvae and adults; in general, only
one or the other have a relevant dietary trait (e.g. if larvae
are parasitic, adults do not have a functional role), and only
several families have larvae and adults with relevant tro-
phic importance (see Table 1). For this reason we noted
the dietary traits of larvae and adult forms separately.
Fig. 2 Pictures of the four study areas
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Table 1 Total abundance (no
of individuals) of Hymenoptera
families and feeding groups at
each site
RRE-BURNT area,
LLOGGING area,
SSUBSOILING area,
UUN-BURNT area. Feeding
groups of larvae and adults:
CH chewing herbivores,
FC flower consumer,
Gr granivorous, Om
omnivorous, Pa parasitoid,
Pr predator, wti without trophic
importance (see text for more
details)
a
Apoidea other than Apidae
b
Gauthier and others (2000)
include Elasmidae as a tribe
within the Eulophidae, but due
to their special morphology and
host insect groups, we have
considered Elasmidae as a
separate group in this study
Code Family R L S U Adult Larvae
Aphe Aphelinidae 6 9 4 1 wti Pa
Apid Apidae 1 2 9 0 FC Wti
Apoi Apoidea
a
1201FCWti
Beth Bethylidae 8 3 3 0 wti Pa
Brac Braconidae 25 38 40 12 wti Pa
Cera Ceraphronidae 4 2 5 2 wti Pa
Chal Chalcididae 3 2 3 0 wti Pa
Chry Chrysididae 1 0 0 0 FC Pa
Diap Diapriidae 1 3 12 1 wti Pa
Elas Elasmidae
b
3 1 0 0 wti Pa
Ency Encyrtidae 8 35 5 9 wti Pa
Eulo Eulophidae 76 129 55 23 wti Pa
Eupe Eupelmidae 2 6 1 0 wti Pa
Eury Eurytomidae 6 8 3 0 wti CH/Pa
Evan Evaniidae 2 4 1 6 FC Pr
Figi Figitidae 6 12 3 0 wti Pa
For Formicidae 310 379 464 271 FC wti
For Formicidae 17 0 0 0 Gr wti
For Formicidae 341 848 529 394 Om wti
For Formicidae 5 5 2 13 Pr wti
Ichn Ichneumonidae 2 1 3 1 wti Pa
Mega Megaspilidae 14 6 4 3 wti Pa
Muti Mutillidae 3 2 18 0 FC Pa
Myma Mymaridae 2 32 6 17 wti Pa
Ormy Ormyridae 0 1 0 0 wti Pa
Plat Platygastridae 14 18 16 2 wti Pa
Pomp Pompilidae 0 0 1 0 Pr/wti Pa
Proc Proctotrupidae 0 0 3 0 wti Pa
Pter Pteromalidae 21 30 20 2 wti Pa
Scel Scelionidae 70 99 198 32 wti Pa
Sign Signophoridae 1 11 0 2 wti Pa
Sphe Sphecidae 2 1 0 0 Pr/FC Pa
Tent Tenthredinidae 1 0 1 0 wti CH
Tory Torymidae 15 4 6 0 wti Pa
Tric Trichogrammatidae 2 8 0 0 wti Pa
Vesp Vespidae 0 0 1 0 FC Wti
Total abundance 973 1701 1416 792
Total famililes 29 28 26 16
Adults FC 320 386 492 280
Adults Gr 17 0 0 0
Adults Om 340 851 529 392
Adults Pr 6 6 3 13
Adults wti 290 458 392 107
Larvae CH 4 4 3 0
Larvae Pa 292 457 407 107
Larvae Pr 2 4 1 6
Larvae wti 675 1236 1005 679
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The potential hosts for parasitoids Hymenoptera families
were determined following Hanson and Gauld (2006).
According to these criteria, we grouped Hymenoptera
families into the following feeding groups (see Table 1):
parasitoids (Pa), predators (Pr), chewing herbivores (CH),
flower consumers (FC, including nectarivorous and polle-
nophagous), granivorous (Gr), omnivorous (Om) and those
without trophic importance (wti).
The remaining arthropods collected, apart from Hymenop-
tera, were separated and identified to taxonomic Order level.
Arthropods that were potential hosts of parasitoid Hymenop-
tera were counted and scored from each site (Table 3).
Statistical Procedures
We recorded the number of Hymenoptera families, total
number of specimens, number of families of each feeding
group and abundance of each feeding group for each site.
This data were then compared for the four areas by ANOVA
(with Student–Newman–Keuls post-hoc tests) or Kruskall–
Wallis (with Dunn post-hoc test) tests, after checking the
homogeneity of variances using the Levene test.
Multivariate analyses were used to examine the similarity
of Hymenoptera families and feeding group composition
(response variables) between the four areas, using dummy
variables as explanatory variables. We tested the linear or
unimodal distribution of family and trait abundance using a
Detrended Correspondence Analysis (DCA) beforehand.
