Forest Ecology and Management 449 (2019) 117462

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Ecologically similar saproxylic beetles depend on diversified deadwood T

resources: From habitat requirements to management implications
Tomasz Jaworskia, , Radosław Plewaa, Grzegorz Tarwackia, Krzysztof Sućkob,
⁎

Jacek Hilszczańskia, Jakub Horákc

a
Department of Forest Protection, Forest Research Institute, Sękocin Stary, Braci Leśnej 3, 05-090 Raszyn, Poland
b
Department of Natural Forests, Forest Research Institute, Białowieża, Park Dyrekcyjny 6, 17-230 Białowieża, Poland
c
Department of Forest Protection and Entomology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcká 1176, 165 00 Prague, Czech
Republic

ARTICLE INFO ABSTRACT

Keywords: Organisms dependent on dead wood (i.e., saproxylic) are some of the most threatened by changes in the forest
Białowieża Forest environment. Aside from anthropogenic disturbances resulting in forest fragmentation and a decrease in dead wood,
Boros schneideri the expansion of homogenous closed-canopy forests due to successional changes is identified as the main threat for
Cucujus cinnaberinus many saproxylic organisms. It is especially important in major conservation areas in Europe. Thus, studies combining
Cucujus haematodes
knowledge about the habitat requirements of saproxylic species with the impacts of different types of forest man-
Traditional forest management
agement on populations of these organisms are essential to identify effective conservation strategies.
Under-bark guild
In this study, we focused on three threatened saproxylic beetles with similar ecology, i.e., Cucujus cinnaber-
inus, C. haematodes and Boros schneideri, in a close-to-natural forest. The study was conducted in the stronghold
of these species in temperate Europe, the Białowieża Forest in Poland, based on a field survey of more than
11,000 dead wood pieces. We investigated the habitat requirements of these species and their relationships with
the environment at the tree and landscape levels. We further analysed the distribution of these beetles in forests
under various levels of management intensity. Based on the results of the present study and published data on
compositional changes in the forests in the study area, we attempt to formulate implications related to the
conservation of the studied beetles.
Cucujus cinnaberinus was the most widespread and frequent species, with a preference for high-diameter dead
aspens in managed forests with high dead wood amounts. The second most abundant species, C. haematodes,
preferred downed ashes and alders with rather fragmented bark. Its distribution was spatially aggregated in un-
managed forests. The rarest beetle in this study, B. schneideri, was associated with forests with large dead pines.
Our results confirm the importance of the Białowieża Forest for the three threatened saproxylic beetles. The
study also revealed the highly diversified demands of these beetles, which may not be met in the future if the
abundance of the preferred habitat tree species is declining. We recommend a conservation strategy that
combines non-intervention towards naturally developed deadwood with monitoring of tree recruitment and if
necessary, measures to assure recruitment of particular tree species, e.g., pine and aspen. Future studies should
investigate the role of natural disturbances for recruitment of these tree species and thus, the long-term per-
sistence of associated saproxylic beetle species.

1. Introduction
Dead wood offers a large supply of habitats for its associates, which
are known as saproxylics (Speight, 1989). One of the most diverse
groups of saproxylic organisms is insects; in northern and central
Europe, saproxylic species constitute 20–30% of all forest insects
(Stockland and Siitonen, 2012; Ulyshen and Šobotník, 2018). Many
saproxylic insects have become threatened with extinction, mainly as a
result of forest fragmentation and a decrease in the amount of dead
wood (e.g., Nieto and Alexander, 2010; Eckelt et al., 2018). Conse-
quently, the necessity for the strict protection of the last remnants of
primeval forests for the conservation of dead wood-dependent insects

Corresponding author.
⁎

E-mail addresses: t.jaworski@ibles.waw.pl (T. Jaworski), r.plewa@ibles.waw.pl (R. Plewa), g.tarwacki@ibles.waw.pl (G. Tarwacki),
k.sucko@ibles.waw.pl (K. Sućko), j.hilszczanski@ibles.waw.pl (J. Hilszczański), jakub.sruby@seznam.cz (J. Horák).

