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Journal of Insect Conservation
An international journal devoted to
the conservation of insects and related
invertebrates
ISSN 1366-638X
J Insect Conserv
DOI 10.1007/s10841-017-9993-z
Diversity of spiders and orthopterans
respond to intra-seasonal and spatial
environmental changes
Konstantina Zografou, George
C.Adamidis, Marjan Komnenov,
Vassiliki Kati, Pavlos Sotirakopoulos,
Eva Pitta & Maria Chatzaki
1 23
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Vol.:(0123456789)
1 3
J Insect Conserv
DOI 10.1007/s10841-017-9993-z
ORIGINAL PAPER
Diversity ofspiders andorthopterans respond tointra-seasonal
andspatial environmental changes
KonstantinaZografou1 · GeorgeC.Adamidis2· MarjanKomnenov1·
VassilikiKati3· PavlosSotirakopoulos1· EvaPitta1· MariaChatzaki1
Received: 5 May 2016 / Accepted: 22 May 2017
© Springer International Publishing Switzerland 2017
and cover of stones was a determinant factor for Orthop-
tera only. There was a significant congruence between the
two groups and Orthoptera provided the best complemen-
tary network. Our results show that diversity patterns of
both spiders and Orthoptera are sensitive to environmental
changes even over short time-scales (e.g. within the sum-
mer period) and space (e.g. across different habitat types),
suggesting that small inexpensive experimental designs
may still reveal community dynamics. For conservation
purposes, we advise a focus on variables regulating habitat
heterogeneity and microhabitat characteristics. We provide
a list of the most influential species and propose the most
effective network for obtaining information on the local
fauna.
Keywords Arthropods· Canopy· Grasshoppers·
Spiders· Diversity· Mediterranean· Seasonality·
Functional groups· Conservation
Introduction
Despite the fact that 85% of all animal species are arthro-
pods, studies examining diversity shifts in ground-dwelling
arthropods are less common than those examining shifts in
vertebrates or charismatic arthropod taxa such as butter-
flies and moths (Chen etal. 2011). In the Mediterranean,
and especially in Greece, arthropod surveys are scarce
and our taxonomic knowledge is still limited, mainly due
to the extreme diversity of the fauna and the relatively few
taxonomists that specialize on this group (Behan-Pelletier
and Newton 1999). Additionally, practical difficulties for
their collection (e.g. cryptic lives, inaccessible microhabi-
tats, short biological cycles) make primary data difficult to
obtain. The lack of basic knowledge on their diversity in an
Abstract Our understanding of arthropod responses to
environmental pressures is limited, especially for the poorly
studied Mediterranean region. In the light of likely fur-
ther environmental change and the need for protocols for
rapid biodiversity assessment, we measured how the abun-
dance and species richness of two taxa, ground spiders and
Orthoptera, belonging to different functional groups, fluc-
tuates intra- seasonally (early-mid-late summer) and across
habitat types (grasslands, maquis, forests). We also tested
their surrogate value. Spiders were found to have higher
species richness and abundance almost throughout the
investigation. Orthoptera had lower species richness and
abundance in forests compared to grasslands and maquis,
while no significant difference between habitats was
revealed for spiders. Early-summer was the richest period
for spiders while mid-summer was the richest for Orthop-
tera. Canopy cover was found to significantly influence
community composition of both groups, while herb height
Electronic supplementary material The online version of this
article (doi:10.1007/s10841-017-9993-z) contains supplementary
material, which is available to authorized users.
* Konstantina Zografou
ntinazografou@yahoo.co.uk
1 Department ofMolecular Biology andGenetics, Democritus
University ofThrace, Dragana, 68100Alexandroupoli,
Greece
2 Biodiversity Conservation Laboratory, Department
ofEnvironment, University oftheAegean, 81100Mytilene,
Lesbos, Greece
3 Department ofBiological Applications andTechnology,
University ofIoannina, 45110Ioannina, Greece
4 Present Address: Temple University, 1900 North 12th Street,
19122Philadelphia, PA, USA
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area hinders ecological research or conservation (Agnars-
son and Kuntner 2007). This explains the almost complete
absence of arthropods from conservation planning at a
national level (Sfenthourakis and Legakis 2001).
Functional groups of species (i.e. sets of species encom-
passing a variety of similar functional attributes) (Díaz
and Cabido 1997) contribute in a similar way to ecosystem
services and properties and thus permit generalizations on
species responses to environmental change (Wilson 1999).
The use of systems of interacting functional groups that
reflect environmental change differently (rather than indi-
vidual species) is an effective way of organizing empirical
research in ecology, thus increasing the value of monitor-
ing (Barton 2011). Investigating changes in arthropod func-
tional groups is a very efficient biodiversity shortcut that
could improve understanding of their ability to respond
to environmental change and provide a useful gateway to
more efficient conservation planning.
This has led us to focus on understanding the environ-
mental factors influencing diversity patterns of arthropods
in the Mediterranean region by combining data on two
different functional groups in different habitats. We chose
ground dwelling spiders (predators) and Orthoptera (herbi-
vores) in one of the most diverse areas in N.E. Greece, the
Dadia-Leukimi-Soufli National Park (Dadia NP hereafter).