The largest gradients obtained in DCA were 1.198 for family
abundance and 0.836 for trait abundance, thus suggesting
linear distribution for both variables (Leps
ˇand S
ˇmilauer
2003). In light of this, we analyzed the taxonomic and
functional response of Hymenoptera to fire and post-fire
management using a Redundancy Analysis (RDA), statisti-
cally testing the significance of the axes using a permutation
Monte Carlo test with 999 permutations (ter Braak and
Smilauer 2002). The observed number of Hymenoptera
families and feeding groups were log-transformed (log
x?1) prior to the DCA and RDA analyses to avoid biases
due to the existence of aggregate families with high sample
sizes at a single sampling point (as is the case of Formicidae).
Hymenoptera families with very low occurrence (less than
two records) were removed from the abundance data matri-
ces to avoid biases due to the presence of very uncommon
families. The multivariate analyses (DCA and RDA) were
performed using the CANOCO software program (ter Braak
and Smilauer 1997–2002).
The relationship between the number of parasitoids and
their potential hosts was assessed using a Spearman Rank
Order Correlation analyses (by means of Sigma Plot v.11
software). Given the association of parasitoid families with
their hosts (see Gauld and Bolton 1988; Quicke 1997), we
correlated the number of individuals of each parasitoid
hymenoptera family and the number of individuals of their
potential host arthropods.
Results
Habitat Variables
Several vegetation and habitat variables differed between
burnt and unburnt sites; for example, the extent of trees and
litter deposited in the soil characterizes the control area,
whereas bare soil characterizes the burnt areas (Fig. 3). In
contrast, shrub and grass cover were similar in all areas.
Amongst the burnt managed areas, the extent of wood debris
on the ground (branches and trunks) was significantly higher
in area LOGGING (Fig. 3). Thus, the combination of
unburnt and burnt managed areas created a mosaic that
produced some level of habitat heterogeneity (see Fig. 2).
Hymenoptera Abundance Data
A total of 4,882 specimens of Hymenoptera belonging to
33 families were obtained (Table 1). Furthermore, there
was no spatial autocorrelation in our Mantel test site design
(Z=100513806, P=0.55), in other words nearby sites
did not have more similar Hymenoptera communities than
distant ones. Formicidae were the most abundant family
accounting for 69% of specimens in area RE-BURNT, 72%
in area LOGGING, 70% in area SUBSOILING and 86% in
area UN-BURNT. More Hymenoptera families were found
in burnt than in unburnt sites, although there were no sig-
nificant differences in the number of individuals. There
were no differences in the number of Hymenoptera fami-
lies between the three burnt areas (Table 2).
Formicidae was also the family with the highest diver-
sification of feeding groups (Table 1). Parasitoids, flower
consumers and omnivores were present in all areas and
represented the majority groups (Table 1). The majority of
families (27) have a parasitoid strategy and, taken together,
show a wide spectrum of potential hosts amongst various
groups of insects, spiders and pseudoscorpions (Tables 1
and 4). Flower consumers were represented by eight fam-
ilies and omnivores were only represented by several
Formicidae species (Table 1). Predators (4 families) were
also present in all areas, although in low abundance
(Table 1). Chewing herbivores (2 families) were absent
from UN-BURNT sites and granivores (1 family) were
only present in RE-BURNT sites (Table 1).
Taxonomic and Functional Differences Between Areas
A higher number of parasitoid families were found in the
three burnt areas compared to the UN-BURNT area. The
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LOGGING area had a higher abundance of parasitoids than
the UN-BURNT area (Table 2). The abundance of omni-
vores showed a marginal significance in the ANOVA test
(p=0.072), with a higher value in area LOGGING
(Table 2).
In the gradient analyses, the four dummy variables
generated three canonical axes. DCA analyses showed that
the Hymenoptera family composition data set (with DCA
total inertia =0.701) had greater variability than the
Hymenoptera traits data set (with DCA total iner-
tia =0.283). The first axis in the two RDA analyses
(Fig. 4) separated unburnt sites in positive values from
sites of the three burnt areas in negative values. This first
axis can therefore be interpreted as a burn/unburn gradient,
and was significant in the two RDAs (see Fig. 4a and b).
The second axis discriminated between burned areas, and
this separation was significant in the Family composition
RDA (see Fig. 4a) but not the Traits composition RDA (see
Fig. 4b). The third axis was not significant in either of the
two RDA analyses.
