Ecological Indicators 23 (2012) 323–331
Contents lists available at SciVerse ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
Saproxylic beetles as indicator species for dead-wood amount and temperature
in European beech forests
Thibault Lachat a,∗ , Beat Wermelinger a , Martin M. Gossner b , Heinz Bussler c , Gunnar Isacsson d ,
Jörg Müller b,e
a
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland
Chair for Terrestrial Ecology, Research Department Ecology and Ecosystem Management, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354 FreisingWeihenstephan, Germany
c
Am Greifenkeller 1b, 91555 Feuchtwangen, Germany
d
Swedish Forest Agency, P.O. Box 63, SE-281 21 Hässleholm, Sweden
e
Bavarian Forest National Park, Freyunger Str. 2, 94481 Grafenau, Germany
b
a r t i c l e
i n f o
Article history:
Received 19 January 2012
Received in revised form 5 April 2012
Accepted 10 April 2012
Keywords:
Habitat evaluation
Biodiversity
Monitoring
Nature conservation
Indicator species analysis
a b s t r a c t
Beech forests in Central Europe are under strong anthropogenic pressure. Yet they play a fundamental
role for biodiversity and are therefore increasingly considered in conservation activities. Sites of high
conservation value can be efficiently defined by the use of indicator species, but very few studies have
identified indicator species for beech forests on a continental scale. Here we determined the efficacy of
saproxylic beetles as indicator species for European beech forests and studied the effect of the amount
of dead wood and temperature on their presence. We analyzed data from 988 trap catches from 209
sites in 7 European countries. Using the flexible indicator approach, which allowed combinations of
two temperature groups (warm and cool) and three dead-wood amount categories (small, intermediate,
high) to be considered, we identified 127 indicator species. Generally, we found more indicator species
of beetles at warmer sites and at sites with larger amounts of dead wood. Indicator species at cooler
sites were found only in combination with larger amounts of dead wood. We present a comprehensive,
data-based list of indicator species of saproxylic beetle for near-natural beech forests, as required in the
framework of the European Natura-2000 concept for habitat evaluation. We identified the conspicuous
Lucanidae as the family with the highest percentage of indicator species and thus recommend it as a
priority indicator group for monitoring. Our results furthermore provide evidence that large amounts of
dead wood are particularly important in cool, montane beech forests for maintaining high diversity.
© 2012 Elsevier Ltd. All rights reserved.
1. Introduction
European Beech (Fagus sylvatica L.) is the dominant tree species
in temperate forests of Central Europe, even though beech forests
cover only a small percentage of their original area. Most of the
present-day beech forests in Europe have been strongly influenced
by humans (Peterken, 1996; Rose, 1992). Anthropogenic disturbance regimes of single-tree or group-wise logging and clear-cuts
dominate and have resulted in artificial structures (e.g., even-aged
forests) and highly fragmented beech forests (Odor et al., 2006).
The pressure on beech forests is expected to increase owing to a
growing demand for timber and fuel wood (Jonsell, 2007). This has
∗ Corresponding author. Tel.: +41 44 7392 309; fax: +41 44 7392 215.
E-mail addresses: [email protected] (T. Lachat), [email protected]
(B. Wermelinger), [email protected] (M.M. Gossner),
[email protected] (H. Bussler), [email protected]
(G. Isacsson), [email protected] (J. Müller).
1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecolind.2012.04.013
already and will increasingly lead to a population decline of many
species associated with dead wood (i.e., saproxylic species) and
old-growth forests and to local and regional extinctions (Siitonen,
2001).
Beech forests play a fundamental role for biodiversity in Central
Europe. For example, 70% of Central European saproxylic beetles
occur in beech-dominated forests (Müller et al., 2012). Therefore,
these forests are increasingly regarded in conservation activities.
The European Union addresses the conservation of almost every
type of beech forest through the Natura 2000 network, established
under the Habitats Directive (Council Directive 92/43/EEC, 21 May
1992), which protects the natural habitats and wild fauna and
flora. This ecological network of protected areas was established to
ensure the survival of Europe’s most valuable species and habitats.
Habitat losses are currently the most serious threats to species
and ecosystems; in forest ecosystems, biodiversity can be maintained by setting aside forest areas (Fahrig, 2001). One of the most
efficient strategies to set aside or monitor sites of high conservation value relies on species lists (Rondinini and Chiozza, 2010).
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T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
However, establishing species lists for all potential protected areas
to evaluate their contribution to the conservation of the overall
biodiversity would be too expensive (Margules and Lindenmayer,
1996).
Furthermore, the assessment of the conservation value of a site
based on the species richness might be affected by several factors, e.g., the size of the sampling unit, the extent of the study area
(Prendergast et al., 1993), the site productivity, and the number of
rare species (Dufrêne and Legendre, 1997). In addition, high diversity does not ensure that a site has a high ecological value (Dunn,
1994), as sites with high diversity do not necessarily provide the
best ecosystem or ensure the presence of characteristic, rare, or
spatially restricted species, especially those organized in metapopulations (Prendergast et al., 1993). It is therefore a great challenge
to derive valuable surrogates for assessing the conservation value
of forest areas. This challenge becomes apparent when selecting
forest areas to set aside and when monitoring the development of
areas of conservation value over time, as is done in the Habitats
Directive within the Natura 2000 network.
Representative diversity would be a more satisfactory criterion
for determining sites of high conservation value (Cousins, 1991;
Webb, 1989). This strategy requires a list of the typical species
assemblages for combinations of habitats and ecological factors
(Dufrêne and Legendre, 1997). As a result, the crucial step is choosing the best possible indicator species (Juutinen and Monkkonen,
2004), which is clearly needed in the fields of nature monitoring, conservation, and management (Dufrêne and Legendre, 1997).
Despite knowing what information is required, conservationists
are faced with the often unsatisfactory current practice in nature
conservation, especially for invertebrates. Within the Natura, 2000
network, only a few insect species are defined as relevant for evaluating the conservation value of a site. For example, in Germany,
only seven saproxylic beetle species are listed. Moreover, the selection of these species is based only on the opinion of an expert rather
than on analyses of comprehensive data sets. Thus, there is a great
need for a scientific-based development of indicator species lists
for particular habitats, such as European beech forests.
McGeoch (1998) classified indicator species into three categories: environmental, ecological, and biodiversity indicators.