Our aim was also to provide conservation biologists with
a tool to help develop effective strategies for conservation
planning in Dadia NP, focusing specifically on arthropods.
Spiders are among the most abundant predators of inver-
tebrates in terrestrial ecosystems (Symondson etal. 2002).
They are significant predators of many herbivore species
and also provide food for other canopy foragers, such as
ants and birds (Halaj etal. 1997). They also contribute to
many ecosystem processes (e.g. nutrient cycling (Lawrence
and Wise 2000)). The high taxonomic and functional diver-
sity of spiders justifies their use as a model group for study-
ing large-scale ecological patterns (Birkhofer and Wolters
2012; Cardoso et al. 2011). Orthopterans are apparently
under threat as their diversity declines in many temperate
regions (Marini etal. 2010), and in Europe 50% are consid-
ered endangered (Hochkirch etal. 2016). In addition, they
are important primary and secondary consumers in grass-
land ecosystems, and they provide an abundant source of
prey for many predators (e.g. insectivorous birds, spiders).
For several regions and biomes Orthoptera have been sug-
gested as appropriate bioindicators (Báldi and Kisbenedek
1997) due to their sensitivity to microclimatic conditions
(Zografou etal. 2009).
Thermal conditions are known to greatly affect all
arthropods because increased ambient temperatures have a
direct effect on their metabolic rates, activity patterns and
developmental rates. For Orthoptera, thermal conditions
might even determine their ability to avoid predators (Pitt
1999). For spiders, different climatic conditions between
early and late spring were found to affect their activity and
density patterns (Öberg et al. 2008). Given that climatic
variability operates over all time scales, even very short
ones (Ghil 2002), different thermal conditions within sea-
sons may control species activity patterns (e.g. within sea-
son abundance shifts), leading to sizeable effects at the
community level.
Another factor that is known to drive diversity patterns
of both ground spiders and Orthoptera is vegetation com-
position and structural characteristics including herb cover
and height, bare ground, and cover of stones (Standish
2004; Stromberg and Tellman 2012). Structural differences
can modify temperature, light intensity, and soil moisture,
which in turn can determine the distribution and diversity
patterns of arthropods (Guido and Gianelle 2001; Nufio
etal. 2010). An example of changes in vegetation structure
is forest re-establishment at the expense of open areas (Bar-
bero etal. 1990; Debussche etal. 1999) due to the reduction
of human densities in many rural areas in the Mediterra-
nean. This, in turn, has led to reduced species richness and
diversity of ground spiders (Zakkak etal. 2014). Likewise,
vegetation coverage and habitat desiccation were found to
constrain the distribution of spiders (Lambeets etal. 2008;
Perner and Malt 2003). Changes in other habitat-specific
variables such as the cover of flower-heads, presence of
shrubs or altitudinal changes were shown to greatly influ-
ence the Orthoptera community (Zografou etal. 2009).
The northern part of Greece was recently found to have
the most prominent seasonal trend in terms of temperature
alterations during the summer as opposed to the winter or
autumn period (Mamara et al. 2016). Given that weather
conditions from June to August are clearly distinct, Dadia
NP provides an excellent opportunity to study the intra-
seasonal activity of arthropods over a short time span i.e.
within summer.
Recent studies in Dadia NP showed that changes in tem-
perature have already impacted diversity patterns, commu-
nity composition and phenological patterns of butterflies
and orthopterans (Zografou et al. 2014, 2015). Further
climate warming (IPCC 2013) is likely to affect spiders
and orthopterans differently (Barton 2010, 2011), and also
cause changes in vegetation structure (Debussche et al.
1999). We adopted this combined approach of time- and
habitat-dependent structure and we documented the differ-
ences on diversity patterns of these two functional groups.
Specifically, we addressed the following questions: (a)
is there a significant difference in abundance and richness
of spiders and orthopterans intra-seasonally? (b) is there a
consistent effect of habitat type on diversity of spiders and
orthopterans? (c) are there any common habitat-specific
variables shaping spider and orthopteran community com-
position? and (d) which species are responsible for possible
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differences in the community structure intra-seasonally and
between habitats? Since each taxon displays an individual-
istic response to current pressures, dictated by its specific
ecological demands (Peñuelas et al. 2013; Rapacciuolo
etal. 2014) we expected to find significant differences in
activity patterns of the study organisms. In particular, we
expected that microhabitat characteristics (e.g. flower-
heads, shrubs, stones) will have a significant impact on
Orthoptera (Kati etal. 2004; Zografou etal. 2009), while
habitat characteristics such as openness (e.g. grasslands)
or closeness (e.g. forests) would affect spiders (Buchholz
2010; Zakkak etal. 2014). For spiders, we expected to find
increased activity in grasslands or maquis in the early-sum-
mer period, as spiders are known to populate open areas
during that time, after leaving their overwintering sites
(Bertrand etal. 2016). Previous studies on the phenology
of ground spiders in other Mediterranean areas (i.e. Maja-
das and Urones 2002; Jiménez-Valverde and Lobo 2006;
Cardoso etal. 2007) or in Greece (i.e. Chatzaki etal. 1998,
2005) confirm that late spring to early autumn is the period
of maximum activity, with variations depending on local
climate fluctuations. Our previous studies of Orthoptera in
the study area (Kati etal. 2004) and elsewhere (Kati etal.
