Biodivers Conserv (2014) 23:449–466
DOI 10.1007/s10531-013-0612-3
ORIGINAL PAPER
Importance of high quality early-successional habitats
in managed forest landscapes to rare beetle species
Diana Rubene • Lars-Ove Wikars • Thomas Ranius
Received: 11 June 2013 / Accepted: 20 December 2013 / Published online: 3 January 2014
! Springer Science+Business Media Dordrecht 2014
Abstract Species adapted to early-successional forest habitats are in managed landscapes
largely confined to clearcuts. To improve habitat quality on clearcuts, green tree and dead
wood retention is widely applied in forestry; however, its effects on rare early-successional
species have rarely been shown. We repeatedly surveyed two red-listed beetle species
(Upis ceramboides and Platysoma minus) on clearcuts in a managed boreal forest landscape. We found that U. ceramboides decreased its occupancy over time while P. minus
increased, indicating that red-listed species vary in their ability to successfully utilise
managed habitats. We found no effect of connectivity on probability of occurrence, colonisation or extinction per clearcut. Trees retained alive improved habitat quality of
clearcuts, since both species were more frequent in dead wood of such trees, in comparison
to logging residues. We suggest that retention can be improved by protecting and creating
dead wood as intact trees during harvesting. Rare specialist species require habitat of high
quality, and consequently it is impossible to meet the requirements of these species on
every clearcut. To preserve all early-successional species at a regional scale, we recommend focusing retention of green trees and dead wood to one or a few trees species on each
clearcut and in each landscape.
Keywords Boreal forest ! Connectivity ! Colonisation ! Dead wood !
Retention forestry ! Saproxylic insects
D. Rubene (&) ! L.-O. Wikars ! T. Ranius
Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, 75007 Uppsala,
Sweden
e-mail: diana.rubene@slu.se
L.-O. Wikars
e-mail: lars.wikars@gmail.com
T. Ranius
e-mail: thomas.ranius@slu.se
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Introduction
Early-successional habitats in natural forests are often characterized by high species
richness, as legacies from previous forest stage combine and interact with new conditions
created by disturbance (Lindenmayer and Franklin 2002; Swanson et al. 2010). In natural
forest landscapes, early-successional habitats are created by various disturbances, from
small scale gap dynamics and individual wind-felled trees, to large stand-replacing events
such as storms and intense forest fires (Esseen et al. 1997; Franklin et al. 2002). The largescale disturbances provide resources that are rare in mature forests, e.g. sun-exposed
injured and dead trees and exposed patches of mineral soil (Swanson et al. 2010), and host
distinct species assemblages (Similä et al. 2002; Boucher et al. 2012).
In Europe and parts of North America, many forests lack natural disturbance dynamics,
because they are managed for wood production. Salvage logging is widely practiced after
windstorms and fires, which removes dead trees left by disturbance and thereby impairs
key ecosystem processes (Lindenmayer et al. 2004; DellaSala et al. 2006; Cobb et al. 2011;
Boucher et al. 2012). Natural early-successional habitats have consequently become rare
with negative consequences for many species (Kaila et al. 1997; Swanson et al. 2010).
Managed forests are denser (to maximize production per area) and conditions thereby more
shaded than in naturally shaped forests, further disfavouring organisms dependent on open
forest conditions (Linder and Östlund 1998). Today, early-successional forest stages in
many managed landscapes are predominantly created by clearcutting. As a consequence,
species that are naturally adapted to utilize habitats created by windstorms, fires and gap
dynamics may be restricted to clearcuts (Kaila et al.1997; Jonsson and Siitonen 2012).