Ecological indicators sensu McGeoch (1998) are used to monitor
habitat changes and to assess the impacts of disturbances on an
ecosystem. Being restricted to one or a few habitat types, they
are better indicators than habitat generalists due to their greater
susceptibility to environmental changes that can lead to local or
regional extinction (Carignan and Villard, 2002). Consequently,
they can be considered as indicator species (characteristic species)
or specialist species for a particular habitat.
Only a few studies to date have analyzed diversity data from
beech forests across several countries in Europe, and only the
amount of dead wood has been characterized as an indicator for
near-natural European beech forests, but without relating dead
wood to the species present (Christensen et al., 2005). All studies dealing with indicator species for natural conditions have been
restricted to only one small region of beech forests in Europe
(Brunet and Isacsson, 2010; Müller et al., 2008b; Winter et al.,
2005). Consequently, species lists resulting from these prior studies
are only meaningful on a local scale and do not meet the expectations of a European network of forest reserves aiming at protecting
the most seriously threatened habitats and species across Europe.
In the present study, we focus on saproxylic beetles as indicator species in beech-dominated forests throughout Europe. These
insects have been suggested as a suitable group for biodiversity
studies in beech forests (Brunet et al., 2010). We used recently
established statistical methods and considered temperature and
the amount of dead wood as major influencing variables. Temperature has a positive effect on species richness, as suggested by
Table 1
Number of sites and traps per site combination with the given dead wood amounts
and temperature. Bold: number of sites (209 sites in total), italics: number of traps
(988 in total).
Dead wood amount (m3 /ha)
≥70 (large amounts)
≥30 to <70 (intermediate amounts)
<30 (small amounts)
Number of sites/number of traps
Cool forest sites
Warm forest sites
18/129
13/50
73/256
21/154
31/168
53/231
the species-energy hypothesis (Wright, 1983). The amount of dead
wood has been shown to influence saproxylic beetles (Müller and
Bütler, 2010) and might also interact with temperature in its effect
on saproxylic beetles. We also determined the conservation value
of the identified indicator species with regard to their conservation status in various national and European lists (e.g., Red Lists).
Specifically, we addressed the following main questions:
1. Which saproxylic beetle species can serve as indicators for beech
forests with large amounts of dead wood in Central Europe?
2. Are there more indicator species in beech forests with a warm
climate than in beech forests with a cool climate?
3. Do dead wood and temperature interact in their effects on
saproxylic beetles?
2. Materials and methods
2.1. Data
We compiled a meta-database from data of various projects
in European beech forests in which flight-interception traps were
used. (see Müller et al., 2012 for more details). The final data set
differed slightly from that published by Müller et al. (2012) in
that data from France were excluded because Staphylinidae and
Pselaphidae were not identified to the species level. A total of
988 traps installed in 209 forest sites of 7 countries (Belgium,
Germany, Luxemburg, Sweden, Switzerland, Slovakia, and Ukraine)
were considered. To avoid pseudo-replications, data from traps
within a site with uniform environmental conditions were pooled,
and the average number of individuals per species was computed.
The number of traps pooled per site ranged from 1 to 18. Deadwood amount was classified into three categories: small amounts
(<30 m3 /ha), intermediate amounts (≥30 to <70 m3 /ha), and large
amounts (≥70 m3 /ha). Two temperature classes of sites were considered: cool (annual temperature mean: 6.8 ◦ C) and warm (8.4 ◦ C).
The threshold between cool and warm sites was determined by the
temperature median of the warmest month (15.8 ◦ C); data were
taken from Wordclim BIO10.
2.2. Data analyses
For analyses of indicator species, sampling sites were grouped
according to the amount of dead wood and temperature. The combination of the three categories of dead-wood amount and the two
temperature groups yielded six different beech forest types ranging from cool sites with small amounts of dead wood to warm sites
with large amounts of dead wood (Table 1). The number of sites,
and consequently the number of traps, differs among the different
site combinations. This issue will be addressed in Section 4 because
the sampling effort is known to influence the species richness.
We used indicator species analysis (Dufrêne and Legendre,
1997) and extended the method with combinations of site groups
according to De Caceres and Legendre (2009). The original method
considers single associations between species and site groups,
whereas the extended method considers all possible combinations
T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
325
conservation value. As the European Red List for saproxylic beetles is incomplete, we classified the species as follows (Nieto and
Alexander, 2010): priority species were defined as species listed
in the European Red List plus species listed in at least one national
Red List (Schmidl and Buche, 2011; Gärdenfors, 2010), species with
a rarity score of 3–4 in France (Brustel, 2004), or species listed in
Central Europe as Urwald relict species (Müller et al., 2005). Consequently, species red listed in only one country will be considered
in this study as priority species, even though they might be very
common in another European country. All remaining species were
classified as common species (non-priority species).
3. Results
Fig. 1. Computed number (bold figures) of indicator species for forest types with
various combinations of temperature and amount of dead wood. The table in the
bottom center explains the sites groups.
of the site groups (union operation). Two vectors are needed as
input: the species occurrence or abundance data, and a partition of
the sites into a set of k non-overlapping classes (De Caceres et al.,
2010).
We identified indicator species for 14 of the possible 63 combinations (=n6 − 1) (see Fig. 1). The number of combinations was
reduced based on ecologically meaningful combinations. For example, it is meaningless to look for indicator species for a group of sites
combining cool sites with small amounts of dead wood and warm
sites with large amounts of dead wood.
As an association measure, we then used the indicator value
statistic (IndValg). All statistical analyses were performed using
R 2.9.2 (www.r-project.org) with the IndVal package (De Caceres
and Legendre, 2009). To avoid the problem of multiple hypotheses
testing, we derived the final list based on the p-value adjusted for
multiple testing using function p.adjust according to Benjamini and
Hochberg (1995).
Based on national and European Red Lists, we classified our
species as priority and non-priority species to establish their
We considered a total of 483,585 individuals representing 813
species and 69 families of saproxylic beetles in this study. Two
saproxylic subfamilies of the Curculionidae were considered as
families in our computing (Platypodinae and Scolytinae). Using the
conservatively adjusted p-value, 127 indicator species were computed for the 14 selected site combinations, which represented 16%
of the 813 species (see indicator list in Table A1). These indicator
species belong to 42 families of saproxylic beetles. Therefore, over
60% of the collected families comprise indicator species for specific
dead wood amount and climate conditions in beech forests.