2012; Zografou etal. 2009) showed that peak abundance
occurs in mid-summer, i.e. the hottest period of the sea-
son. Finally, we explored the value of ground spiders and
Orthoptera as biodiversity surrogates as well as their com-
plementarity. When data availability and funds are limited
but diversity is high, it is suggested to rely on few biodi-
versity surrogates for data acquisition, suitable for proper
prioritization of conservation efforts.
Materials andmethods
Study area andsites
The study area was Dadia NP in N.E. Greece
(41°07′–41°15′N, 26°19′–26°36′E) (Fig. 1). It is a hilly
area extending over 43,000ha, with altitudes ranging from
20 to 650m. It includes two strictly protected core areas
(7290 ha), where only low-intensity activities such as
extensive grazing and selective wood cutting are allowed
on a periodical basis. The climate is sub-Mediterra-
nean, with a mean annual rainfall of 653mm and a mean
annual temperature of 14.3 °C, (min in January and max
in July–August), while the hot and arid summer season
extends from July to September (mean temperature 25 °C,
mean rainfall 210mm) (Maris and Vasileiou 2010). Along
with the dry and hot summers that characterise Dadia NP,
a significant increase in average temperature of 0.95 °C has
been documented in a 22 year-period (1990–2012) (Zogra-
fou et al. 2014). Seventy-five percent of the reserve is
covered by pinewoods (Pinus nigra, Pinus brutia), broad-
leaved woods (Quercus frainetto, Quercus cerris, Quercus
pubescens), mixed pine-oak woods and maquis, whilst
Fig. 1 Map of Greece showing
the location of Evros prefec-
ture (left figures), the area of
Dadia-Lefkimi-Soufli National
Park (right figure) with the core
areas (polygons in dotted lines)
and the 12 sites where sampling
took place. Two out of the
twelve sites are located outside
the borders of the National Park
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the semi-open forested zone covers 5%, agricultural fields
cover 16% and grasslands and open habitats cover only 4%
(Poirazidis etal. 2002). Both pine and oak habitats reflect
the original Mediterranean vegetation at low altitudes. We
recognised three dominant habitat types: forests, grass-
lands and maquis and we located four sampling sites in
each, resulting to a total of 12 sites (Supplementary Online
Material, TableS1). The mean distance between sites was
1.2 km ± 0.5 (SE) so that each site represented an inde-
pendent sample in which diversity measures depend much
more on local activity of organisms than on immigration
from neighbouring sites.
Arthropod sampling
On the basis of a significant intra-seasonal variation of
mean temperature values from early to late summer (June
has significantly lower temperature from July and July
greater than August) sampling was conducted during the
extended summer period from late May to early Septem-
ber 2011. Orthoptera sampling was conducted along two
transects of 30m length and 2m width in each sampling
site, with a minimum distance of 100 m between the 24
transects. Adult specimens of Orthoptera were caught in a
sweep net, counted, and identified ex situ using the Greek
Orthoptera guide (Willemse 1985). Ground dwelling spi-
ders were sampled using pitfall traps. Five traps were
located at 10m intervals along every orthopteran transect,
(5 traps/transect and 10 traps/site) resulting in a total of 120
traps. The traps remained active for 94 (± 6) days on aver-
age from late May to early September and were emptied
three times. The three sampling periods were: 20. 5–25. 6.
2011 (early-summer), 25. 6–27. 7. 2011 (mid-summer) and
27. 7–3. 9. 2011 (late-summer). On average only nine (± 1)
traps were active per site due to losses from animal interfer-
ence and heavy rain. Each trap was filled with 200ml of
ethylene glycol (preservative) and was covered with a stone
roof for protection against rain. Samples were transferred
to 95% isopropyl-alcohol and subsequently sorted. As there
are no extensive keys available for Greek spiders, identifi-
cation was from existing literature related to the region and
the online database for European spiders (http://www.ara-
neae.unibe.ch/). Our taxonomic results were presented in a
separate paper (Komnenov etal. 2016). Species names fol-
low the nomenclature of the World Spider Catalog (Catalog
2016). The material is deposited in the Araneae collection
of the Natural History Museum of the University of Crete.
Habitat-specific variables
We recorded ten habitat-specific variables for orthopterans
and spiders in standard plots (5 ×2m2) by systematically
locating four orthopteran plots along each transect (every
10m: 96 plots) and one spider plot around every pitfall trap
(120 plots). Using a hand GPS we took the coordinates and
recorded the altitude (1). To estimate the temperature (2)
and soil humidity (3) at each site, we extracted data from
a Hobo data logger (U12) that was placed at the beginning
of each orthopteran transect and remained there for as long
as the sampling was conducted (15min with one record per
minute). In addition, we estimated the average percentage
canopy cover (4) per plot using a spherical densiometer
(measures at four cardinal directions in July 2011), as well
as the cover of herbs (5), shrubs (6), bare ground (7) and
stones (8) using the Braun–Blanquet scale (5: 75–100%,
4:50–75%, 3: 25–50,% 2: 5–25%, and 1: 0–5%). Finally,
we estimated mean herb height (9) as the average of four
measures corresponding to four dominant herb species as
well as the number of flower-heads (10) in May (2011)
using a five grade scale (1 ≤ 10, 2 > 10, 3 > 50, 4 > 100,
5 > 200).