All Hymenoptera families in the family composi-
tion RDA analysis showed a greater association with
burnt areas (negative values of axis 1), except Evaniidae,
which was associated with unburned areas (positive
values of axis; Fig. 4a). The second axis separates
SUBSOILING (positive values) from LOGGING (nega-
tive values), thus indicating that these two post-fire
Fig. 3 Cover percentage of the six vegetation and ground-cover
variables (mean per site ±SE) as regards unburnt and post-fire
managed burnt areas (UUN-BURNT, LLOGGING, SSUBSOILING,
RRE-BURNT). Each figure includes the ANOVA or Kruskall–Wallis
analysis and letters (a, b) refer to post hoc comparisons between areas
Table 2 Mean hymenoptera abundance and number of families in each area
RE-BURNT LOGGING SUBSOILING UN-BURNT Test p
Mean se Mean se Mean se Mean se
Abundance
Total hym 194.6 30.67 340.2 75.14 283.2 74.55 158.4 28.43 F =2.115 0.138
A_FC 63.9 6.61 77.9 39.63 98.5 32.55 55.6 12.09 H =2.733 0.435
A_Gr 3.4 3.16 0.0 0.00 0.0 0.00 0.0 0.00 H =6.316 0.097
A_Om 68.1 15.66 169.6 36.08 105.9 33.69 78.8 16.05 F =2.821 0.072
A_Pr 1.2 0.56 1.1 0.71 0.5 0.22 2.6 1.47 H =1.345 0.718
L_CH 0.8 0.56 0.8 0.37 0.5 0.32 0.0 0.00 H =4.312 0.230
L_Pa 58.4
ab
11.54 91.4
a
22.12 81.5
ab
22.83 21.4
b
5.53 F =3.294 0.048
L_Pr 0.4 0.40 0.8 0.80 0.2 0.20 1.2 0.49 H =4.321 0.229
Number of families
Total hym 16.2
a
1.02 16.2
a
1.24 14.8
a
2.01 8.6
b
1.03 F =6.852 0.004
A_FC 2.6 0.51 2.4 0.40 2.6 0.40 2.0 0.32 F =0.471 0.707
A_Gr 0.4 0.24 0.0 0.00 0.0 0.00 0.0 0.00 H =6.333 0.096
A_Pr 1.0 0.45 0.6 0.40 0.6 0.24 0.6 0.24 H =0.772 0.856
L_CH 0.8 0.37 0.6 0.24 0.6 0.40 0.0 0.00 F =1.333 0.299
L_Pa 14.4
a
0.68 14.2
a
1.11 12.8
a
1.77 6.6
b
0.93 F =9.450 \0.001
L_Pr 0.20 0.20 0.20 0.20 0.20 0.20 0.80 0.20 H =5.637 0.131
For all means and tests n=5. Columns:Mean arithmetic mean, se standard error of the mean, Test ANOVA (F) or Kruskall–Wallis (H) statistic, Ptest
probability level. Rows:Total hym total hymenoptera, Aadults, Llarvae, CH chewing herbivores, FC flower consumer, Gr granivorous, Om omnivorous,
Pa parasitoid, Pr predator. Letters (a, b) refer to post hoc comparisons between areas. Adults and larvae without trophic importance (wti) not analysed.
Number of families of adult Omnivorous (A_Om) feeding group not analysed because only one family (Formicidae) had this trait
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treatments generate significant differences in Hymenop-
tera family composition.
Predators (adults and larvae) were arranged in positive
values of axis 1, which is associated with unburnt sites, in
the traits composition RDA analysis, whereas the rest of
the feeding groups were associated with burnt sites (neg-
ative values of the axis; Fig. 4b). No differences were
observed in traits composition between post-fire treat-
ments, as neither the second nor the third RDA axes were
significant.
With the exception of Diptera, the potential hosts of
parasitoids showing significant differences between sites
were more abundant in the burnt areas (Table 3). We found
a significant positive correlation between the number of
parasitoids and potential hosts in 12 out of 27 Hymenoptera
parasitoid families (Table 4). These 12 families accounted
for 85% (1,073 individuals) of the total parasitoid indi-
viduals collected.
Discussion
Taxonomic Response to Fire
Unburnt sites are characterized by a large extension of pine
trees and a layer of humus and dead leaves on the ground,
whereas burnt areas have a simpler vegetation structure
with no tree cover and a large extension of bare ground.
The taxonomic response of Hymenoptera to this habitat
shift has resulted in an increased number of Hymenoptera
families at all burnt sites. The 33 families found, except
Fig. 4 Redundancy-analysis
biplots of changes in taxonomic
(a) and functional
(b) Hymenoptera composition
in response to fire and post-fire
management. The first two
canonical axes show variance
explained and pvalues from
Monte Carlo permutation test of
significance (9999 iterations).
Families and traits codes can be
found in Table 1
Table 3 Total abundance (no of individuals) of potential host Arthropods for Hymenoptera parasitoids
R L S U Test P
Blattodea 3 7 3 0 F =0.835 0.494
Coleoptera 153
ab
372
ab
387
a
107
b
F=3.891 0.029
Diptera 40
b
74
b
67
b
147
a
F=4.905 0.013
Homoptera 1110
ab
2812
a
1051
ab
494
b
F=3.228 0.050
Insecta holometabolous larvae 73
ab
136
a
112
ab
45
b
F=3.382 0.044
Lepidoptera 18 38 30 16 F =0.630 0.606
Mantodea 4 5 3 0 F =1.244 0.327
Neuroptera 1 2 4 1 F =1.143 0.362
Orthoptera 192
a
112
bc
146
ab
77
c
F=6.974 0.003
Thysanoptera 164 541 359 41 F =1.548 0.241
Pseudoescorpionida 0 3 2 4 F =1.296 0.310
Araneida 374 370 348 272 F =0.403 0.753
Total potential host Arthropods 2132
b
4472
a
2512
b
1204
b
H=8.874 0.031
RRE-BURNT area, LLOGGING area, SSUBSOILING area, UUN-BURNT area. Test =ANOVA (F) or Kruskall–Wallis (H) statistic, Ptest
probability level. Letters (a, b, c) refer to post hoc comparisons between areas
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Evaniidae (whose larvae forage on cockroach eggs),
showed higher abundances in burnt sites than in unburnt
sites.