https://doi.org/10.1016/j.foreco.2019.117462
Received 14 January 2019; Received in revised form 4 July 2019; Accepted 5 July 2019
Available online 10 July 2019
0378-1127/ © 2019 Elsevier B.V. All rights reserved.
T. Jaworski, et al.
has been emphasized (e.g., Lachat and Müller, 2018). At the same time,
many studies have shown that sun-exposed dead trees provide preferred
habitat for many saproxylic insects, including rare species (e.g.,
Blažytė-Čereškienė and Karalius, 2011; Goczał and Rossa, 2017; Kašák
and Foit, 2018). Thus, the hands-off approach that is commonly applied
to reserves and national parks may have a detrimental effect on sa-
proxylic insects if natural disturbances that would create open and early
successional habitats are absent (Sebek et al., 2015). Furthermore,
several studies have indicated the benefits that this group derives from
moderate forest management and other activities related to forest use,
e.g., pasturing, prescribed fires, and coppicing, which are largely due to
an increase in sun exposure and the heterogeneity of habitats in forests
(Horák et al., 2012, 2018; Bernes et al., 2015; Vandekerkhove et al.,
2016; Miklín et al., 2018).
The successful conservation of saproxylic insects requires knowl-
edge regarding their ecological demands. The number of studies on the
habitat requirements of threatened species in temperate Europe has
increased significantly in recent decades. Authors have focused mainly
on single species (e.g., Horák et al., 2010, 2012; Gutowski et al., 2014b;
Goczał and Rossa, 2017; but see, e.g., Seibold et al., 2015a). Thus, the
potential of the management-related implications derived from these
studies for the conservation of wide array of saproxylic taxa may be
limited. Furthermore, past studies were often conducted in secondary
managed forests, where the observations might have been distorted by
human-driven changes that have taken place in these forests. However,
it should be expected that forests under various management options
(i.e., managed, traditionally managed, unmanaged) also differ in terms
of their value for particular saproxylic insect species. Unfortunately,
studies aimed at identifying the impacts of different management ap-
proaches on rare saproxylic insects are rather scarce (Müller et al.,
2008a).
Our study focused on three specialist saproxylic beetles, Cucujus
cinnaberinus (Scopoli, 1763), Cucujus haematodes (Erichson, 1845) and
Boros schneideri (Panzer, 1796). These species are characterized by re-
latively similar ecology. Namely, their larvae live in the subcortical
space of dead wood. These beetle species are currently threatened with
extinction; therefore, their conservation is of interest to many European
countries (Cálix et al., 2018). They are also considered to be species of
high conservation value because they share habitats with many other
saproxylic organisms and can thus be regarded as umbrella or indicator
species (e.g., Mazzei et al., 2011). Our study was carried out in one of
the last old-growth forests in central Europe, i.e., the Białowieża Forest,
which is the stronghold of these three beetle species.
Our main scientific question was what are the true habitat re-
quirements of C. cinnaberinus, C. haematodes and B. schneideri within the
spatially and temporally continuous Białowieża Forest, where the three
species co-occur. We further aimed to reveal the mechanisms under-
lying the present distribution of these beetles in the study area. Namely,
we explained their occurrence and abundance on the basis of the dis-
tribution of the preferred dead wood resources and potential influence
of management intensity. Based on the habitat requirements of the
study species and published data on the structural changes observed in
the forest within the study area, we attempted to formulate implications
related to conservation-oriented forest management.
2. Materials and methods
2.1. Study area
The study was conducted in the Polish part of the Białowieża Forest
(ca. 630 km2). The area (Fig. 1) consists of the Białowieża National Park
(105 km2) and the forests administered by the Polish State Forests
(525 km2). The Białowieża National Park (hereafter BNP) encompasses
two protective units, Orłówka and Hwoźna. The former unit (hereafter
strict reserve) has been excluded from management since 1921, and the
latter unit consists of forests that were included in the park in 1996 (i.e.,
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Forest Ecology and Management 449 (2019) 117462
they were mainly formerly managed forests). The remaining area
mostly comprises managed forests. Because of various regulations (e.g.,
a ban on logging in stands older than 100 years) and conservation re-
gimes (e.g., Natura 2000 site), wood extraction is not intensive com-
pared to that in the commercial forests in Poland, i.e., 1.31 m3/ha/year
and 5.65 m3/ha/year, respectively (data obtained from Bureau for
Forest Management and Geodesy). There are also 23 nature reserves
with a total area of approximately 120 km2 with practically no man-
agement activity.
The Białowieża Forest is covered by a mosaic of broadleaved, con-
iferous and mixed stands. The typical landscape is flat (131.6–195.6 m
a.s.l.) with valleys containing small rivers and meadows. Detailed
characteristics of the study area were given by Faliński (1986).
2.2. Study organisms
The studied species are characterized by similar ecology. Larvae live
beneath the bark of recently dead trees (usually those that had died up
to 5 years ago), either standing or downed. Larval development lasts up
to 3 years, with pupation taking place in the same microhabitat. Adult
beetles are active from spring to autumn and can be encountered under
the bark and sometimes, but rarely, outside of it (e.g., when they dis-
perse to seek trees suitable for inhabitation).
The studied species are rare or extinct in many areas of their dis-
tribution. They are red-listed and legally protected in most European
countries. Cucujus cinnaberinus and B. schneideri are listed in Annex II,
and the former species is also listed in Annex IV of the EU Habitat
Directive.
Cucujus cinnaberinus is distributed throughout Europe; however,
most populations are confined to its central parts (Horák et al., 2010).
Until recently, the species was considered a relic of primeval forests;
however, some studies also indicate its occurrence in human-modified
environments, including commercial forests and tree plantations
(Bussler, 2002; Horák et al., 2010). The detection of this species has
increased in recent years, most likely due to the intensification of stu-
dies and increased abundance of local populations resulting from the
observed dieback of several tree species and consecutive expansion to
new areas. The list of preferred host trees includes broadleaved as well
as coniferous species, particularly poplars (Populus spp.), willows (Salix
spp.), oaks (Quercus spp.), alders (Alnus spp.), ashes (Fraxinus spp.), and
pines (Pinus spp.) (e.g., Horák et al., 2010; Vrezec et al., 2017).
The congeneric species, C. haematodes, is distributed in Eurasia. It is
categorized as critically endangered in the territory of the European
Union (Cálix et al., 2018). Some authors have suggested a preference of
C. haematodes for coniferous trees, especially silver fir (Abies alba Mill.)
and Norway spruce (Picea abies (L.) H. Karst) (Burakowski et al., 1986);
nevertheless, it has also been recorded on broadleaved trees (Horák
et al., 2009, 2011).
The distribution of B. schneideri includes most central and northern
European countries; however, the species is declining or has become
extinct in many areas, particularly in western parts of its distribution
(Karalius and Blažytė-Čereškienė, 2009; Pettersson et al., 2010). Fur-
thermore, B. schneideri is also found in Russia, China, Mongolia, Japan
and Korea (Gutowski et al., 2014b). The usual host tree for B. schneideri
larvae is Scots pine (Pinus sylvestris L.).
2.3. Data collection
Study data were collected in 2016 and 2017. To identify the current
distribution patterns of the studied beetles and avoid potential bias
resulting from the subjective selection of sample sites, we used a rec-
tangular (650 × 650 m) grid, which was generated over a map of the
Białowieża Forest (Fig. 1). The nodal points of the grid indicated the
forest sub-compartments, i.e., smallest forest units, which were uniform
with respect to species, age, and habitat composition. The forest sub-
compartments (hereafter forest patches) were then surveyed in the field
T. Jaworski, et al. Forest Ecology and Management 449 (2019) 117462