Data analysis
Our dataset consisted of 12 sites and three samples (early-
mid-late summer period). In order to standardize sampling
effort in the whole experiment, for each sample in each site,
we estimated spider abundance as the total number of indi-
viduals caught in all pitfall traps, divided by the number of
active traps and the number of active sampling days, multi-
plied by 1000 thus rendering it to a standardised measure of
number of individuals per 1000 trap-days. For Orthoptera,
we considered both transects in each site as one sample
and we estimated a mean value of Orthoptera abundance in
terms of the number of individuals counted per site. Beta-
diversity was also used to quantify species turnover within
the summer period and across the habitat types using Whit-
taker’s formula for beta diversity (bw = S/ā − 1), where S
is the total number of species in that period or habitat and
ā the average number of species in these periods or habi-
tats (Whittaker 1960). We calculated the proportion of spe-
cies exclusively found in only one repetition for each target
group separately.
The time andhabitat effect indiversity patterns
We used general linear models to investigate differences
in ground spider and Orthoptera species (a) richness
and (b) abundance in time and habitat types. In particu-
lar, each model described the response variable (species
richness or species abundance) as a function of the fac-
tors “taxon”, “intra-season”, “habitat type”, “site” and the
interactions of “taxon×intra-season” and “taxon×habi-
tat type”. The response variables were normalized using
log-transformation allowing the specification of a normal
error distribution. Models were validated by checking for
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homoscedasticity and normality of the residuals (Zuur
etal. 2009), and in all cases, diagnostic graphs showed that
model assumptions were met. Post-hoc tests (Tukey) were
conducted to further explore the interaction terms. Statis-
tical analyses were performed in R (R Core Team 2014)
using library faraway for lm () function, and library esti-
mability for lsmeans () function for post hoc tests (Lenth
2016).
The effect ofhabitat-specific variables incommunity
composition
In order to explore the effect of habitat-specific variables
(ten in total) on species composition, we conducted Redun-
dancy Analysis (RDA) using CANOCO software (ter Braak
and Smilauer 2002). Preliminary analyses were made
using Detrended Correspondence Analysis [DCA, Hill and
Gauch (1980)] to check the magnitude of change in spe-
cies composition along the first ordination axis. Since the
gradient length was found to be smaller than 4 SD-units
(gradient length in standard deviation (SD) units, RDA
was the appropriate ordination method to perform analysis
and determine how much of the variation in species data
is accounted for by the environmental data (Ter Braak and
Prentice 1988). The RDA method extracts the major gra-
dients in the data that are accounted for by the measured
environmental parameters. The position of a species in the
resulting diagram indicates the degree of dependence on
the closest environmental parameters (arrows). The dia-
gram shows only the species sufficiently influenced by the
parameters (fit > 10%), and only the significant (P < 0.05)
environmental variables that did not show collinearity
(1,000 iterations of the Monte–Carlo test).
The most influential species
To pinpoint the most influential spider and orthopteran spe-
cies that contributed most to the observed differences dur-
ing the three summer periods and between open and closed
canopy cover areas, we used the SIMPER (Similarity
Percentage) method and the Bray-Curtis similarity meas-
ure (Clarke 1993). The classification between open and
closed areas was done on the basis of canopy cover per-
centage (%): sites with >50% of canopy cover were clas-
sified as closed and sites with <50% as open. In addition,
each species was given a vulnerability index from one (the
least vulnerable) to three (the most vulnerable). An index
of “one” was attributed to species that were found to be
the most influential during the mid-summer period. This
is because they are expected to be better synchronized to
their food resources compared to species represented ear-
lier or later (Donoso etal. 2016). An index of “two” was
given to species that increased their influential role in
late-summer, but for which the open/closed areas did not
seem to be effective. An index of “three” was given to spe-
cies that were found to be most influential both in the early-
or late-summer period and in open habitats. One of the best
studied species responses to climate change is the advanced
appearance. The response is more pronounced for species
that appear early or late in the season (McKinney et al.
2012). Therefore, species that will be found to be the most
influential in terms of the early- or late-summer period are
expected to have a higher vulnerability in the light of cli-
mate warming. Also, as the open areas are known to posi-
tively affect arthropod communities, if these areas are lost
or decreased at the expense of forests, this might present a
possible threat to these arthropods. We used PAST version
2.17c for SIMPER analysis (Hammer etal. 2001).
Surrogate value
We tested the surrogate value of (a) ground spiders and
(b) Orthoptera by comparing the congruence of their spe-
cies richness patterns using the Spearman rank correlation
coefficient. Using one group as the surrogate group and the
other as the target group, we formed the complementary
network after the surrogate group, starting with the most
species-rich site and adding those sites progressively con-
tributing more new species, until all species were included
in the network (Cardoso etal. 2004; Zografou etal. 2009).
By calculating the proportion of species in every group
included in each step of the networking procedure, we were
able to assess the most efficient complementary network,
thus eliminating the bias of the different number of sites
forming the network.