Considering the absolute number of indicator species, the
Scolytinae (subfamily of Curculionidae) had the highest number
of indicator species (n = 16), followed by the Staphylinidae (n = 11),
Elateridae (n = 8), Histeridae (n = 7), and Cerambycidae (n = 7). The
ratio between the number of indicator species and the number of
sampled species within a family differed, with the highest ratio
found for Lucanidae (ratio of 0.67), followed by Malachidae, Trogossitidae, Platypodinae (subfamily of Curculionidae), Silvanidae,
and Histeridae (all with a ratio of 0.5). Since large individuals are
usually easier to identify than smaller individuals, we considered
the average body size taken from literature on the species of individuals collected (Lucanidae (16 mm) > Malachidae, Trogossididae,
Platypodinae (5 mm) > Silvanidae (3.5 mm) > Histeridae (1.6 mm).
In general, more indicator species (74 species) were found at
warm sites than at cool sites (28 species) (Fig. 1). Only one site
combination yielded more species at cool sites (13 species) for a
given amount of dead wood than at warm sites (6 species), namely
cool sites with the largest amount of dead wood.
At warm sites, every site combination yielded at least one indicator species, whereas no indicator species were found for cool
sites with small amounts of dead wood. Consequently, the indicator species for cool sites were strictly associated with intermediate
and large amounts of dead wood.
Generally, an increase in the amount of dead wood induced an
increase in the number of indicator species. When temperature
was not considered (Fig. 1, center column, cool and warm sites
pooled) and at cool sites, no indicator species were found at site
combinations without large amounts of dead wood. In contrast, at
site combinations with ≥70 m3 /ha dead wood, 25 (19 + 6) indicator species were associated when temperature was not considered,
and 28 (13 + 15) indicator species were found at cool sites. At the
warm site combinations, the affect of dead-wood amount was not
obvious because most of the indicator species seemed to be affected
more by temperature. Only a few more indicator species occurred
at warm sites rich in dead wood than at warm sites with small
amounts of dead wood, and the highest number of indicator species
(36 species) was even found at a warm site without considering the
amount of dead wood (Fig. 1, right column).
Of the 813 species analyzed, 40.7% were priority species as
defined in Section 2.2; 28.3% of the 127 indicator species were priority species. For only one site (warm and rich in dead wood) was the
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T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
Table 2
Number of priority and non-priority species among the indicator species for different site combinations with at least one indicator species. The figure on the right indicates
the numbering of the site combinations (bold: warm site combinations, non-bold: cool site combinations, see Fig. 1 for code explanations).
Species category
Non-priority species
Priority species
Total species
Proportion of priority species (%)
Group of sites
2
5
6
2+4
3+5
4+6
5+6
2+4+6
3+4+5+6
1
0
1
0
10
3
13
23
0
6
6
100
9
5
14
36
12
3
15
20
11
6
17
35
5
1
6
17
28
8
36
22
15
4
19
21
proportion of priority indicator species higher than the proportion
of all species considered in this study (Table 2).
4. Discussion
4.1. Temperature and dead wood affect the presence of indicator
species
In the European beech forests, we generally found more indicator species living at warm sites than at cool sites (74 vs. 28 species;
Fig. 1). Temperature is known to have a positive effect on species
richness, as described by the species-energy hypothesis, which
indicates that when more energy is available, more biomass and
therefore more species are supported (Wright, 1983) and as shown
by the general pattern of higher diversity at higher temperature
(Gillooly and Allen, 2007). However, higher temperatures are not
compulsorily associated with more indicator species. According to
Menendez et al. (2007), the species richness of habitat specialists
depends on the diversity of the environment and resources available to them. The admixture of oak in approximately half of the
warm stands, a tree species well known to provide various dead
wood structures with increasing age (Buse et al., 2008), can be
considered as an enrichment of the structural biodiversity which
positively influences the diversity of specialized species.
More indicator species were also observed as the amount of dead
wood increased. This was most conspicuous at cool sites and when
cool and warm sites were considered together (Fig. 1). At these combinations of sites, indicator species were observed only with large
amounts of dead wood (≥70 m3 /ha). A large amount of dead wood is
thus compulsory for the conservation of these species. The positive
effect of dead wood on saproxylic species richness and on the number of indicator species has also been observed in mixed stands of
spruce, beech, and fir (Müller et al., 2010). However, a large amount
of dead wood is not the only important factor that ensures the conservation of saproxylic beetles – also the diversity of dead wood in
terms of size and quality is equally important as its volume (Brin
et al., 2009; Ranius and Jonsson, 2007; Siitonen, 2001). For example, both large pieces of dead wood (Brin et al., 2011; Hammond
et al., 2004; Jonsell et al., 1998) as well as small branches (Schiegg,
2001) have been identified as critical habitats for rare or red-listed
beetle species or for saproxylic indicator species. Regarding quality, different diameters, decay stages, tree species, sun exposures,
and the presence of polypores are necessary for a high diversity of
saproxylic beetles (Brin et al., 2011; Brunet and Isacsson, 2009a).
The habitat tradition also seems to play an important role for preserving biodiversity. Brunet and Isacsson (2009b) highlighted the
importance of the continuity of dead wood and old trees for the
conservation of red-listed species, and Buse (2012) showed that
relict saproxylic species are correlated with the continuity of the
forest cover. Long-lasting habitat continuity should therefore also
be considered when setting aside forest reserves.
The effects of temperature and dead-wood amounts should have
direct consequences for the conservation of saproxylic beetles in
beech forests. The results support the view that different strategies
Total number of
indicator species
Total number of
species
91
36
127
28
482
331
813
41
should be adopted for warm and cool forest sites, and must be considered also in strategies mitigating the effects of global warming.
In any case, the amount of dead wood has to be optimized for the
general species richness of saproxylic beetles. However, indicator
species in cool beech forests require a very large amount of dead
wood (≥70 m3 /ha), whereas some indicator species of warm forest
sites are less demanding. Our observations support the findings of
Lassauce et al. (2011), who found a stronger correlation between
saproxylic species and dead-wood amount in cool boreal forests
than in warmer, temperate forests.
4.2. Other influencing factors
As the sampling effort was not equal at the different site combinations analyzed in this study, the results should be considered
carefully in some cases (Table 1). The number of sites included in a
site group combination ranged from 13 to 73, and consequently the
number of traps varied too. However, even though the species number increased with the sampling effort and the number of indicator
species increased with the number of species sampled per site, this
effect would only marginally reduce the difference between cool
and warm sites for two reasons: first, cool and warm sites were
represented by the same number of sites because the threshold
was the median of the warmest monthly temperature of all sites.