Fig. 1. Study design: location of the Białowieża Forest in NE Poland (upper left), division of the study area (lower left) into zones with different management
intensities, i.e., managed forests (light grey), reserves and parts of the BNP under partial protection (dark grey), and the strict reserve of the BNP (black). The dashed
line indicates the border of the BNP. The right panel illustrates the distribution of the sampled dead trees (dark grey dots) within the study area.

for the presence of trees suitable for the studied beetles, i.e., standing or
downed dead trees with slightly loose bark and hard wood on the
surface (e.g., Horák et al., 2012; Goczał and Rossa, 2017). The studied
beetles inhabit trees killed by natural as well as anthropogenic causes;
therefore, the sampled trees were not categorized in this respect. The
survey within a particular forest patch continued until 10 dead trees
were sampled or until the whole area was surveyed.
As a result, 1,321 forest patches were visited, and 11,623 trees were
sampled (Table 1, Fig. 1). Each tree was inspected for the presence of
the studied beetles by peeling off bark from approximately 1 m2 of the
trunk surface. Larvae were identified at the species level based on
morphological characteristics (Saalas, 1937; Bonacci et al., 2012;
Gutowski et al., 2014a) and then released under the bark of the same
tree. Data on adult beetles were omitted from further analyses because
their presence on a particular tree does not reflect actual preferences; it
may be a result of accidental arrival to that tree, hiding behaviour, etc.
Tree-level characteristics were recorded: tree species, diameter (i.e.,
DBH for standing and downed trees or diameter in the middle of the
length for logs and limbs; measured in cm), bark coverage (estimation
in 10% intervals), and tree position (standing/downed).
Landscape-level characteristics were also recorded. Namely, forest
patches were categorized with respect to management intensity based
on the present administrative division of the Białowieża Forest. We used
three categories: managed (forests under low-to-moderate manage-
ment), reserves (forest within reserves and parts of the BNP with partial
protection – mainly managed forests in the past but excluded from
management since several decades), and strict (forests within the strict
reserve of the BNP – excluded from human intervention since almost
100 years). Hence, the distribution patterns of the studied beetles were
investigated along a gradient representing an increasing level of dis-
turbance intensity related to forest management within the study area.
We further investigated the influence of dead wood amount and habitat
area on the abundance of the studied beetles. Dead wood (m3) within
each forest patch was measured in circular 400 m2 plots (data from the
inventory performed by the Polish State Forests in 2016). The influence
of habitat area was investigated using the area (ha) of each forest patch.
2.4. Statistics
Host tree preferences of the studied beetles were analysed using a
modified Ivlev’s electivity index (Jacobs, 1974). The following formula was
used: D = (r-p)/(r + p-2rp), where r represents the fraction of inhabited
trees of a given species among all inhabited trees, and p represents the
fraction of analysed trees of a given species among all analysed trees.
Further analyses were performed in R 3.0.2. The relationship of the
abundance of the species with space was tested using Geary’s C test