Formicidae was the most abundant family in all areas,
with a clear tendency to show higher abundances in burnt
sites. This result agrees with previous studies, which
reported that ants respond positively to fire because of the
increase in resource availability and the reduction of
obstacles to locomotion (Andersen 1988; Neumann 1991,
1992; Jackson and Fox 1996). An increase of ant abun-
dance in burnt Mediterranean habitats has also been noted
by Arnan and others (2006). In contrast, Moretti and others
(2004) found a reduction of ant abundance in burnt Cas-
tanea sativa forests from the southern Swiss Alps. This
contrasting result could relate to differences in climate, as
has been found in other Hymenoptera groups (i.e., bees,
Moretti and others 2009).
Functional Response to Fire
The most remarkable functional response to fire was the
increased number of parasitoid families at burnt sites (27
out of 33 Hymenoptera families were primary parasitoids
with a large diversity of hosts). Hymenoptera parasitoids
have been recognized as being more sensitive to habitat
changes than other insect taxa, including their hosts
(Jonsell and others 1999; Kruess and Tscharntke 1999;
Weslien and Schroeder 1999; Komonen and others 2000;
Hilszczajski and others 2005). Hymenoptera parasitoids are
known to have a high discriminatory power for the detec-
tion of habitat disturbance and to be useful for biological
monitoring (Basset and others 2004), and our findings
highlight the value of Hymenoptera for monitoring the
functional responses of organisms to habitat disturbance
and landscape heterogeneity.
Table 4 Spearman Rank Order Correlation (r) between abundances of parasitoid Hymenoptera families and their potential host arthropods
Hymenoptera family r p Potential host
Aphelinidae 0.630 0.002* Hom
Bethylidae 0.401 0.077
?
Col, Lep
Braconidae 0.734 0.000* Ins
Ceraphronidae -0.118 0.617 Col, Hom, Hym, Dip, Thy, Neu,
Chalcididae 0.118 0.617 Lep, Dip, Hym, Col
Chrysididae 0.179 0.444 Hym
Diapriidae 0.328 0.155 Dip, Hym
Elasmidae 0.108 0.644 Hym, Lep
Encyrtidae 0.510 0.021* Ins
Eulophidae 0.659 0.001* Ins
Eupelmidae 0.270 0.246 Ins, Spi
Eurytomidae 0.483 0.030* Ins
Figitidae 0.585 0.006* Dip, Hym, Neu
Ichneumonidae -0.099 0.672 Ins
Megaspilidae 0.132 0.572 Col, Hym, Neu, Dip
Mutillidae 0.201 0.388 Hym, Dip, Lep, Col, Bla
Mymaridae 0.243 0.295 Col, Hom
Ormyridae 0.099 0.672 Hym, Dip
Platygastridae 0.532 0.015* Dip, Col, Hom
Pompilidae 0.380 0.097 Spi
Proctotrupidae -0.252 0.280 Col, Dip
Pteromalidae 0.660 0.001* Ins
Scelionidae 0.591 0.006* Ins, Spi
Signophoridae 0.414 0.068
?
Hom
Sphecidae 0.109 0.639 Bla, Hym Lep, Man, Ort, Spi
Torymidae 0.140 0.551 Dip, Hym, Lep, Man
Trichogrammatidae 0.533 0.015* Ins
n=20 for all analyses: Bla Blattodea, Col Coleoptera, Dip Diptera, Hom Homoptera, Hym Hymenoptera, Ins Insecta (= Bla ?Col ?
Dip ?Hom ?Hym ?Lep ?Man ?Neu ?Ort ?Thy ?holometabous larvae), Lep Lepidoptera, Man Mantodea, Neu Neuroptera, Ort
Orthoptera, Pse Pseudoescorpionida, Spi Araneida, Thy Thysanopterap. probability. * P\0.05,
?