Second, although more traps were considered at warm sites than at
cool sites (553 vs. 435 traps), the effect is likely to be minor because
of the high total number of traps. With regard to the amount of dead
wood, the unequal sampling effort would even reduce the difference of the number of indicator species because more traps and
sites were considered in site combinations with small amounts of
dead wood than with large amounts of dead wood.
Several individuals well distributed among sites of a specific
category are required for identifying an indicator species by the
IndVal analysis. Thus, the number of indicator species might be
influenced by the flight activity of insects, which in turn is positively related to temperature. In our study, on average more than
twice as many individuals were collected at warm sites than at
cool sites (682 ± 109 vs. 290 ± 92 individuals). This general pattern of ectotherms (Gillooly et al., 2001) is well reflected by
flight-interception traps, which are known to be activity traps. Consequently, species with low activity and species that are rarely
caught by flight-interception traps will not be selected as indicator
species for a group of sites, even though they may be associated
with one single habitat.
4.3. Broad spectrum of specialized species
The indicator species identified in our study well reflected the
broad range of mixed host trees and the large ecological amplitude of beech forests, which are adapted to conditions ranging
from moist to xerothermic (Müller et al., 2012): 17 species are
associated with conifers, 16 species show a preference for oak,
and 37 species prefer beech. Only four indicator species identified
are strictly associated with beech (Möller, 2009). This supports the
T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
327
Fig. 2. Species list and distribution of the Lucanidae indicator species with regard to dead-wood amount (horizontal axis) and temperature (vertical axis). *p-Value as indicator
<0.1.
Pictures: ©U. Schmidt.
results of Brändle and Brandl (2001), who found a limited number of phytophagous species in Germany associated with beech (44
species) compared to the number associated with oak (252 species)
or spruce (75 species). Southwood (1961) has suggested that the
number of insect species associated with a tree is a reflection of
the cumulative abundance of that tree species throughout recent
geological history. The expansion of beech in Europe is relatively
recent as it started to colonize the lowland only after 4000 years
BP reaching its maximum extension some 1000 years ago (Magri
et al., 2006), which might explain the low number of beech specialists. However, the processes shaping the specialist/generalist ratio
on a host plant are far from clear (Brändle and Brandl, 2001; Lawton
and Schroder, 1977).
4.4. Conservation value of indicator species
Our indicator species list permits us to highlight the importance
of different beech forest types for biodiversity. This is of prime
concern because the homogenization of anthropogenically influenced ecosystems, which is defined as the process whereby species
assemblages become increasingly dominated by a small number
of widespread species, is one of the main threats to biodiversity
(Millennium Ecosystem Assessment, 2005). Therefore, forest areas
that have been set aside should not be optimized only for their
species number, but should also include as many indicator species
as possible. The indicator species identified in this study should
consequently be used to determine conservation areas of high ecological value.
Indicator species are known to have a more limited distribution range in habitats under study (here beech-dominated forests)
and are more vulnerable to disturbances than generalists (Schouten
et al., 2010). However, in our study, the percentage of priority
species relative to the total species number was lower among
the indicator species than among the total number of sampled
saproxylic beetles species (28 vs. 42% priority species, Table 2).
This result may be biased by the analysis method (IndVal) because
rare and threatened species occurring at only a few sites with
few individuals will hardly be retained as indicator species. Only
the combination of warm sites and sites with high amount of
dead wood showed a higher percentage of priority species than
the total number of beetles. With these site combinations, all
of the six indicator species are considered as priority species
(Tables 2 and A1). A comparison of both temperature categories
confirmed that warm sites have a higher conservation value than
cool sites – forests with a warm climate harbor the highest number of indicator species and 25 priority species were identified at
warm sites, whereas six priority species were identified at cool sites
(Table 2).
4.5. Most suitable indicator family
The percentage of indicator species within a family gives information about the reliability of a single beetle family as an indicator.
The stag beetles (Lucanidae) had the highest percentage of indicator
species; 4 of 6 species (67%) were identified as indicator species at
p < 0.05 and one at p < 0.10. Stag beetles are suitable indicators from
the applied perspective as they can be easily identified in the field
because of their size (average body size = 16 mm), except Platycerus caprea and Platycerus caraboides. The observed differences in
habitat requirements of all lucanid indicator species in terms of
site combinations (Fig. 2) underlines their suitability as indicator
group in nature conservation. Platycerus caraboides was not sensitive to the amount of dead wood, but was an indicator for sites
with high temperatures. This corresponds well to the broad distribution of this species at warm sites below 500 m a.s.l. (Brechtel
and Kostenbader, 2002). In contrast, P. caprea was associated with
cooler sites which is in line with the described preference for higher
altitude (Klausnitzer, 1995). Similarly to P. caprea, Dorcus parallelipipedus was associated with a larger amount of dead wood, but
this thermophilous species is restricted to warm sites at lower altitudes (Brechtel and Kostenbader, 2002), which is also supported by
results of a local study in Sweden (Brunet and Isacsson, 2010). The
indicator for intermediate and high dead wood amount, Sinodendron cylindricum was indifferent to temperature which supports
the observed broad climatic range of S. cylindricum at altitudes
of 100–1200 m a.s.l. (Brechtel and Kostenbader, 2002). Ceruchus
chrysomelinus can be considered as an indicator for large amounts
of dead wood at both warm and cool sites. Nilsson et al. (2000)
proposed this species already as an indicator for forests with high
conservation value in Sweden owed to its dependence on long
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T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
continuity of dead wood in the forests. This might explain the overall low abundance of this species in our catches.
It is noteworthy that few long-horned beetles (Cerambycidae)
were identified as indicator species (Table A1) even though this
group is predominant in many ecological studies in forests and also
appears in the European Red List (Nieto and Alexander, 2010). This
family is a well-known group relatively easy to identify (average
body size = 12.6 mm) and thus would be well suited to serve as an
indicator family. In our study, these beetles were characteristic of
intermediate to large amounts of dead wood in both warm and
cool forests, but only 7 of 61 collected species were identified as
indicator species for our beech forests. One explanation may be the
lack of inflorescences in many beech forests as many adult longhorned beetles feed on pollen and nectar (Bense, 1995).
When the absolute number of indicator species is considered,
the Staphylinidae (11 indicator species) and the Scolytinae (16
indicator species) had the highest number of indicator species per
family or subfamily respectively. However, the percentage of indicator species within these groups is low, which means that most
sampled individuals would not be listed as indicator species. Furthermore, these families need to be identified by specialists in
the laboratory, inter alia because of their small average body size
(Scolytinae: 2.3 mm; Staphylinidae: 5.2 mm), which does not facilitate their use.