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T. Jaworski, et al. Forest Ecology and Management 449 (2019) 117462

Table 1 coverage were analysed with spline functions. Tree species were treated
Tree species analysed for the presence of the study beetles in the Białowieża as random factors. For the model at the landscape level, we used
Forest in 2016–2017. management intensity (coded as 1 for strict protection, 2 for reserves,
Tree species Management intensity Total % and 3 for managed forests; see previous subsection for the categoriza-
tion of areas). Dead wood amount and habitat area were analysed with
Scientific name Common Managed Reserves strict spline functions. The number of sampled trees was treated as a random
name
factor.
Picea abies Norway 2,178 768 382 3,328 28.6
spruce
Fraxinus excelsior European 944 849 333 2,126 18.3 3. Results
ash
Pinus sylvestris Scots pine 1,334 368 147 1,849 15.9
Alnus glutinosa Black alder 656 566 90 1,312 11.3 3.1. Incidences
Quercus robur Common 753 281 89 1,123 9.7
oak We observed 2,953 larvae of C. cinnaberinus (mean 0.254 ± 0.011
Betula pendula Silver birch 657 233 62 952 8.2 SE; 0–38 larvae per sampled tree) on 1,134 trees (hereafter incidences),
Populus tremula Aspen 331 100 43 474 4.1
2,040 larvae of C. haematodes (0.176 ± 0.007; 0–18) with 1,031 in-
Carpinus betulus Hornbeam 110 58 38 206 1.8
Tilia cordata Small- 45 34 27 106 0.9 cidences and 472 larvae of B. schneideri (0.041 ± 0.004; 0–15) with
leaved lime 186 incidences (Fig. 2). The number of trees inhabited by any of the
Salix spp. Willow 54 34 0 88 0.8 study species was 2,148 (18.5% of all sampled trees). We did not ob-
Acer platanoides Norway 27 4 7 38 0.3
serve any of the species on 9,475 trees.
maple
Ulmus spp. Elm 5 4 5 14 0.1
Corylus avellana Hazel 0 0 6 6 0.1
Sorbus aucuparia Rowan 0 1 0 1 < 0.01 3.2. Tree level
Total 7,094 3,300 1,229 11,623 100

The abundance and incidence of C. cinnaberinus larvae were highest

on aspen, followed by willow and ash (Table 2). The most preferred tree
with randomizations with the library spdep. The result was that the
species by C. haematodes were ash and alder. The third studied beetle,
abundance of C. cinnaberinus was not influenced by space (C = 0.99;
B. schneideri, occurred almost exclusively on pine. Spruce and birch
P = 0.22), while C. haematodes (C = 0.94; P < 0.001) and B. schneideri
were mainly avoided by all studied species.
(C = 0.94; P < 0.001) had an aggregated pattern of spatial distribu-
Standing dead trees were preferred by B. schneideri, while C. hae-
tion. Due to the significant influence of space, autocovariates were
matodes was more abundant in downed dead wood at the tree level
computed for the latter two species using the GPS coordinates of par-
(Table 3). The effect of space had no significant influence on the spatial
ticular dead wood samples and were added to the analyses for these two
distribution of C. cinnaberinus (i.e., its distribution in the Białowieża
species (de Frutos et al., 2007; Horak, 2013) with the library spdep.
Forest was random). Cucujus haematodes and B. schneideri showed more
We were interested in the detailed responses of species; therefore,
clustered distribution patterns. The results regarding the diameter of
we used non-linear statistical methods. The relationships between the
dead wood revealed the preference of C. cinnaberinus and B. schneideri
species population densities (i.e., abundance of larvae) and the ex-
for large trees. Both species showed polynomial trends in response;
planatory variables were tested using generalized additive mixed-effect
their abundance first increased with diameter, with an approximate
models (GAMMs) with the libraries mgcv and HH. The distribution of
peak at 65 cm for C. cinnaberinus and the most significant peak at 75 cm
the dependent variable was treated as a negative binomial due to po-
for B. schneideri, and then decreased, with a rather low response re-
tential overdispersion (e.g., Wood, 2006). We used the appropriate Θ-
flected by the high dispersion of the confidence intervals (Fig. 3). In-
value on the basis of the histogram of the dependent variable dis-
creasing bark coverage positively influenced the abundance of B.
tribution. For the model at the tree level, we used tree position (coded
schneideri and mainly decreased the abundance of C. haematodes larvae
as 0 for downed and 1 for standing dead trees) and space (for C. hae-
(Fig. 3).
matodes and B. schneideri) as linear parameters. Diameter and bark