Species specialized in disturbed forest habitats can only persist in a certain habitat patch
for a limited amount of time, until it becomes unsuitable through succession. Long-term
species persistence is thus only possible on landscape level and requires a continuous
creation of new patches that can be colonised by species to compensate for deterministic
local extinctions (Jonsson 2012). Many species that depend on early post-fire forest habitats may be able to survive in harvested forest patches, if habitat quality and patch network
density in the landscape is high enough (Hanski 2008). In attempt to emulate natural
disturbance in managed forests, retention of living trees, in particular deciduous trees, and
dead wood on clearcuts is today a common silvicultural practice (Franklin et al. 1997;
Gustafsson et al. 2010). However, dead wood volume retained at harvesting is insufficient
to fully mimic the natural post-disturbance habitat (Gustafsson et al. 2010). Insufficient
dead wood amount and diversity sets strong limitations on managed forests’ capacity to
host species-rich communities (Siitonen 2001; Similä et al. 2003). Furthermore, soil
preparation and planting is used to speed up reforestation, significantly shortening the time
span during which clearcut habitat can be used by early-successional species (Swanson
et al. 2010). In addition, deciduous trees, which are characteristic components of natural
disturbance-shaped boreal forests, have decreased in many regions of Northern Europe as a
consequence of management (Fransson 2011). Therefore, species associated with deciduous trees or dead wood, with high demands for habitat quality or connectivity might be
unable to persist in managed forest landscapes.
Studies on early-successional species have mostly considered diversity patterns at forest
stand level a year or two after clearcutting (e.g. Hyvärinen et al. 2009), but there is a lack
of understanding of species temporal dynamics on landscape level. In this study, we have
analysed the importance of habitat quality on clearcuts and spatiotemporal dynamics on
landscape scale of two rare early-successional beetles, Upis ceramboides and Platysoma
minus. We chose these as model species as they are considered to be negatively affected by
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intensified forest management, since in natural landscapes they occur in recently burned
forests (Palm 1951; Pettersson and Ehnström 2010). Threatened dead wood dependent
species appear to particularly depend on high amount and diversity of dead wood, and to
have lower occurrence in managed compared to semi-natural forests (Similä et al. 2002).
We have repeatedly surveyed U. ceramboides and P. minus in early-successional
habitats created by clearcutting in a forest landscape in central Sweden in order to
(i) analyse which factors affect colonisation and extinction probability by observing
changes in species occurrences over time, (ii) determine the importance of amount and
spatial distribution of dead wood within clearcuts for species occurrence and (iii) study the
successional patterns in habitat use of the main study species vs. more common dead wood
inhabiting beetle species over time. We expect that species occupancy per clearcut will
change over time according to the amount of suitable habitat. We predict that habitat
amount and suitability will affect species occurrence on several scales: by the properties of
the dead wood objects, properties of the habitat patches (clearcuts) themselves and by
connectivity to dispersal sources in the landscape.
Methods
Study species
The studied species, U. ceramboides (Tenebrionidae) and P. minus (Histeridae), are
saproxylic (=dependent on dead wood) beetles that inhabit boreal forests of Europe, Asia
and North America. These species are thought to benefit from forest fires which create
open, sun-exposed habitats rich in dead wood (Palm 1951). In managed forests of North
America, U. cerambiodes appears to be strongly associated with open areas on clearcuts
(Webb et al. 2008). Also in Sweden, the species does not appear to use closed canopy
forest as habitat, which makes it particularly dependent on quality of clearcuts (L. Wikars,
pers. obs., from previous surveys of *1,000 substrates in forests, most of them close to
clearcuts with the species present). Larvae of both species develop under bark of sunexposed dead deciduous wood, usually birch, which is white-rotted by fungi like Fomes
fomentarius (Palm 1951; Ehnström and Axelsson 2002). Upis ceramboides larvae feed and
develop in the phloem and superficial wood of dead birch over 2–3 years (Pettersson and
Ehnström 2010). Larvae and adults of P. minus are predators (Baranowski 1994).
In Sweden, both species are included in the red list (U. ceramboides VU, P. minus NT),
because their distribution area is limited, highly fragmented and currently shrinking
(Gärdenfors 2010). Upis ceramboides has in Sweden a clearly documented regional
extinction pattern from the South to the North. It has been recorded from most Swedish
provinces, but gone regionally extinct from southern Sweden during late 1800s and early
1900s (Gärdenfors 2010). The southernmost population is today found in our study area,
separated from a larger distribution area in the North by about 200 km. The species seems
to still be abundant on clearcuts in northernmost Sweden (Naalisvara 2013). Platysoma
minus is widely distributed across Sweden, but very little is known about its ecology, and it
is thought to be declining on national level (Gärdenfors 2010).