Residual probability
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The question now remains as to what causes the positive
response of parasitoid species to fire. According to
Eggleton and Gaston (1990), parasitoids are species that
develop on/in another single organism (host), feed on/from
it and kill it as a direct or indirect result of such develop-
ment. For this reason, the abundance and diversity of
parasitoids are mainly conditioned by the abundance and
diversity of their potential prey (Caballero-Lo
´pez and
others 2010; Haddad and others 2001; Knops and others
1999; Koricheva and others 2000). In an agricultural
grassland environment, Anderson and others (2011) poin-
ted out that both the abundance and taxon-richness of
parasitoid Hymenoptera were more closely related with
overall arthropod diversity than any other arthropod group
they investigated. Our correlation between the majority of
parasitoids and their potential hosts suggests that the gen-
eral increase of arthropod abundance in burnt areas favors
the increase of parasitoids. It is well known that parasitoids
are more diverse in ecologically complex systems than in
simple landscapes (Heraty 2009) since their life-cycle
strategies have evolved in a highly diverse community,
thus meaning that they attack virtually every possible host
niche available (Hawkins and others 1992; Hawkins 1994).
Parasitoid abundance and diversity would therefore appear
to be a good surrogate for arthropod diversity (Shaw and
Hochberg 2001; Anderson and others 2010).
The low number of parasitoids from the unburnt pine
forest, together with the correlated low number of arthro-
pods, suggests that pine forest may be a low-quality habitat
for arthropod communities in our study area. In the same
way, several studies based on other arthropod groups have
shown lower abundance and richness in coniferous forests
when compared to open areas and broadleaf forests (Fahy
and Gormally 1998 for Carabidae, Mullen and others 2003
for Hemiptera, Vance and others 2007 for Hymenoptera).
In fact, our study area was completely afforested and
covered by vineyards during the early 20th century (see
Supplementary Materials of Santos and Poquet 2010 for a
picture of the study area from that period), and later
replaced by pines after the Phylloxera plague in the mid
20th century. This land-use history, with severe shifts in
vegetation structure and landscape simplification, may
explain the poor taxonomic and functional composition of
Hymenoptera communities in unburnt areas and agrees
with the general landscape changes in many areas of the
Mediterranean basin, whereby forest cover in the past was
not as uniform as today, and many landscapes were origi-
nally heterogeneous with a more intricate mixture of oaks,
pines, junipers and deciduous trees (Blondel and others
2010). Pines recover better and spread faster than other tree
species, which is why pines are more frequently planted
than other kinds of Mediterranean tree (Blondel and others
2010).
Response to Post-Fire Management
The three post-fire managed areas showed a significant
taxonomic, although not functional, response of Hyme-
noptera, in agreement with the conclusions reported by
Moretti and others (2009) for bee species. In other words,
managed areas differed in taxonomic composition although
not in the dietary trait. This diet redundancy, at least
between post-fire managed areas, could be related to the
adaptation of Hymenoptera communities to high landscape
heterogeneity, as occurs in the Mediterranean region
(Blondel and others 2010). The environmental differences
between burnt areas were small, although the logged area
(LOGGING) had more branches and dead trunks on the
ground than other burnt areas. These branches and trunks
appear to have created favorable microenvironments that
attract large numbers of arthropod species and several
Hymenoptera families, essentially those with parasitoid
and omnivorous strategies. Due to the profound, and often
highly specialised, interactions between Hymenoptera and
other organisms, Hymenoptera as a group has a dispro-
portionately large role in maintaining the diversity of other
animals and plants (LaSalle and Gauld 1993a), and also
there are indications that parasitoids promote diversity and
stability within insect communities at the second trophic
level (Freeland and Boulton 1992; LaSalle and Gauld 1992,
1993b). Therefore, post-fire management that promotes an
increased number of Hymenoptera parasitoids may also
lead to high levels of biodiversity for other taxonomic
groups. Indeed, the response of Hymenoptera to post-fire
management in the logged area is mirrored by the positive
response observed for terrestrial snails (Bros and others
2011). In contrast, this management is unfavorable to other
species, such as rabbits, since wood debris may hinder their
movements (Rollan and Real 2010). Wood debris on the
ground is also beneficial in facilitating post-fire tree-seed-
ling establishment (Castro and others 2010). Thus, post-fire
management practices are either favorable or unfavorable
for species or groups depending on their habitat require-
ments. This conclusion suggests that heterogeneous land-
scapes may be the most desirable scenario for sustaining
high gamma-diversity scores on a landscape scale (Blondel
and others 2010).
Conclusions
We have found a strong functional and taxonomic response
of Hymenoptera to fire and a lesser response to post-fire
management. The most evident differences between burnt
and unburnt sites relate to the habitat’s transformation from
woodland to open area. This result agrees with previous
studies that reported Hymenoptera, Diptera and other flying
Environmental Management (2011) 48:1000–1012 1009
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arthropods to be habitat-type dependent (i.e., forest vs.
meadow) (Hughes and others 2000). Thus, post-fire shifts
in vegetation structure (i.e., from forest to open areas) are
relevant factors affecting the community composition of
arthropod groups, as occurs with other animal assemblages
(Herrando and others 2003; Brotons and others 2005;
Apigian and others 2006; Santos and others 2009; Santos
and Poquet 2010).