Fig. 2. Distribution and abundance of larvae of C. cinnaberinus (left), C. haematodes (middle) and B. schneideri (right) in the Białowieża Forest, Poland. Circles
represent the number of larvae/m2. The dark line indicates the border of the BNP (classification of the study area into management intensity zones is presented in
Fig. 1).

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T. Jaworski, et al. Forest Ecology and Management 449 (2019) 117462

Table 2
Incidence (I), abundance (A) and values of modified Ivlev’s electivity index (D) for tree species inhabited by C. cinnaberinus, C. haematodes and B. schneideri in the
Białowieża Forest, Poland. Note that I is the percent of inhabited trees of a given species among all analysed trees of this species; A is the number of larvae per 1 m2 of
trunk surface; D ranges from −1 (=total avoidance) to +1 (=total preference). Data for tree species with n < 50 are not shown; see Table 1.
Tree species C. cinnaberinus C. haematodes B. schneideri

I A D I A D I A D

Alnus glutinosa 4.6 0.10 −0.38 16.9 0.36 0.37 0.6 0.01 −0.48
Betula pendula 3.4 0.07 −0.51 8.2 0.17 −0.04 0.5 0.01 −0.53
Carpinus betulus 12.6 0.38 0.13 5.8 0.14 −0.21 0.0 0.00 −1.00
Fraxinus excelsior 17.2 0.35 0.36 17.5 0.34 0.43 0.0 0.00 −0.95
Picea abies 4.3 0.10 −0.47 2.9 0.05 −0.59 1.0 0.02 −0.29
Pinus sylvestris 10.7 0.36 0.05 6.8 0.13 −0.15 7.1 0.21 0.85
Populus tremula 29.7 0.92 0.54 6.8 0.16 −0.14 0.0 0.00 −1.00
Quercus robur 11.5 0.36 0.09 6.6 0.13 −0.16 0.6 0.01 −0.47
Salix spp. 25.0 0.63 0.44 9.1 0.16 0.01 0.0 0.00 −1.00
Tilia cordata 10.4 0.26 0.03 3.8 0.09 −0.40 0.0 0.00 −1.00