It seemed peculiar to find the notorious spruce pest Ips typographus as an indicator species for cool beech forests with large
amounts of dead wood. Although all studied stands were dominated by beech, an important proportion of dead wood at these
sites might be the result of bark beetle outbreaks on spruce,
but tree species specific dead wood data was not available. On
average, the sites of this combination were situated at approximately 730 ± 60 m a.s.l. (66 m a.s.l. in Sweden to 1241 m a.s.l. in
Germany), which coincides well with the location of mixed beechspruce forests. Scolytine species can not only be considered as pest
species, but also as ecosystem engineers driving forest regeneration
by producing snags, opening gaps, and promoting a rich patchiness in forest canopies (Jonasova and Prach, 2004; Martikainen
et al., 1999; Müller et al., 2008a) or as important pioneers in the
decomposition of dead wood. For example, the arthropod complex associated with I. typographus includes more than 140 species
(Weslien, 1992). Ips typographus therefore fulfills the majority of
criteria for a keystone species by maintaining forest biodiversity
(Müller et al., 2008a).
5. Conclusions
Our study provides a list of indicator species for cool and warm
European beech forests with different amounts of dead wood and
for some combinations of these two factors. This is a first step
toward a statistics-based list of indicator species as a baseline for
conservation activities in selecting priority sites and improving
monitoring. Temperature and the amount of dead wood influence
the number of indicator species identified by the Indval method
and the proportion of priority species. To ensure the conservation
of saproxylic beetle species, the protection of cool beech forests
should concentrate on stands with large amounts of dead wood.
In warm beech forests, the amount of dead wood seems to be less
crucial than in cool beech forests.
Acknowledgments
We thank W.W. Weisser, M. Fischer, E.-D. Schulze, and D. Hessenmöller for providing the data from the three regions, gathered
in the DFG Priority Program 1374 “Infrastructure-BiodiversityExploratories”. We thank U. Bense, T. Blick & W. Dorow (Senckenberg Forschungsinstitut und Naturmuseum Frankfurt/Main),
U. Schulte (Landesbetrieb Wald und Holz Nordrhein-Westfalen),
U. Gehlhar (Landesforst Mecklenburg-Vorpommern), and P. Balcar (Forschungsanstalt für Waldökologie und Forstwirtschaft,
Rheinland-Pfalz) for data from federal projects; K. Vanderkerkhove
(Instituut voor Natuur- en Bosonderzoek Brussel) and D. Murat
for data from Belgium and Luxemburg; F. Köhler for providing
data from several projects in nature forest reserves in Belgium,
Germany and Luxemburg in collaboration with Administration des
Eaux et Forêts Luxembourg (D. Murat); M.K. Obrist and K. SchieggPasinelli (Swiss Federal Institute for Forest, Snow and Landscape
Research WSL) for data from Switzerland; and V. Chumak (Uzhgorod National University) for data from Ukraine. The study was
financially supported by the German Federal Agency for Nature
Conservation.
Appendix A.
Table A1
List of the 127 indicator species of saproxylic beetles, with their indicator value (IndVal), the adjusted p-value (De Caceres and Legendre, 2009), the site groups for which
they are characteristic (cf. Fig. 1 for code explanations), and their priority level as defined in Section 2.2.
Species
Family/subfamily
IndVal
Adjusted p
Group of sites
Priority level
Allecula morio
Allecula rhenana
Mycetochara linearis
Pseudocistela ceramboides
Anobium emarginatum
Dorcatoma dresdensis
Dorcatoma robusta
Dryophilus pusillus
Anthribus albinus
Malthinus punctatus
Malthodes alpicola
Malthodes fuscus
Malthodes hexacanthus
Malthodes mysticus
Anoplodera sexguttata
Leiopus nebulosus
Leptura quadrifasciata
Pachytodes cerambyciformis
Alleculidae
Alleculidae
Alleculidae
Alleculidae
Anobiidae
Anobiidae
Anobiidae
Anobiidae
Anthribidae
Cantharidae
Cantharidae
Cantharidae
Cantharidae
Cantharidae
Cerambycidae
Cerambycidae
Cerambycidae
Cerambycidae
0.449
0.368
0.584
0.384
0.435
0.512
0.477
0.484
0.558
0.530
0.402
0.426
0.407
0.372
0.407
0.459
0.462
0.419
0.015
0.044
0.005
0.044
0.014
0.005
0.026
0.003
0.020
0.015
0.016
0.012
0.027
0.045
0.010
0.040
0.014
0.047
4+6
4+6
2+4+6
4+6
3+5
4+6
4+6
5
2+4+6
2+4+6
3+5
5
3+5
5
6
5+6
2+4
5+6
Priority
Priority
Common
Priority
Common
Common
Priority
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Common
Common
T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
329
Table A1 (Continued)
Species
Family/subfamily
IndVal
Adjusted p
Group of sites
Priority level
Plagionotus arcuatus
Rhagium bifasciatum
Rhagium mordax
Cis castaneus
Cis jacquemartii
Cis nitidus
Thanasimus formicarius
Bitoma crenata
Cicones variegatus
Synchita humeralis
Orthoperus mundus
Cryptophagus micaceus
Pediacus depressus
Acalles dubius
Dryophthorus corticalis
Megatoma undata
Ampedus erythrogonus
Ampedus nigrinus
Ampedus pomorum
Anostirus castaneus
Denticollis rubens
Diacanthous undulatus
Hypoganus inunctus
Melanotus rufipes
Mycetina cruciata
Dacne bipustulata
Hylis cariniceps
Hylis olexai
Melasis buprestoides
Abraeus granulum
Abraeus perpusillus
Aeletes atomarius
Dendrophilus punctatus
Paromalus flavicornis
Paromalus parallelepipedus
Plegaderus dissectus
Placonotus testaceus
Corticaria abietorum
Corticarina lambiana
Latridius hirtus
Stephostethus rugicollis
Dorcus parallelipipedus