Study area
We studied a 225 km2 landscape in central Sweden, situated at an elevation of 250–500 m
and covered by managed boreal forest, with Scots pine (Pinus sylvestris) and Norway
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Table 1 Descriptive characteristics of the inventoried clearcut sites (mean values)
No. of
substrates
analysed
Clearcut
area (ha)
Year
No. of cleracuts
analysed
(nr of searched
substrates)
2004
65 (927)
231a
17.05
2010
110 (898)
898
18.37
Clearcut
age (years)
Dead wood
aggregation
density
(m3 ha-1)
Substrate
decay
class
Prop. of
substrates
with
white-rot
8.21
35.57b
2.87
0.52
9.61
47.04b
3.45
0.50
a
Substrate properties were measured on three clearcuts in 2004
b
Highest dead wood density was measured on different scales (59 smaller scale in 2010)
spruce (Picea abies) as the dominant tree species. The forest has been managed by
clearcutting for about 50 years and is owned by a private company, Holmen Skog AB,
which has been certified by FSC since 1998 and by PEFC since 2003. The area has
historically (until 1900) been strongly affected by fires and has therefore had a considerable component of deciduous trees. Currently, on regional level, only about 10 % of the
forest stands have [35 % deciduous trees. The average amount of dead deciduous wood is
2.3 m3 ha-1 (Fransson 2011). During the last decade, at least two large forest wildfires
(followed by salvage logging) have occurred and prescribed burning has been employed on
some clearcuts, resulting in approximately 340 ha burned and harvested area.
Site selection
We conducted landscape surveys in 2004 and 2010. Clearcut forest stands for the surveys
were selected using aerial photographs in 2004 (Wikars and Orrmalm 2005) and using GIS
data from the forest company on forestry operations in 2010. Stands of age 3–14 years
(harvested 1990–2001) were included in the first survey, and the age limit was based on
previous knowledge about U. ceramboides habitat use. We set the minimum age to three
years due to that the species does not use fresh dead wood (L. Wikars, pers. obs.) and most
of the dead wood is created during harvesting. Further, the species have only been found on
sun exposed substrates (see Study species) and almost all substrates become too shaded
when planted forests are more than 14 years old (Jonsson et al. 2006). In the second
survey, we revisited all the previously surveyed clearcuts and additionally all newly
established ones, which were at least three years old (harvested 2001–2007). Totally 73
clearcut stands were surveyed in 2004 and 213 in 2010. All stands in the landscape
harvested in 2001–2007 were surveyed and 40 % of the stands harvested in 1990–2000.
When calculating connectivity, we took into account all clearcuts, also those not surveyed
(see section on connectivity). Prior to analyses, clearcuts bordered to each other and within
5 years of age difference were pooled to one single data point, as species likely perceive
them as one single habitat patch. Data were then combined as a weighted average for the
whole area. Clearcuts where no birch wood was present were excluded from analyses as
they do not constitute habitat. In the final analysis there were 65 clearcuts for 2004 and 110
for 2010. Summary of descriptive habitat properties of the surveyed clearcuts can be found
in Table 1.
Species survey
The aim of the first survey was to analyse U. ceramboides occupancy in relation to habitat
properties on clearcut level and substrate (dead wood object) level. In addition, we
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recorded presence/absence of P. minus adults and larvae of another two common beetle
species inhabiting dead birch: the longhorn beetle Rhagium mordax (found in birch wood
in our study region) and the lamellicorn beetle Trichius fasciatus (deciduous wood)
(Ehnström and Axelsson 2002). The common species were recorded in order to obtain a
basis of comparison for habitat associations and changes in occupancy of the more poorly
known threatened species. Population sizes may vary over time, both due to long-term
trends and annual variation in weather, thus validity of any observed changes in occupancy
of the threatened species would benefit from a comparison to a larger number of species.