Table 3 et al., 2014b), and our results support the need for the maintenance of
Species responses to the environmental variables at the tree level in the such trees as the preferred habitat for this species.
Białowieża Forest, Poland. Values were derived from GAMMs. Tree size and bark characteristics (e.g., coverage and thickness) are
Species Variable t F P the most important factors influencing the species richness and com-
position of saproxylic beetles (Økland et al., 1996; Ranius and Jansson,
Cucujus cinnaberinus Position −1.5 0.134 2000; Horák and Pavlicek, 2013), and some rare species often depend
Diameter 58.59 < 0.001
on large trees with thick bark (Blažytė-Čereškienė and Karalius, 2011;
Bark 2.09 0.184
Cucujus haematodes Position −6.72 < 0.001 Miklín et al., 2018). The diameter of dead wood is also considered to be
Space 5.88 < 0.001 an important factor (Buse et al., 2016) and, together with the amount of
Diameter 3.49 0.062 dead wood, is a characteristic that is potentially useful for evaluating
Bark 8.49 < 0.001 the species-area relationships of saproxylic organisms (Seibold et al.,
Boros schneideri Position 4.01 < 0.001
2015b; Mazzei et al., 2018; Mladenović et al., 2018). The results of this
Space 15.61 0.001
Diameter 20.84 < 0.001 study are in line with those from previous research concerning the ef-
Bark 5.80 0.016 fects of tree diameter on the populations of the studied beetles. Namely,
the preference of C. cinnaberinus for large trees has been both directly
(i.e., by measurements of the tree diameter; see Vrezec et al., 2017) and
3.3. Landscape level indirectly (i.e., as reflected by bark thickness; see Goczał and Rossa,
2017) demonstrated. Increasing tree diameter has also been found to
Management intensity influenced both Cucujus species. Cucujus positively influence B. schneideri (Blažytė-Čereškienė and Karalius,
cinnaberinus had the highest abundances in managed forest patches, 2011). This indicates that both species require large dead trees, which
whereas C. haematodes showed the opposite pattern (Table 4). In- are most likely more suitable in terms of the availability of food and
creasing dead wood accumulation and forest patch area positively in- space, humidity, etc., than smaller trees.
fluenced the abundance of C. cinnaberinus larvae. Cucujus haematodes Bark coverage is a specific characteristic of dead wood habitats
was negatively affected by the increasing area of forest patches (Fig. 4). because it is related mainly to species living under the bark (Dynesius
et al., 2010; Ulyshen et al., 2016). The relationship with bark coverage
was not significant in past studies on C. cinnaberinus (Horák et al., 2012;
4. Discussion
Goczał and Rossa, 2017), which is relatively consistent with our study.
We revealed that larvae of B. schneideri were rather positively influ-
4.1. Habitat requirements at the tree level
enced by increasing bark coverage, which contrasts with observations
from Lithuania suggesting a preference of B. schneideri for trees with
Our study demonstrated the diversified habitat requirements of the
fragmented bark (Blažytė-Čereškienė and Karalius, 2011). The results of
studied species in the Białowieża Forest. First and foremost, the beetles
both studies, however, must be interpreted with caution due to the
differed in host tree choice. There were profound differences even be-
different methods used for estimating bark coverage on the sampled
tween the two Cucujus species, which was interesting given that phy-
trees. Interestingly, the larvae of the third studied species, C. haema-
logenetically similar saproxylic insects tend to inhabit rather closely
todes, were more abundant when the bark only partly covered the dead
associated tree species (Kohlmayr et al., 2002; Bertheau et al., 2009;
wood, which suggests that this species prefers terminal stages of
Wallin et al., 2009). Second, downed dead wood was preferred by C.
phloem decomposition. This finding is also corroborated by the pre-
haematodes, while C. cinnaberinus was rather indifferent regarding tree
ferences of C. haematodes for downed trees, which are often more de-
position. At the same time, B. schneideri preferred standing dead trees.
void of bark than standing trees.
Discrimination of dead wood position is one of the most important
aspects driving saproxylic beetle composition (Jonsell and Weslien,
2003; Gibb et al., 2006; Johansson et al., 2007). Our results are con- 4.2. Effects of landscape-level attributes
sistent with those from a previous study by Horák et al. (2012), who
found no response of C. cinnaberinus regarding the position of dead Studies on the influence of humans on saproxylic beetles in forests
trees. However, to the best of our knowledge, the preference of C. that are excluded from modern forest management are not frequent.
haematodes for lying dead wood has not been indicated in past studies; Authors have mainly studied the differences between managed and
therefore, these results are also important for potential management abandoned forests (Väisänen et al., 1993; Hilszczański et al., 2007). In
strategies aimed at the conservation of this saproxylic beetle. The se- the present study, we found that the management intensity within a
lection of standing dead trees by B. schneideri was indicated (Gutowski forest patch affected two Cucujus species, which furthermore had

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T. Jaworski, et al. Forest Ecology and Management 449 (2019) 117462

Fig. 3. Species responses to tree diameter (a, b) and bark coverage (c, d) at the tree level in the Białowieża Forest, Poland. Visualization was derived from GAMMs
with Cucujus cinnaberinus (a), C. haematodes (c) and B. schneideri (b, d). Values in brackets on the y-axis are DF of the spline function (full line), dashed lines indicate
confidence intervals.

Table 4 and willows, in comparison to the strict reserve (see Table 1). Fur-
Species responses to the environmental variables at the landscape level in the thermore, disturbances related to management (even though manage-
Białowieża Forest, Poland. Values were derived from GAMMs. ment intensity is generally low in the study area) are usually related to
Species Variable t F P the creation of a more open canopy – a factor that has been indicated to
enhance the abundance of C. cinnaberinus (Horák et al., 2012; Goczał
Cucujus cinnaberinus Management 2.50 0.013 and Rossa, 2017). In contrast, C. haematodes preferred tree species often
Dead wood 4.04 0.045
associated with moist sites (Beck et al., 2016; Houston Durrant et al.,
Area 8.23 0.004
Cucujus haematodes Management −3.09 < 0.001 2016), which could have been less intensively managed in the past, e.g.,
Dead wood 3.81 0.051 owing to their inaccessibility to humans. Furthermore, large areas of
Area 7.13 0.008 moist and wet forests in the Białowieża Forest have been formerly in-
Boros schneideri Management 0.07 0.942 cluded in the BNP (Faliński, 1986) and reserves (e.g., Regulation of the
Dead wood 0.02 0.886
Area 2.93 0.087
Minister of Environment, 2003). This could have likely caused bias
resulting in more frequent observations of C. haematodes in unmanaged
forest fragments.
opposite responses to this variable, i.e., C cinnaberinus tended to prefer The quantity of dead wood is crucial for many saproxylic insects
managed sites, while C. haematodes avoided them. These contrasting (e.g., Franc et al., 2007; Müller and Bütler, 2010, and the literature
patterns, however, may not directly result from the impact of forest cited therein). In our study, only C. cinnaberinus positively responded to
management but are rather a reflection of the distribution of the pre- dead wood accumulation. However, this species was the least abundant
ferred habitat trees in the study area. Namely, managed forests could in the strictly protected part of the Białowieża Forest, which is char-
have been favourable for C. cinnaberinus because they contained a re- acterized by significantly higher amounts of dead wood and its con-
latively high proportion of the preferred dead trees, particularly aspens tinuity in comparison to other sites (e.g., Bobiec, 2002). One plausible