Platycerus caprea
Platycerus caraboides
Sinodendron cylindricum
Platycis minutus
Hylecoetus dermestoides
Malachius bipustulatus
Phloiotrya rufipes
Serropalpus barbatus
Dasytes plumbeus
Rhizophagus grandis
Tomoxia bucephala
Litargus connexus
Mycetophagus atomarius
Mycetophagus multipunctatus
Mycetophagus piceus
Mycetophagus quadripustulatus
Cryptarcha strigata
Cryptarcha undata
Cychramus luteus
Cychramus variegatus
Epuraea binotata
Epuraea variegata
Calopus serraticornis
Platypus cylindrus
Bibloporus minutus
Salpingus planirostris
Vincenzellus ruficollis
Cetonia aurata
Valgus hemipterus
Cyclorhipidion bodoanus
Ernoporicus fagi
Hylastes cunicularius
Cerambycidae
Cerambycidae
Cerambycidae
Cisidae
Cisidae
Cisidae
Cleridae
Colydiidae
Colydiidae
Colydiidae
Corylophidae
Cryptophagidae
Cucujidae
Curculionidae
Curculionidae
Dermestidae
Elateridae
Elateridae
Elateridae
Elateridae
Elateridae
Elateridae
Elateridae
Elateridae
Endomychidae
Erotylidae
Eucnemidae
Eucnemidae
Eucnemidae
Histeridae
Histeridae
Histeridae
Histeridae
Histeridae
Histeridae
Histeridae
Laemophloeidae
Latridiidae
Latridiidae
Latridiidae
Latridiidae
Lucanidae
Lucanidae
Lucanidae
Lucanidae
Lycidae
Lymexylidae
Malachiidae
Melandryidae
Melandryidae
Melyridae
Monotomidae
Mordellidae
Mycetophagidae
Mycetophagidae
Mycetophagidae
Mycetophagidae
Mycetophagidae
Nitidulidae
Nitidulidae
Nitidulidae
Nitidulidae
Nitidulidae
Nitidulidae
Oedemeridae
Platypodinae
Pselaphidae
Salpingidae
Salpingidae
Scarabaeidae
Scarabaeidae
Scolytinae
Scolytinae
Scolytinae
0.353
0.578
0.714
0.516
0.415
0.554
0.498
0.522
0.600
0.481
0.509
0.389
0.517
0.375
0.352
0.506
0.505
0.519
0.673
0.530
0.590
0.378
0.417
0.718
0.510
0.596
0.504
0.582
0.684
0.376
0.580
0.399
0.444
0.611
0.496
0.599
0.443
0.511
0.517
0.549
0.525
0.464
0.463
0.507
0.587
0.396
0.723
0.443
0.416
0.343
0.535
0.408
0.654
0.791
0.615
0.443
0.487
0.601
0.509
0.494
0.619
0.574
0.373
0.487
0.361
0.433
0.474
0.709
0.650
0.423
0.398
0.553
0.699
0.569
0.043
0.003
0.011
0.045
0.013
0.047
0.047
0.006
0.003
0.015
0.049
0.042
0.006
0.046
0.037
0.007
0.006
0.003
0.003
0.003
0.006
0.016
0.044
0.003
0.003
0.003
0.006
0.012
0.003
0.040
0.003
0.044
0.022
0.003
0.011
0.005
0.036
0.005
0.003
0.034
0.006
0.016
0.022
0.042
0.035
0.035
0.027
0.030
0.029
0.049
0.037
0.010
0.003
0.003
0.003
0.035
0.014
0.003
0.035
0.034
0.029
0.035
0.027
0.044
0.034
0.034
0.029
0.046
0.007
0.035
0.045
0.003
0.044
0.010
6
3+5
3+4+5+6
2+4+6
3+5
3+4+5+6
2+4+6
4+6
2+4+6
2+4
2+4+6
2+4
2+4
2
6
2+4+6
3+4+5+6
3+5
2+4+6
6
5+6
6
2+4+6
2+4+6
5+6
2+4+6
2+4+6
2+4+6
2+4+6
6
4+6
2+4
2+4
2+4+6
2+4+6
2+4+6
4+6
3+5
3+5
3+4+5+6
3+5
4+6
3+5
2+4+6
3+4+5+6
5+6
3+4+5+6
4+6
3+4+5+6
5
3+4+5+6
5
2+4+6
2+4+6
3+4+5+6
4+6
2+4
2+4+6
2+4
2+4
5+6
3+5
5
3+4+5+6
5
2+4+6
2+4
2+4+6
2+4+6
2+4+6
2+4+6
4+6
3+4+5+6
3+5
Priority
Common
Common
Priority
Priority
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Priority
Common
Priority
Priority
Common
Priority
Priority
Priority
Priority
Common
Common
Common
Priority
Priority
Common
Priority
Common
Priority
Priority
Common
Common
Priority
Common
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Common
Common
Priority
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Common
Common
Common
Priority
Common
Common
Priority
Priority
Common
Common
Priority
Common
Common
Common
Common
Common
330
T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
Table A1 (Continued)
Species
Family/subfamily
IndVal
Adjusted p
Group of sites
Priority level
Hylurgops palliatus
Ips typographus
Pityophthorus pityographus
Polygraphus poligraphus
Scolytus intricatus
Taphrorychus bicolor
Trypodendron lineatum
Xyleborus monographus
Xyleborus saxeseni
Xylechinus pilosus
Xylosandrus germanus
Xyloterus domesticus
Xyloterus laevae
Anaspis flava
Anaspis frontalis
Anaspis maculata
Anaspis thoracica
Stenichnus godarti
Silvanus unidentatus
Uleiota planata
Atrecus pilicornis
Hapalaraea pygmaea
Hypnogyra glabra
Phloeopora corticalis
Phyllodrepa linearis
Quedius plagiatus
Scaphisoma agaricinum
Siagonium quadricorne
Thamiaraea hospita
Velleius dilatatus
Xylostiba monilicornis
Bolitophagus reticulatus
Corticeus unicolor
Uloma culinaris
Nemosoma elongatum
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scolytinae
Scraptiidae
Scraptiidae
Scraptiidae
Scraptiidae
Scydmaenidae
Silvanidae
Silvanidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Staphylinidae
Tenebrionidae
Tenebrionidae
Tenebrionidae
Trogossitidae
0.530
0.513
0.579
0.506
0.521
0.770
0.616
0.581
0.737
0.444
0.731
0.727
0.333
0.449
0.545
0.401
0.458
0.492
0.460
0.503
0.549
0.457
0.411
0.553
0.333
0.561
0.626
0.392
0.464
0.510
0.333
0.552
0.621
0.387
0.590
0.015
0.003
0.003
0.003
0.035
0.016
0.003
0.003
0.003
0.006
0.003
0.003
0.044
0.040
0.003
0.034
0.044
0.016
0.010
0.007
0.003
0.039
0.041
0.035
0.044
0.003
0.005
0.036
0.040
0.014
0.049
0.013
0.011
0.035
0.034
3+4+5+6
5
3+5
3+5
4+6
3+4+5+6
3+4+5+6
2+4+6
2+4+6
5
2+4+6
3+4+5+6
5
2+4+6
3+4+5+6
2+4
3+4+5+6
4+6
4+6
2+4+6
5
4+6
2+4+6
2+4+6
5
3+5
2+4
2+4
2+4
2+4+6
5
3+4+5+6
2+4+6
4+6
3+4+5+6
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Priority
Common
Common
Priority
Common
Common
Common
Common
Common
Priority
Common
Common
Common
Common
Common
Common
Common
Common
Common
Priority
Common
Common
Priority
Common
Priority
Common
References
Benjamini, Y., Hochberg, Y., 1995. Controlling the false discovery rate – a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B: Method. 57,
289–300.