Results
Single taxon diversity
Our dataset consisted of 136 spider species (22 fami-
lies, 2,403 individuals) out of which 12 species are new
records for Greece and seven species are new for science
(Komnenov etal. 2016) (Supplementary Online Material,
Table S2). The most abundant families were Gnaphosi-
dae (36.5%; 878 ind.), Dysderidae (20.6%; 496 ind.) and
Lycosidae (16%; 392 ind.). More spider species (26%)
were encountered exclusively in early summer and fewer in
mid (13%) and late summer (12.5%). Species turnover was
lower from the first to the second period (bw = 0.36) and
second to third (bw = 0.48) than first to third (bw = 0.54).
Accordingly, species turnover was greater between forests
and maquis (b
w = 0.67), and between forests and grass-
lands (b
w = 0.6) than grasslands and maquis (bw = 0.34).
We recorded 39 species of orthopterans (five families,
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2,628 individuals), with Acrididae (57%; 1,497 ind.) and
Tettigoniidae (34%; 893 ind.) being the most abundant
families (TableS2). The most important species in terms
of conservation, listed as endangered in the IUCN 2016
list (Hochkirch etal. 2016) is Paranocarodes chopardi, an
apterous pamphagid, with low dispersal ability that renders
it prone to extinction if its habitat changes (Kati and Wil-
lemse 2001). Most orthopteran species were encountered
exclusively in mid-summer (20.5%), fewer in early summer
(15.4%) and the least in late summer (8%). Species turno-
ver was higher from the first to the second period (bw=0.7)
and first to third (bw=0.6) than second to third (bw=0.37).
Species turnover across habitat types was higher between
forests and grasslands or maquis (bw = 0.5) than between
grasslands and maquis (bw =0.38).
The effect oftime andhabitat type ondiversity patterns
The main effects of “taxon”, “habitat type” and “site” on
abundance were significant, while no significant main
effect of “intra-season” was revealed (Table 1). The post-
hoc Tukey test for the factor “taxon” showed a significantly
higher abundance for spiders than Orthoptera (P < 0.001).
Forests had significantly lower abundance than both grass-
lands and maquis habitats (Tukey: P = 0.003 and P = 0.038
respectively), while grasslands and maquis had similar
abundance (Tukey: P = 0.61). The two interactions included
in the model were found to be significant at the 0.05 level
(Table1) indicating that differences between both habitat
types and intra-seasonally affected the response of abun-
dance to taxon. The post-hoc Tukey tests revealed that
spiders always had higher abundance than Orthoptera
(Fig.2a, b) except in the maquis habitats (P = 0.07; Fig.2a)
and in the mid-summer period which were marginally
significantly different in abundance (P = 0.056; Fig. 2b).
Orthoptera were significantly less abundant in forests
than in grasslands (Tukey: P = 0.005; Fig.2a) and maquis
habitats (Tukey: P = 0.007; Fig. 2a). However, the abun-
dance of orthopterans was similar in grasslands and maquis
(Tukey: P = 0.062; Fig.2a). Interestingly, spider abundance
did not significantly differ in the different habitat types
(Tukey: P > 0.05 in all cases; Fig.2a). Finally, there was no
Table 1 Effect of habitat
type and intra-seasonal
differentiation between the
two taxa (ground spiders,
Orthoptera) in terms of species
richness and abundance
Response Predictors df F value P value Tukey post hoc tests
Abundance Habitat type 3 586.63 *** Grassland > forest
Taxon 1 80.68 *** Spiders > Orthoptera
Intra-season 2 0.23 ns
Sites 9 2.87 **
Habitat type × taxon 2 6.93 ** (See Fig.2a)
Intra-season × taxon 2 8.00 *** (See Fig.2b)
Species richness Habitat type 3 435.12 *** Grassland, maquis > forest
Taxon 1 114.27 *** Spiders > Orthoptera
Intra-season 2 0.59 ns
Sites 9 1.29 ns
Habitat type × taxon 2 0.51 ns (See Fig.3a)
Intra-season × taxon 2 12.31 *** (See Fig.3b)
Fig. 2 Abundance of Orthoptera and spiders across a different habi-
tat types and b intra-seasonally. Different lower case letters indicate
significant differences (at P < 0.05) among the two taxa, by Tukey
post-hoc tests. All results are means of original data ± SE
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significant difference in abundance of either taxa intra-sea-
sonally (Tukey: P > 0.05 in all cases; Fig.2b).
The second model, with species richness as the response
variable, showed that the main effects of the factors
“taxon” and “habitat type” were significant, but not signifi-
cant was the effect of “intra-season” and “site” (Table1).
Species richness was significantly higher for spiders than
for Orthoptera (Tukey: P < 0.001). In addition, grass-
lands and maquis had higher species richness than forests
(Tukey: P < 0.001 in both cases; Fig.3a), while grasslands
and maquis had similar species richness (Tukey: P = 0.82;
Fig. 3a). The only significant interaction “taxon × habitat
type” indicates that differences between habitat types did
not affect the response of species richness to taxon. Spiders
had significantly higher species richness than Orthoptera,
across all different habitat types (Fig.3a) and intra-season-
ally (Fig. 3b). Orthoptera had significantly lower species
richness in forests than in grasslands (Tukey: P = 0.005;
Fig. 3a) and maquis habitats (Tukey: P = 0.006; Fig.3a).