6
T. Jaworski, et al.
Fig. 4. Species responses to dead wood volume (a) and forest patch area (b, c) at the landscape level in the Białowieża Forest, Poland. Visualization was derived from
GAMMs with Cucujus cinnaberinus (a, b) and C. haematodes (c). Values in brackets on the y-axis are DF of the spline function (full line), dashed lines indicate
confidence intervals.
explanation for this phenomenon is related to dead wood quality,
namely, a low abundance of the preferred tree species within the
strictly protected parts of the study area (see Table 1). It cannot be
excluded that other factors, including unfavourable light conditions for
C. cinnaberinus in the strict reserve, may have also negatively influenced
this species.
Our last studied habitat attribute, i.e., forest patch area, had op-
posite impacts on the two Cucujus species, i.e., C. cinnaberinus positively
responded to this variable, while C. haematodes was negatively affected.
This finding is relatively easy to unravel for C. cinnaberinus, given that
larger areas tend to contain more of the large-diameter trees preferred
by this species, which was indicated by our results and by previous
research (Vrezec et al., 2017). Understanding the negative area-abun-
dance relationship for C. haematodes is a challenging task, but one
possible explanation might be that trees preferred by this species ty-
pically grow at wet and moist sites (Beck et al., 2016; Houston Durrant
et al., 2016) and are thus often spatially confined to small forest pat-
ches.
4.3. Habitat requirements and distribution patterns
Saproxylic insects are spatially limited by dead wood availability
(e.g., Groove, 2002). Therefore, our results regarding the different
distribution patterns of the studied beetles should be mainly explained
by the diversified distribution of the preferred dead trees in the Biało-
wieża Forest. The first of the studied beetles, C. cinnaberinus, inhabited
nearly the entire study area with almost no white spaces. However, this
species had the lowest abundance in the strict reserve of the BNP, which
might be correlated with the loss of the preferred habitat trees in this
area. Although C. cinnaberinus is considered relatively opportunistic
regarding inhabited trees (Vrezec et al., 2017), our study indicated its
strong preference for aspens and willows. These trees are currently
vanishing from the strict reserve of the BNP (Bernadzki et al., 1998;
Brzeziecki et al., 2012; Paluch, 2014, 2015), and the same is observed
in forests under low levels of management in the remaining parts of the
Białowieża Forest (Drozdowski et al., 2012). Another important reason
for the relatively small abundance of C. cinnaberinus in strict reserves
may be related to unfavourable thermal conditions for this sun-pre-
ferring species (Horák et al., 2010, 2012; Goczał and Rossa, 2017).
Cucujus haematodes appeared to be relatively widespread in the
study area; however, its distribution was clustered, which leads to the
conclusion that it differs in terms of habitat requirements from those of
the previous species. Indeed, our study indicated the preference of C.
haematodes for tree species related to moister habitats, which are ty-
pically more spatially limited (e.g., to lower elevations, watercourses,
etc.), which could have influenced its distribution in the Białowieża
Forest.
7
Forest Ecology and Management 449 (2019) 117462
The third saproxylic beetle, B. schneideri, was found least and re-
vealed a scattered pattern of distribution in the whole study area. The
reason for this, in our opinion, is related to its preference for large
pines, which was demonstrated by our study and by previous research
(Blažytė-Čereškienė and Karalius, 2011; Gutowski et al., 2014b).
Namely, old pines are currently rare or even lacking from the landscape
of the Białowieża Forest (Bernadzki et al., 1998; Drozdowski et al.,
2012; Miścicki, 2012, 2016; Paluch, 2014, 2015; Brzeziecki et al., 2012,
2016, 2017). On the other hand, younger pine stands in the study area
may still be unsuitable for this species (Blažytė-Čereškienė and Karalius,
2011; Gutowski et al., 2014b). Another explanation for the observed
scattered distribution of B. schneideri might be related to its preference
for sun-exposed sites in forests (Blažytė-Čereškienė and Karalius, 2011,
but see Gutowski et al., 2014b), which are currently rare in the area due
to the dominance of overshading trees.
4.4. Conservation perspectives and management implications
The results of this study indicate several problems related to the
conservation of the three saproxylic beetles in the Białowieża Forest
and other protected areas. Namely, the regeneration of the preferred