As reported previously in other scenarios of habitat
disturbance, a functional response to fire based on dietary
preferences is a sensitive indicator of changes in environ-
mental conditions (Perner and others 2003; Voigt and
others 2007). Indicators that make use of functional traits
therefore complement the taxonomic indices usually used
in biodiversity monitoring (Vandewalle and others 2010),
and both types of data are essential for evaluating conser-
vation management practices. An understanding of the
taxonomic and functional animal and plant composition of
disturbed habitats is relevant to understanding the ecolog-
ical mechanisms of communities in order to respond to
environmental changes and to apply corrective measures
through management policy.
Acknowledgments We thank the staff of the Sant Llorenc¸ del Munt
i l’Obac Natural Park for their logistic support. This study was par-
tially funded by the Diputacio
´de Barcelona and La Caixa. XS was
supported by a Beatriu de Pino
´s postdoctoral grant from the Gov-
ernment of Catalonia (BP-B1 10211). Xavier Espadaler and Joan A.
Herraiz identified Formicidae to species level. Robert R. Parmenter
and two anonymous reviewers provided helpful comments that
improved the manuscript.
References
Andersen AN (1988) Immediate and longer-term effects of fire on
seed predation by ants in sclerophyllous vegetation of south-
eastern Australia. Australian Journal of Ecology 13:285–293
Anderson A, McCormack S, Helden A, Sheridan H, Kinsella A,
Purvis G (2011) The potential of parasitoid Hymenoptera as
bioindicators of arthropod diversity in agricultural grasslands.
Journal of Applied Ecology 48:382–390
Apigian KO, Dahlsten DL, Stephens SL (2006) Fire and fire surrogate
treatment effects on leaf litter arthropods in a western Sierra
Nevada mixed-conifer forest. Forest Ecology and Management
221:110–122
Arnan X, Rodrigo A, Retana J (2006) Post-fire recovery of
Mediterranean ground ant communities follows vegetation and
dryness gradients. Journal of Biogeography 33:1246–1258
Basset Y, Mavoungou JF, Mikissa JB, Missa O, Miller SE, Kitching
RL, Alonso A (2004) Discriminatory power of different
arthropod data sets for the biological monitoring of anthropo-
genic disturbance in tropical forests. Biodiversity and Conser-
vation 13:709–732
Bengtsson J, Nilsson G, Franc A, Menozzi P (2000) Biodiversity,
disturbance, ecosystem function and management of European
forests. Forerst Ecology and Management 132:39–50
Bernard F (1968) Les fourmis (Hymenoptera Formicidae) d’Europe
occidentale et septentrionale. Masson, Paris, p 411
Blondel J, Aronson J, Bodiou J-Y, Bœuf W (2010) The Mediterranean
Region. Biological Biodiversity in Space and Time. Oxford
University Press, Oxford
Bond WJ, Woodward FI, Midgley GF (2005) The global distribution
of ecosystems in a world without fire. New Physiologist 165:
525–538
Bros V, Moreno-Rueda G, Santos X (2011) Does postfire manage-
ment affect the recovery of Mediterranean communities?
The case study of terrestrial gastropods. Forest Ecology and
Management 261:611–619
Brotons L, Pons P, Herrando S (2005) Colonization of dynamic
Mediterranean landscapes: where do birds come from after fire?
Biogeography 32:789–798
Caballero-Lo
´pez B, Blanco-Moreno JM, Pe
´rez N, Pujade-Villar J,
Ventura D, Oliva F, Sans FX (2010) A functional approach to
assessing plant–arthropod interaction in winter wheat. Agricul-
ture, Ecosystems and Environment 137:288–293
Castro J, Moreno-Rueda G, Ho
´dar JA (2010) Experimental test of
postfire management in pine forests: impact of salvage logging
versus partial cutting and nonintervention on bird-species
assemblages. Conservation Biology 24(3):810–819
Day MC (1991) Towards the conservation of Aculeate Hymenoptera
in Europe. Nature and Environment series 51. Council of Europe
Press, Strasbourg
Dent DR, Walton MP (1997) Methods in ecological and agricultural
entomology. CAB International, Wallingford
Drake CM, Lott DA, Alexander KNA, Webb J (2007) Surveying
terrestrial and freshwater invertebrates for conservation evalu-
ation. Natural England Research Report NERR005, Natural
England
Duelli P, Obrist MK, Schmatz DR (1999) Biodiversity evaluation in
agricultural landscapes: above-ground insects. Agriculture Eco-
systems and Environment 74:33–64
Eggleton P, Gaston KJ (1990) Parasitoid species and assemblages—
convenient definitions or misleading compromises. Oikos 59:
417–421
Fahy O, Gormally M (1998) A comparison of plant and carabid beetle
communities in an Irish oak woodland with a nearby conifer
plantation and clearfelled site. Forest Ecology and Management
110:263–273
Fortin MJ, Gurevitch J (2001) Mantel tests: spatial structure in field
experiments. In: Scheiner SM, Gurevitch J (eds) Design and
analysis of ecological experiments. Oxford University Press,
New York, pp 308–326
Freeland WJ, Boulton WJ (1992) Coevolution of food webs:
parasites, predators and plant secondary compounds. Biotropica
24:309–327
Gauld I, Bolton B (1988) The Hymenoptera. British Museum (Natural
History), London
Gauld ID, Collins NM, Fitton MG (1990) The biological significance
and conservation of Hymenoptera in Europe. Nature and Envi-
ronment series 44. Council of Europe Press, Strasbourg, pp 1–47
Gauthier N, Lasalle J, Quicke DLJ, Godfray HCJ (2000) Phylogeny of
Eulophidae (Hymenoptera: Chalcidoidea), with a reclassification
of Eulophinae and the recognition that Elasmidae are derived
eulophids. Systematic Entomology 25:521–539
Goulet H, Huber JT (1993) Hymenoptera of the world: an identifi-
cation guide to families. Centre for Land and Biological
Resources Research, Ottawa
Haddad NM, Tilman D, Haarstad J, Richtie M, Knops JMH (2001)
Contrasting effects of plant and decomposition on insects
communities: a field experiment. The American Naturalist 158:
17–35
Hammond PM (1992) Species inventory. In: Groombridge B (ed)
Global biodiversity, status of the Earths living resources.