However, orthopterans had similar species richness in
grasslands and maquis (Tukey: P > 0.05; Fig. 3a). The
species richness of spiders was not significantly different
across the different habitat types (Tukey: P > 0.05 in all
cases; Fig. 3a). Orthoptera presented significantly lower
species richness values in the early-summer than in the two
following periods (Tukey: P = 0.002 and P = 0.001 respec-
tively; Fig.3b), while the mid and late-summer had simi-
lar species richness (Tukey: P > 0.05 in all cases; Fig.3b).
On the contrary, spiders had significantly higher species
richness in early-summer than in the late-summer (Tukey:
P = 0.04; Fig.3b), while the mid-summer period had simi-
lar species richness to all other periods (Tukey: P > 0.05 in
all cases, Fig.3b).
Environmental factors shaping community composition
Among habitat-specific variables, increased canopy cover
was found to be the most influential factor for spider com-
munities, negatively affecting 72% of the species (61%
of the total variance explained, Fig. 4). Among newly
described spider species, some (Dysdera kati, Dysdera
krisis and Harpactea wolfgangi) were positively affected
by increased canopy cover, while others (Harpactea ice,
Phrurolithus thracia and Zodarion beroni) were nega-
tively affected (Fig. 4, Table S2). In addition to canopy
cover, herb height and cover of stones were found to sig-
nificantly influence the Orthoptera community. Increased
canopy cover negatively affected 74% of species, while
P. chopardi, a typical species for semi-shaded oak woods
with Mediterranean scrub undergrowth and leaf litter (Kati
etal. 2010), was positively affected by this factor. Increased
herb height and cover of stones positively affected 59 and
64% of species respectively (46.5% of the total variance
explained, Fig.4, TableS2).
Most influential species
Nine spider species belonging to six families were respon-
sible for more than 50% of the intra-seasonal differences,
while six species were responsible for the differences
between open and closed canopy areas; six species were
common in both cases (Table2). For Orthoptera, SIMPER
analysis indicated seven species that explained more than
50% of the differences intra-seasonally and between closed
and open canopy areas (Table2).
Surrogate value
We found significant congruence between patterns of
species richness of spiders and Orthoptera (rho = 0.73,
P = 0.007). Orthoptera served as the best surrogate group
where complementarity is concerned. Their network
included nine sites as opposed to twelve sites of the spider
Fig. 3 Species richness of Orthoptera and spiders across a differ-
ent habitat types and b intra-seasonally. Different lower case letters
indicate significant differences (at P < 0.05) among the two taxa, by
Tukey post-hoc tests. All results are means of original data ± SE
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J Insect Conserv
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network, which, basically, corresponded to the whole study
system (12 sites). The Orthoptera network conserved 88.9%
of the ground spider species and when comparing the aver-
age species richness included in each step of the comple-
mentary network selection, it succeeded in conserving
even more orthopterans (13%) and lost only 6.6% of spider
species.
Discussion
Time andhabitat effect
In this study, we found both season and habitat type sig-
nificantly influenced the arthropod assemblages in the
Dadia NP. As expected, responses were not consistent
between Orthoptera and spiders and their diversity meas-
ures. Regarding the within-season results, patterns of
variation in both species richness and abundance between
the two groups were different. Also, ground spiders were
always more abundant and rich in species than Orthop-
tera, except during the mid-summer period where differ-
ences in abundance of the two groups were not signifi-
cant. The species turnover analysis showed that many of
the spider species that are highly active in the early-sum-
mer period, also persist into mid-summer, but then they
are replaced by a few other species that are only highly
active in late summer. This phenological pattern has been
reported for Mediterranean Gnaphosidae before (Chat-
zaki etal. 2005). The analysis of the most influential spe-
cies showed that there are two highly influential spider
species with maximum activity in the early summer (Har-
pactea babori and Pardosa alacris) and two in the late
summer (Scytodes thoracica and Zelotes erebeus), but
only one in mid-summer (Civizelotes caucasius). These
observations, in conjunction with the short life cycle of
Orthoptera with peak activity in mid-summer (Kati etal.
2004) could explain the reduced differentiation between
the two groups during this period. The higher species
richness of spiders in the early-summer period indicates
the importance of this season for local biodiversity sug-
gesting it is the optimal time for sampling spiders in case
of low duration/budget inventories.
The results showed that grasslands and maquis hosted
more species than forests in both taxa examined. Habi-
tat openness, therefore, is the main driver of spider and
Orthoptera species richness in Dadia NP (Kati etal. 2004).
In fact, the positive effect of the open habitat structure
explains the lack of any significant interaction between the
factors “taxon” and “habitat type” in our models. How-
ever, for spider abundance, the pattern is not repeated since
both forests and grasslands host an equally high number of
individuals, resulting in non-significant variation among
habitat types (Fig.2a). Five out of the six most important
spider species that affect differences between open and
closed canopy cover areas had maximum activity in closed
forest habitats. Species turnover analysis, however, showed
that species inhabiting forests differed from those of grass-
lands or maquis, clearly demonstrating niche separation of
ground spiders. Given the lower species richness in forests,
a lessened inter-species competition may be expected and
hence an increase in the numbers of individuals of the spe-
cies that persist there. The preference of some of the spe-
cies for closed habitats has been previously documented, as
in the case of P. alacris which is known to prefer deciduous
oak and beech woods (Töpfer-Hofmann etal. 2000). How-
ever in most cases this study is the first to demonstrate clear
ecological preferences of the spider species recorded.