tree species in many parts of the Białowieża Forest is now extremely
limited, which may result in the disruption of the spatial and temporal
habitat continuity for the studied beetles. For example, Bernadzki et al.
(1998) observed no recruitment of Scots pine in the strict reserve of the
BNP in the period of 1936–1992, and similar situations were also ob-
served for other light-demanding trees (Bernadzki et al., 1998;
Brzeziecki et al., 2012). The authors indicated compositional shifts re-
lated to the expansion of shade-tolerant trees (particularly hornbeam)
as the main factors impeding the regeneration of light-demanding trees.
This process is also facilitated by the suppression of human-related
disturbances, including fires and pasturing, which were relatively fre-
quent in the past and enabled pine regeneration (Niklasson et al., 2010;
Samojlik et al., 2016; Zin, 2016). In consequence, habitat trees of major
importance for populations of these organisms are declining in areas
under full protection (e.g., Bernadzki et al., 1998; Brzeziecki et al.,
2012; Paluch, 2014, 2015) and even in non-protected sites that are
subjected to low-intensity management (Drozdowski et al., 2012). This
process is particularly evident for aspen and pine, which are preferred
by C. cinnaberinus and B. schneideri, respectively. A similar situation is
observed for alder and ash, which are the primary habitat trees of C.
haematodes. Even if these trees are still relatively abundant in some
parts of the Białowieża Forest, they usually cannot grow to large di-
mensions, which is mainly due to competition with other trees
(Miścicki, 2016).
Regarding natural disturbances, the ongoing outbreak of the spruce
bark beetle Ips typographus L. in the Białowieża Forest could potentially
T. Jaworski, et al.
have positive effects for the studied beetles. By killing large numbers of
trees, bark beetles create gaps and increase light accessibility in the
forest, which induces the regeneration of some tree species (e.g.,
Jonášová and Prach, 2004). Disturbance by bark beetles was also found
to positively influence saproxylic insects by creating sunny openings
and more complex habitats in mountain spruce forests (e.g., Müller
et al., 2008b). However, due to the abovementioned rapid growth of
shade-tolerant trees, natural gap formation alone did not support the
regeneration and recruitment of light-demanding trees in the Biało-
wieża Forest. High browsing pressure by wild animals is yet another
factor contributing to the limited tree regeneration in this area (Kuijper
et al., 2010; Hedwall et al., 2018). Furthermore, closed-canopy forests,
which now prevail in the landscape of the Białowieża Forest, may not
fulfil the requirements of the species of interest due to the occurrence of
unfavourable thermal conditions. This may have negative effects for at
least two of the studied species, namely, C. cinnaberinus (Horák et al.,
2010, 2012, Goczał and Rossa, 2017) and B. schneideri (Blažytė-
Čereškienė and Karalius, 2011), as well as for some other threatened
saproxylic beetles (Kašák and Foit, 2018; Miklín et al., 2018).
From the perspective of the conservation of the studied beetles, the
establishment and maintenance of more open conditions within the
Białowieża Forest is recommended to ensure continuity of the preferred
habitat trees and fulfil their demands for sun-exposed sites. If this goal
is not achieved by the non-intervention approach (e.g., due to spatial
and/or temporal scarcity of natural disturbances) the combination of
low-intensity forest management and other practices of forest use
should be considered. These practices may include array of manage-
ment techniques which were frequent in the past in this area, e.g.,
pasturing of domestic animals, prescribed burning, litter gathering,
wild bee-keeping (Latałowa et al., 2015; Samojlik, 2016; Samojlik et al.,
2016; Zin, 2016). These activities may allow regeneration of sun-de-
manding tree species on the one hand, and maintain more open habitats
in forest on the other. Furthermore, they go hand in hand with the
presence of some threatened and rare animals (e.g., Horák and Rébl,
2013; Samojlik et al., 2018) and plants (e.g., Douda et al., 2016). Future
studies are needed to confirm which of those options are the most fa-
vourable to maintain populations of the three studied species.
Acknowledgements
This study was financed by the Polish State Forests, National Forest
Holding, under the project Biodiversity assessment of the Białowieża Forest
based on selected natural and cultural components.
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.foreco.2019.117462.
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