We recorded only larval stage of U. ceramboides because the adult beetles do not live
under bark and can only rarely be observed. Both larvae and adults of P. minus live in dead
wood, however, only adults can be recorded reliably, since the larvae are very small and
could not be identified in the field. In 2010, P. minus was also included as a main study
species, as it is red-listed and seemed to depend on similar habitats as U. ceramboides. The
aim of the second survey was, in addition to habitat analyses as in 2004, to also study
events of colonisation and extinction in relation to habitat characteristics.
The surveys were carried out from middle of May to beginning of July. Dead wood of
birch (cut logs and fallen trees) was searched for larvae of U. ceramboides and adults of P.
minus by peeling off 0.25 m2 of bark per substrate and noting species presence/absence
(see Table 1 for total number of substrates). In 2004, number of searched substrates per
clearcut depended on dead wood availability and reached a maximum of 47 objects. In
2010, up to twenty substrates per harvested stand (one clearcut could contain several
stands) were searched for beetles. If fewer suitable objects were available, all were surveyed. Only objects with diameter [5 cm and length [1 m with intact bark were included
in the survey, as smaller objects were unlikely to be suitable for larval development. Also,
objects of decay class 1 or 6 were considered to be unsuitable for the species, based on
previous ecological knowledge. Such objects were only searched in occasions when no
other substrates were available. The search was stopped on the particular clearcut when
both main species were encountered, because the search method is destructive for species
habitat.
Habitat characteristics
Species presence/absence was related to habitat characteristics on two spatial scales,
clearcut level and substrate level. For each clearcut, data on habitat characteristics were
obtained from the forest company (age and area) or estimated in the field (amount of dead
birch wood). Connectivity was calculated for each clearcut by accounting for distance to
occupied clearcuts in the surroundings and their habitat amount. Geographic coordinates of
each clearcut were included in analyses to account for spatial North–South and East–West
patterns. Colonisation and extinction events were observed by comparing the occurrence
data from 2004 and 2010. As P. minus was not the main focus of the first survey, we could
only be confident about colonisations of new clearcuts (created after the first survey).
Clearcuts present in 2004 were therefore excluded from analyses.
Clearcut level
Clearcut age (time since clearcutting) was divided into categories prior to analysis, in order
to better assess non-linear species response to age. We chose an assignment that gave the
most similar number of clearcuts per category, resulting in a slightly different grouping for
2004 and 2010 (Table 2).
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Table 2 Habitat characteristics, measured for each clearcut; variables measured in two or more classes
were analysed as categories
Variable
Units and description
Area
ha (sum for contiguous clearcuts)
Age
Years since clearcutting (average for contiguous clearcuts) Divided in classes for
analyses; 2004: 1 = 3–6 years, 2 = 7 years, 3 = 8–9 years, 4 = 10–14 years;
2010: 1 = 3–4 years, 2 = 5–8 years, 3 = 9–11 years, 4 = 12–14 years,
5 = 14–20 years
Burned
Clearcut burned (1) or not (0)
South-North
Geographic coordinates (m) for location of each clearcut
West-East
Geographic coordinates (m) for location of each clearcut
Connectivity
Calculated according to Eq. 1
Nr birch
Number of dead birch substrates ha-1 (measured 2004)
Area birch
Area on clearcut with dead birch wood present (ha) (2010)
Density birch
Maximum aggregation density of dead birch wood (m3 ha-1) (2010)
The amount of dead birch wood per clearcut in 2004 was estimated as number of
substrates ha-1 in 10 9 50 m transects in the most substrate-rich parts of the clearcut
(Fig. 1). Two or three transects per clearcut (depending on area) were placed in parts of the
clearcut with the highest density of birch dead wood (Fig. 1a). Number of substrates ha-1
was calculated from the transect data and the highest value used in analysis.