Fig. 4 Redundancy analysis diagram (RDA) presenting the signifi-
cant (P = 0.05) environmental factors affecting the community of spi-
ders and Orthoptera. Only species with a fit of more than 10% are
shown. Full names of the newly described spider species (>10% fit)
are given on the plots while all others are symbolized with a num-
ber (for corresponding species numbers and names see TableS2). For
Orthoptera, only the name of the most important species in terms of
conservation concern is provided
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Table 2 Species responsible for the observed differences intra-seasonally and between open versus closed areas using the Bray–Curtis similarity measure
According to this index, species having their maximum abundance in the start or in the end of the summer period and indicative for open areas will take the highest index number (i.e. “three”)
O orthopteran, S spiders, Intra-seasonal maximum abundance in early-mid-late summer, Canopy maximum abundance in open or closed canopy cover areas, Summer contr% ranked percentage
abundance per species considering the summer period, Early-Mid-Late summer contr% percentage of abundance per species considering early-mid-late summer period, Canopy contr% percent-
age of abundance per species considering the whole study area (all 12 sites), Close–open contr% percentage of abundance per species considering either open or closed canopy cover areas, Vul.
Ind the vulnerability index for each species based on climate sensibility and vegetation alterations scenarios (further details in the main text)
Taxon Species name Intra-seasonal Canopy Summer contr% Early sum-
mer contr%
Mid sum-
mer contr%
Late sum-
mer contr%
Canopy contr % Close contr% Open contr% Vul. Ind
OChorthippus bornhalmi Late Open 12.44 0.792 0.417 1.79 7.80 2 3.5 3
OTylopsis lilifolia Mid Open 8.44 0.667 1.67 0.25 9.31 0.75 3.5 1
OPoecilimon brunneri Early Open 7.51 1.42 0 0 5.73 0.25 2 3
OCalliptamus italicus Mid Open 6.98 0 1.79 0.167 8.79 0 2.94 1
OAcrida ungarica Mid Open 6.92 0 1.46 0.375 7.84 0 2.75 1
OOedipoda caerulescens Mid Open 6.44 0 1.17 0.667 7.41 0.125 2.69 1
OPezotettix giornae Mid Open 5.51 0.25 0.875 0.458 5.83 1 1.88 1
SHarpactea babori Early Closed 14.25 23.2 4.42 5.83 23.82 88.30 6.00 3
SCivizelotes caucasius Mid Open 8.95 2.33 11.9 4.5 7.86 0.00 28.10 1
SScytodes thoracica Late Closed 6.63 1.5 3.25 7.92 6.31 19.80 9.13 3
SAlopecosa albofasciata Early Ineffective 4.82 7.17 0.417 0.167 3
SZodarion morosum Late Ineffective 4.71 2.25 3.17 4.33 2
SHogna cf. radiata Late Ineffective 4.05 0 2.42 3.83 2
SPardosa alacris Early Closed 4.05 10.5 1.92 0.333 6.93 37.50 0.38 2
SZelotes erebeus Late Closed 3.48 0 0 6.33 4.16 19.00 0.00 3
SDrassyllus praeficus Early Ineffective 2.04 4.5 1 0 2
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Orthoptera showed a consistent pattern of preference
for open canopy cover areas. As found in previous stud-
ies in Dadia NP (Kati etal. 2004) and elsewhere (Kati
etal. 2012; Zografou etal. 2009), our results for Orthop-
tera demonstrated the importance of open habitats for
the conservation of this group. The conservation value
of open habitats, and the importance of habitat-specific
variables (e.g. shade, herb height, stones) at a com-
munity level are discussed below (Guido and Gianelle
2001; Zografou etal. 2009).
Habitat-specific variables shaping community
composition
Both spider and orthopteran communities were negatively
affected by canopy cover (72 and 74% respectively). In
a recent review of biodiversity indicators for forest eco-
systems in Europe, the authors found that there is strong
evidence for a negative correlation between tree canopy
cover and spider species richness (Gao etal. 2014). Simi-
larly, a study conducted in the Greek mountains of Pindos
(Zakkak etal. 2014) showed that community composition
of ground spiders of the family Gnaphosidae is signifi-
cantly affected by land-abandonment with their diversity
and species richness being negatively correlated with for-
est cover. Orthoptera are well known to prefer open, dry
and warm habitats with short vegetation (Uvarov 1966),
although there are a few exceptions such as P. chopardi,
a species typical to oak woodlands with a very narrow
distribution restricted to Dadia NP and few localities in
Bulgaria (Kati etal. 2004).