Chapman and Hall, London, pp 17–39
1010 Environmental Management (2011) 48:1000–1012
123
Author's personal copy
Hanson PE, Gauld ID (eds) (2006) Hymenoptera de la Regio
´n
Neotropical. Memoirs of the American Entomological Institute
77, 997 pp
Hawkins BA (1994) Pattern and process in host-parasitoid interac-
tions. Cambridge University Press, Cambridge
Hawkins BA, Shaw MR, Askew RR (1992) Relations among
assemblage size, host specialization, and climatic variability in
North-American parasitoid communities. American Naturalist
139:58–79
Heraty J (2009) Parasitoid biodiversity and insect pest management.
In: Foottit R, Adler P (eds) Insect biodiversity: science and
society, 1st edn. Blackwell Publishing 632, pp 445–462
Herrando S, Brotons L, Llacuna S (2003) Does fire increase the
spatial heterogeneity of bird communities in Mediterranean
landscapes? Ibis 145:307–317
Hilszczajski J, Gibb H, Hja
¨lte
´n J, Atlegrim O, Johansson T,
Pettersson RB, Ball JP, Danell K (2005) Parasitoids Hymenop-
tera, Ichneumonoidea) of Saproxylic beetles are aVected by
forest successional stage and dead wood characteristics in boreal
spruce forest. Biological Conservation 126:456–464
Huber JT (2009) Biodiversity of Hymenoptera. In: Foottit R, Adler P
(eds) Insect biodiversity: science and society, 1st edn. Blackwell
Publishing 632. pp 303–323
Hughes JB, Daily GC, Ehrlich PR (2000) Conservation of insect
diversity: a habitat approach. Conservation Biology 14(6):
1788–1797
Jackson GP, Fox BJ (1996) Comparison of regeneration following
burning, clearing or mineral sand mining at Tomago, NSW: II.
Succession of ant assemblages in a coastal forest. Australian
Journal of Ecology 21:200–216
Jonsell M, Nordlander G, Jonsson M (1999) Colonization patterns of
insects breeding in wood decaying fungi. Journal of Insects
Conservation 3(2):145–161
Knops JMH, Tilman D, Haddad NM, Naesm S, Mitchell CE, Haarstad
J, Richtie ME, Howe KM, Reic PB, Siemann E, Grtoth J (1999)
Effects of plant species richness on invasion dynamics, disease
outbreaks, insect abundances and diversity. Ecology Letters
2:286–293
Komonen A, Pentila
¨R, Lindgren M, Hanski I (2000) Forest
fragmentation truncates a food chain based on an old-growth
forest bracket fungus. Oikos 90:119–126
Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K (2000)
Numerical responses of different trophic groups of invertebrates
to manipulation of plant diversity in grasslands. Oecologia
125(2):271–282
Kruess A, Tscharntke T (1999) Species richness and parasitism in a
fragmented landscape: experiments and field studies with insects
on Vicia sepium. Oecologia 122:129–137
LaSalle J, Gauld ID (1992) Parasitic Hymenoptera and the biodiver-
sity crisis. Redia 74:315–334
Lasalle J, Gauld ID (1993a) Hymenoptera and biodiversity. CAB
International, Wallingford
LaSalle J, Gauld ID (1993b) Hymenoptera: their diversity and their
impact on the diversity of other organisms. In: LaSalle J, Gauld
ID (eds) Hymenoptera and biodiversity. CAB International,
Wallingford, pp 1–26
Leps
ˇJ, S
ˇmilauer P (2003) Multivariate analysis of ecological data
using CANOCO. Cambridge University Press, Cambridge
Lewis CN, Whitfield JB (1999) Braconid wasp (Hymenoptera:
Braconidae) diversity in forest plots under different silvicultural
methods. Environmental Entomology 28(6):986–997
Lockwood JA, Shaw SR, Struttman JM (1996) Biodiversity of wasp
species (Insecta:Hymenoptera) in burned and unburned habitats
of Yellowstone National Park, Wyoming, USA. Journal of
Hymenoptera Research 5:1–15
Losey JE, Vaughan M (2006) The economic value of ecological
services provided by insects. BioScience 56(4):311–323
Moretti M, Obrist MK, Duelli P (2004) Arthropod biodiversity after
forest fires: winners and losers in the winter fire regime of the
Southern Alps. Ecography 27:173–186
Moretti M, de Bello F, Roberts SPM, Potts SG (2009) Taxonomical
vs. functional responses of bee communities to fire in two
contrasting climatic regions. Journal of Animal Ecology 78:
98–108
Mullen K, Fahy O, Gormally M (2003) Ground flora and associated
arthropod communities of forest road edges in Connemara,
Ireland. Biodiversity and Conservation 12:87–101
Neumann FG (1991) Responses of litter arthropods to major natural
or artificial ecological disturbances in mountain ash forest.