Bense, U., 1995. Longhorn Beetles Illustrated key to the Cerambycidae and Vesperidae of Europe. Markgraf Verlag, Germany.
Brändle, M., Brandl, R., 2001. Species richness of insects and mites on trees: expanding Southwood. J. Anim. Ecol. 70, 491–504.
Brechtel, F., Kostenbader, H. (Eds.), 2002. Die Prach- und Hirchkäfer BadenWürtenbergs. Verlag E. Ulmer, Stuttgart.
Brin, A., Bouget, C., Brustel, H., Jactel, H., 2011. Diameter of downed woody debris
does matter for saproxylic beetle assemblages in temperate oak and pine forests.
J. Insect Conserv. 15, 653–669.
Brin, A., Brustel, H., Jactel, H., 2009. Species variables or environmental variables
as indicators of forest biodiversity: a case study using saproxylic beetles in
Maritime pine plantations. Ann. Forest Sci. 66.
Brunet, J., Fritz, Ö., Richnau, G., 2010. Biodiversity in European beech forests – a
review with recommendations for sustainable forest management. Ecol. Bull.
53, 77–94.
Brunet, J., Isacsson, G., 2009a. Influence of snag characteristics on saproxylic
beetle assemblages in a south Swedish beech forest. J. Insect Conserv. 13,
515–528.
Brunet, J., Isacsson, G., 2009b. Restoration of beech forest for saproxylic beetles –
effects of habitat fragmentation and substrate density on species diversity and
distribution. Biodivers. Conserv. 18, 2387–2404.
Brunet, J., Isacsson, G., 2010. A comparison of the saproxylic beetle fauna between
lowland and upland beech forests in southern Sweden. Ecol. Bull. 53, 131–139.
Brustel, P.H., 2004. Coléoptères saproxyliques et valeur biologique des forêts francaises, vol. 13.
Schmidl, J., Büche, B.,;1; 2011. Die Rote Liste der Käfer Deutschlands. Rote Liste
gefährdeter Tiere, Pflanzen und Pilze Deutschlands Band 4. Bundesamt für
Naturschutz, Bad Godesberg, Germany.
Buse, J., 2012. “Ghosts of the past”: flightless saproxylic weevils (Coleoptera: Curculionidae) are relict species in ancient woodlands. J. Insect Conserv. 16, 93–102.
Buse, J., Ranius, T., Assmann, T., 2008. An endangered longhorn beetle associated
with old oaks and its possible role as an ecosystem engineer. Conserv. Biol. 22,
329–337.
Carignan, V., Villard, M.A., 2002. Selecting indicator species to monitor ecological
integrity: a review. Environ. Monit. Assess. 78, 45–61.
Christensen, M., Hahn, K., Mountford, E.P., Odor, P., Standovar, T., Rozenbergar,
D., Diaci, J., Wijdeven, S., Meyer, P., Winter, S., Vrska, T., 2005. Dead wood
in European beech (Fagus sylvatica) forest reserves. Forest Ecol. Manag. 210,
267–282.
Cousins, S.H., 1991. Species-diversity measurement – choosing the right index.
Trends Ecol. Evol. 6, 190–192.
De Caceres, M., Legendre, P., 2009. Associations between species and groups of sites:
indices and statistical inference. Ecology 90, 3566–3574.
De Caceres, M., Legendre, P., Moretti, M., 2010. Improving indicator species analysis
by combining groups of sites. Oikos 119, 1674–1684.
Dufrêne, M., Legendre, P., 1997. Species assemblages and indicator species: the need
for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366.
Dunn, C., 1994. Gaps in GAP. Plant Sci. Bull. 40, 120–121.
Fahrig, L., 2001. How much habitat is enough? Biol. Conserv. 100, 65–74.
Gärdenfors, U., 2010. Rödlistade arter i Sverige 2010. ArtDatabanken, Uppsala.
Gillooly, J.F., Allen, A.P., 2007. Linking global patterns in biodiversity to evolutionary
dynamics using metabolic theory. Ecology 88, 1890–1894.
Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M., Charnov, E.L., 2001. Effects of size
and temperature on metabolic rate. Science 293, 2248–2251.
Hammond, H.E.J., Langor, D.W., Spence, J.R., 2004. Saproxylic beetles (Coleoptera)
using Populus in boreal aspen stands of western Canada: spatiotemporal variation and conservation of assemblages. Can. J. Forest Res. 34, 1–19.
Jonasova, M., Prach, K., 2004. Central-European mountain spruce (Picea abies (L.)
Karst.) forests: regeneration of tree species after a bark beetle outbreak. Ecol.
Eng. 23, 15–27.
Jonsell, M., 2007. Effects on biodiversity of forest fuel extraction, governed by processes working on a large scale. Biomass Bioenergy 31, 726–732.
Jonsell, M., Weslien, J., Ehnstrom, B., 1998. Substrate requirements of red-listed
saproxylic invertebrates in Sweden. Biodivers. Conserv. 7, 749–764.
Juutinen, A., Monkkonen, M., 2004. Testing alternative indicators for biodiversity
conservation in old-growth boreal forests: ecology and economics. Ecol. Econ.
50, 35–48.
Klausnitzer, B., 1995. Die Hirschkäfer. Spektrum Akad. Verl., Heidelberg.
Lassauce, A., Paillet, Y., Jactel, H., Bouget, C., 2011. Deadwood as a surrogate for
forest biodiversity: meta-analysis of correlations between deadwood volume
and species richness of saproxylic organisms. Ecol. Indic. 11, 1027–1039.
Lawton, J.H., Schroder, D., 1977. Effects of plant type, size of geographical range and
taxonomic isolation on number of insect species associated with British plants.
Nature 265, 137–140.