The Orthoptera community was also found to be
greatly affected by herb height and concomitant changes
in rock cover. As herbs are the main food source for all
orthopterans, although bush-crickets have a mixed diet
consisting of other insects and flower parts, it seems rea-
sonable that increased herb cover positively affected 59%
of the species. With a range of more than half a meter,
herb height creates multiple microhabitats that can sup-
port a great variety of species with different ecological
requirements, providing also shelter from predators and
extreme climatic conditions (Kemp etal. 1990). However,
tall herbs might be an indication of increased shading or
lack of grazing that are well-known to negatively affect
egg and nymph development of some orthopteran species
(van Wingerden etal. 1991). The second element, rock
cover, seems to have an even greater positive influence
on Orthoptera (64%). It is known that rocks are important
structures, aiding in orthopteran thermoregulation as well
as providing shelter (Chappell 1983) and their positive
correlation to species richness has been previously dem-
onstrated (Crous etal. 2013).
The most influential species
Another interesting finding of this study is the list with
the most influential species (Table2). As climate warm-
ing is linked to a changing onset of phenological events
for a variety of taxonomic groups (Menzel et al. 2006;
Parmesan 2007; Primack etal. 2009) we expect that spe-
cies most abundant in early or late summer (e.g. Chorthip-
pus bornhalmi, Poecilimon brunneri, H. babori) will be
strongly influenced by climate warming. It is also plausi-
ble to assume that species that are most abundant in open
areas (e.g. Tylopsis lilifolia, Civizelotes caucasius) might
be seriously threatened by shifts in vegetation structure
such as, for example, forest encroachment on open habi-
tats (Debussche etal. 1999; IPCC 2013). On the basis of
anticipated further changes in climate and landscape, we
proposed a “vulnerability index” for each of the most influ-
ential species so that conservation efforts could be prior-
itized accordingly.
Surrogate value
Spiders and Orthoptera share no similar traits in their life
history and ecology (Barton 2011). However, our results
reveal a strong congruence in their species richness pat-
terns, suggesting the possible use of each taxon as a good
surrogate for the other. Although Orthoptera have been
previously tested for their surrogate value (Bazelet and
Samways 2012; Zografou et al. 2009), fewer studies can
be found on the surrogate value of spiders (but see Car-
doso etal. 2004), and none, to our knowledge, that inves-
tigates the surrogate value of spiders for Orthoptera and
vice versa. Given that, only recently, the rich spider fauna
of Dadia NP started to be investigated or described (Kom-
nenov etal. 2016), the identification of shortcuts such as
Orthoptera species network is expected to provide cost- and
time-effective monitoring schemes improving our ability
to better conserve the local fauna (Margules and Pressey
2000).
Conclusions
Seasonal variation in species activity is a normal event
in temperate ecosystems. However, our results demon-
strated that significant differentiation of species richness
and abundance can occur even within a season, such as
the summer period. Our findings highlight the value of
low-cost, short-term inventories for revealing commu-
nity dynamics and confirming that the choice of sampling
period is highly taxon-specific. Our study also suggests
the importance of open habitats for the conservation of
both herbivores and predators. However, some influen-
tial spiders’ species seem to benefit from closed habitats.
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Therefore, although the presence of grasslands or maquis
would greatly favour herbivores, forests too play a ben-
eficial role for spiders. It is suggested that for predators
and especially for spiders, preservation of landscape het-
erogeneity rather than openness is the most crucial factor
for their diversity as has been proposed in previous stud-
ies (Zakkak etal. 2014). In addition, the different effects
of other environmental factors we studied, showed that
arthropods do not respond in the same way, emphasizing
the need for multi-taxa approaches in ecological studies.
In the light of future land-use changes in the Medi-
terranean (Barbero et al. 1990; Debussche et al. 1999;
Gerard etal. 2010), we identified a pool of nine spiders
and seven orthopterans that drives community patterns
and can be a useful tool for conservation biologists.
Apart from its conservation value, this analysis offers a
well-documented observational framework of species
activity in the Mediterranean region, contributing to the
otherwise limited knowledge about their ecological pref-
erences. Finally, the proposal of the Orthoptera species
network as the best surrogate group in terms of comple-
mentarity accentuates the important role of biodiversity
studies in high biodiversity areas such as Greece. The
importance of spider and orthopteran diversity in the
Dadia NP, merits further ecological study and monitoring
in order to obtain detailed information on their popula-
tion trends.
To conclude, analysing summer samplings that incor-
porate both open and closed canopy sites with a high var-
iability of habitat-specific variables seems necessary to
better assess how time and habitat structure affect groups
with different ecological attributes. Conservation man-
agers should prioritize their conservation efforts in the
light of the most influential/vulnerable species but also
consider the complementarity value of Orthoptera when
planning future conservation actions.
Acknowledgements This project was co-funded by the European
Union (European Social Fund) and National Resources under the
Operational Programme “Education and Lifelong Learning” Action
81324 - SPIDOnetGR, ARISTEIA II Programme, NSRF 2007–2013.
In addition, it has been co-financed by the European Union (European
Social Fund - ESF) and Greek national funds through the Operational
Program “Education and Lifelong Learning” of the National Strategic
Reference Framework (NSRF) - Research Funding Program: Hera-
cleitus II. Investing in knowledge society through the European Social
Fund. We are grateful to the Forestry Department of Dadia NP, and
WWF for supporting the field research. Finally we wish to thank the
two anonymous reviewers for their valuable help in improving the
manuscript analyses and structure. We are deeply grateful to Dr A.
Russell-Smith who -as a native speaker – performed a thorough lin-
guistic revision of the last version of the manuscript.
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