Australian Journal of Ecology 16:19–32
Neumann FG (1992) Responses of foraging ant populations to high-
intensity wildfire, salvage logging and natural regeneration
processes in Eucalyptus regnans regrowth forest of the Victorian
Central Highlands. Australian Forestry 55:29–38
Noss RF (1996) The naturalists are dying off. Conservation Biology
10:1–3
Perner J, Voigt W, Ba
¨hrmann R, Heinrich W, Marstaller R, Fabian B,
Gregor K, Lichter D, Sander FW, Jones H (2003) Responses of
arthropods to plant diversity: changes after pollution cessation.
Ecography 26:788–800
Petchey L, Gaston KJ (2002) Functional diversity (FD), species
richness and community composition. Ecology Letters 5:402–411
Petchey L, Gaston KJ (2006) Functional diversity: back to basics and
looking forward. Ecology Letters 9:741–758
Pujade-Villar J, Ferna
´ndez-Gayubo S (2004) Himeno
´pteros. In:
Barrientos JA (ed) Curso pra
´ctico de entomologı
´a. Servei de
Publicacions de la Universitat Auto
`noma de Barcelona, Barce-
lona, pp 813–854
Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, London
Rollan A, Real J (2010) Effect of wildfires and post-fire forest
treatments on rabbit abundance. European Journal of Wildlife
Research. doi:10.1007/s10344-010-0412-y
Rosenberg MS (2004) Passage version 1.1. Pattern analysis, spatial
statistics and geographic exegesis.\www.passagesoftware.net[.
Arizona State University
Santos X, Poquet JM (2010) Ecological succession and habitat
attributes affect the post-fire response of a Mediterranean reptile
community. European Journal of Wildlife Research 56:895–905
Santos X, Bros V, Min
˜o A (2009) Recolonization of a burnt
Mediterranean area by terrestrial gastropods. Biodiversity and
Conservation 18:3153–3165
Shaw MR, Hochberg ME (2001) The neglect of parasitic Hymenop-
tera in insect conservation strategies: the British fauna as a prime
example. Journal of Insect Conservation 5:253–263
ter Braak CJF, Smilauer P (1997–2002) CANOCO for windows
version 4.5. Biometrics-Plant Research International
Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ,
Collingham YC, Erasmus BFN, Ferreira de Siqueira M, Grainger
A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley
GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL,
Williams SE (2004) Extinction risk from climate change. Nature
427:145–148
Vance CC, Smith SM, Malcolm JR, Huber J, Bellocq MI (2007)
Differences between forest type and vertical strata in the
diversity and composition of Hymenpteran families and Mym-
arid Genera in Northeastern Temperate Forests. Environmental
Entomology 36(5):1073–1083
Vandewalle M, de Bello F, Berg MP, Bolger T, Dole
´dec S, Dubs F,
Feld CK, Harrington R, Harrison PA, Lavorel S, Martins da
Silva P, Moretti M, Niemela
¨J, Santos P, Sattler T, Sousa JP,
Environmental Management (2011) 48:1000–1012 1011
123
Author's personal copy
Sykes MT, Vanbergen AJ, Woodcock BA (2010) Functional
traits as indicators of biodiversity response to land use changes
across ecosystems and organisms. Biodiversity and Conservation
19:2921–2947
Voigt W, Perner J, Jones H (2007) Using functional groups to
investigate community response to environmental changes: two
grassland case studies. Global Change Biology 13:1710–1721
Weslien J, Schroeder LM (1999) Population levels of bark beetles and
associated insects in managed and unmanaged spruce stands.
Forest Ecology and Management 115:267–275
Whitehead P (1990) Systematics—an endangered species. Systematic
Zoology 39:179–184
Wood A, Stedman-Edwards P, Mang J (eds) (2000) The root causes
of biodiversity loss. Earthscan Publications Ltd, London
1012 Environmental Management (2011) 48:1000–1012
123
Author's personal copy