Magri, D., Vendramin, G.G., Comps, B., Dupanloup, I., Geburek, T., Gomory, D., Latalowa, M., Litt, T., Paule, L., Roure, J.M., Tantau, I., van der Knaap, W.O., Petit, R.J.,
de Beaulieu, J.L., 2006. A new scenario for the Quaternary history of European
beech populations: palaeobotanical evidence and genetic consequences. New
Phytol. 171, 199–221.
T. Lachat et al. / Ecological Indicators 23 (2012) 323–331
Margules, C.R., Lindenmayer, D.B., 1996. Landscape level concepts and indicators
for the conservation of forest biodiversity and sustainable forest management.
In: UBC-UPM Conference on the Ecological, Social and Political Issues of the
Certification of Forest Management, pp. 65–83.
Martikainen, P., Siitonen, J., Kaila, L., Punttila, P., Rauh, J., 1999. Bark beetles
(Coleoptera, Scolytidae) and associated beetle species in mature managed and
old-growth boreal forests in southern Finland. Forest Ecol. Manag. 116, 233–245.
McGeoch, M.A., 1998. The selection, testing and application of terrestrial insects as
bioindicators. Biol. Rev. 73, 181–201.
Menendez, R., Gonzalez-Megias, A., Collingham, Y., Fox, R., Roy, D.B., Ohlemuller, R.,
Thomas, C.D., 2007. Direct and indirect effects of climate and habitat factors on
butterfly diversity. Ecology 88, 605–611.
Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-being: Biodiversity Synthesis. World Resources Institute, Washington, DC.
Möller, G., 2009. Struktur- und Substratbindung holzbewohnender Insekten, Schwerpunkt Coleoptera – Käfer. Freie Universität, Berlin.
Müller, J., Brunet, J., Brin, A., Bouget, C., Brustel, H., Bussler, H., Förster, B., Isacsson, G.,
Köhler, F., Lachat, T., Gossner, M.M., 2012. Implications from large-scale spatial
diversity patterns of saproxylic beetles for the conservation of European Beech
forests. Insect Conserv. Divers., Online.
Müller, J., Bussler, H., Bense, U., Brustel, H., Flechtner, G., Fowles, A., Kahlen,
M., Möller, G., Mühle, H., Schmidl, J., Zabransky, P., 2005. Urwald relict
species–Saproxylic beetles indicating structural qualities and habitat tradition.
Waldökologie 2, 106–113, Online.
Müller, J., Bussler, H., Gossner, M., Rettelbach, T., Duelli, P., 2008a. The European
spruce bark beetle Ips typographus in a national park: from pest to keystone
species. Biodivers. Conserv. 17, 2979–3001.
Müller, J., Bussler, H., Kneib, T., 2008b. Saproxylic beetle assemblages related to
silvicultural management intensity and stand structures in a beech forest in
Southern Germany. Eur. J. Insect Conserv. 12, 107–124.
Müller, J., Bütler, R., 2010. A review of habitat thresholds for dead wood: a baseline
for management recommendations in European forests. Eur. J. Forest Res. 129,
981–992.
Müller, J., Noss, R.F., Bussler, H., Brandl, R., 2010. Learning from a benign neglect
strategy in a national park: response of saproxylic beetles to dead wood accumulation. Biol. Conserv. 143, 2559–2569.
Nieto, A., Alexander, K.N.A., 2010. European Red List of saproxylic beetles. Publications of the European Union, Luxembourg.
Nilsson, S., Baranowski, R., Ehnströhm, B., Eriksson, P., Hedin, J., 2000. Ceruchus
chrysomelinus (Coleoptera, Lucanidae), a disappearing virgin forest relict
species? Entomol. Tidskr. 121, 137–146.
331
Odor, P., Heilmann-Clausen, J., Christensen, M., Aude, E., van Dort, K.W., Piltaver, A.,
Siller, I., Veerkamp, M.T., Walleyn, R., Standovar, T., van Hees, A.F.M., Kosec, J.,
Matocec, N., Kraigher, H., Grebenc, T., 2006. Diversity of dead wood inhabiting
fungi and bryophytes in semi-natural beech forests in Europe. Biol. Conserv. 131,
58–71.
Peterken, G.F., 1996. Natural Woodland. Ecology and Conservation in Northern Temperate Regions. Cambridge University Press, Cambridge.
Prendergast, J.R., Quinn, R.M., Lawton, J.H., Eversham, B.C., Gibbons, D.W., 1993.
Rare species, the coincidence of diversity hotspots and conservation strategies.
Nature 365, 335–337.
Ranius, T., Jonsson, M., 2007. Theoretical expectations for thresholds in the relationship between number of wood-living species and amount of coarse woody
debris: a study case in spruce forests. J. Nat. Conserv. 15, 120–130.
Rondinini, C., Chiozza, F., 2010. Quantitative methods for defining percentage
area targets for habitat types in conservation planning. Biol. Conserv. 143,
1646–1653.
Rose, F., 1992. Temperate forest management, its effect on bryophyte and lichen
floras and habitats. In: Bates, J.W., Farmer, A.M. (Eds.), Bryophytes and Lichens
in a Changing Environment. Clarenden Press, Oxford, pp. 223–245.
Schiegg, K., 2001. Saproxylic insect diversity of beech: limbs are richer than trunks.
Forest Ecol. Manag. 149, 295–304.
Schouten, M.A., Barendregt, A., Verweij, P.A., Kalkman, V.J., Kleukers, R.M.J.C.,
Lenders, H.J.R., Siebel, H.N., 2010. Defining hotspots of characteristic species
for multiple taxonomic groups in the Netherlands. Biodivers. Conserv. 19,
2517–2536.
Siitonen, J., 2001. Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forests as an example. Ecol. Bull. 49, 11–41.
Southwood, T.R.E., 1961. The number of species of insect associated with various
trees. J. Anim. Ecol. 30, 1–8.
Webb, N.R., 1989. Studies on the invertebrate fauna of fragmented heathland
in Dorset, UK, and the implications for conservation. Biol. Conserv. 47,
153–165.
Weslien, J., 1992. The arthropod complex associated with Ips-Typographus (L)
(Coleoptera, Scolytidae), species composition, phenology, and impact on bark
beetle productivity. Entomol. Fenn. 3, 205–213.
Winter, S., Flade, M., Schumacher, H., Kerstan, E., Möller, G., 2005. The importance of
near natural stand structures for the biocoenosis of lowland beech forests. For.
Snow Lansc. Res. 79, 127–144.
Wright, D.H., 1983. Species-energy theory – an extension of species-area theory.
Oikos 41, 496–506.