The amount of dead birch wood on clearcut level was estimated with two different
proxies in 2010. First, we estimated the clearcut area where dead birch wood was present,
i.e. habitat area for the species. Second, we estimated the maximum aggregation density of
substrate for each clearcut. Area with dead wood was estimated by walking all over the
clearcut and counting 25 9 25 m squares where dead birch substrate with a diameter
C5 cm of totally C3 m in length was present, i.e. a minimum density of 0.4 m3 ha-1
(Fig. 1b). The counting was done in a way that minimises the number of squares, e.g. two
objects 20 m apart made up one, not two squares. The number of habitat squares was
summed for each clearcut and recalculated into hectares of habitat area. Aggregation
density was estimated in 10 9 10 m squares (1–3 per clearcut) in areas with the highest
dead wood density (Fig. 1c). Diameter and length of all objects was measured within the
squares and the total volume calculated. If a part of an object lay outside the square, only
the part within the square was included. The volume of the square with highest density was
used to calculate volume ha-1.
Substrate level
Effect of substrate properties and dead wood aggregation on U. ceramboides was studied in
detail on three clearcuts which had the highest amounts of dead wood and highest species
frequency in 2004. To test if U. ceramboides benefit from aggregation of dead wood (as
spatial distribution of dead wood may be important for saproxylic beetles: Schiegg 2000),
total volume of all birch substrates within four transects (10 9 50 m) on each clearcut was
calculated. Between 10 and 24 substrates per transect were searched for beetles. Substrate
properties, such as decay class, size, presence of fungi, etc. were measured and related to
species presence/absence for each investigated object (Table 3).
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455
Fig. 1 Dead wood survey
methods: a Nr Birch 2004,
b Area Birch 2010 and c Density
Birch 2010. The larger rectangles
represent clearcuts, the smaller
squares or rectangles are sample
plots and the black dots are dead
wood objects
In 2010, in order to gain a better understanding of species habitat use across the
landscape, species-substrate associations were studied on all clearcuts for both U. ceramboides and P. minus. Decay stage was recorded at several positions for large dead
wood objects and the average calculated, resulting in a continuous variable used in analyses. We also recorded if a substrate was in direct contact with another dead wood object (a
measure of small-scale aggregation), whether it was burned and whether it was an intact
fallen tree, i.e. trees likely retained for conservation purpose, not logging residues
(Table 3). Burning was included as a factor in the analyses on both clearcut and substrate
levels, as many saproxylic beetles are more frequent in burned wood (e.g., Hyvärinen et al.
2009). 95 burned substrates were surveyed in 2010 on five burned clearcuts.
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Table 3 Substrate characteristics, measured for each investigated dead wood object
Variable
Units and description
Length
m
Diameter
cm
Decay class (1–6)
1: fresh wood to 6: highly decomposed wood (scale according to Siitonen and
Saaristo 2000); treated as continuous variable in 2010
Bark cover (%)
Proportion of object with bark (used to calculate bark area)
Sun exposure (1–3)
1: completely open, 2: predominantly open, 3: partially shaded
Ground contact (1–4)
Proportion of object in direct contact with the ground: 1 = \25 %,
2 = 25–50 %, 3 = 50–75 %, 4 = [75 %
White-rot fungi
2004: presence (1)/absence (0) of fruiting bodies (F. fomentarius, Trametes
zonatella, T. hirsuta); 2010: mycelium in wood, living (1) or dead (0)
Burned
Object burned (1) or not (0); there were no burned objects in 2004
Additional variables 2010
Contact
Object in contact with other object (1) or not (0)
Intact tree
Downed intact tree (1) or cut fragment (0)
Variables measured as two or more classes were analysed as categories
Connectivity
We estimated connectivity (S) for each clearcut i in 2004 and 2010 using the following
equation:
Si ¼
n
X
j¼1
expð$a dij Þpj Hj ;
for all j 6¼ i
ð1Þ
where dij = distance between clearcut i and j; n = total number of clear-cuts (including
those not surveyed); p = species presence, with p = 1 at species presence, p = 0 at
species absence and p = average probability of occurrence in the landscape, when species
had not been surveyed; Hj = habitat amount in clearcut j; and a is a parameter controlling
the rate with which the frequency of dispersal events, or correlation between probability of
occurrence, decrease with distance. We used the negative exponential function, because it
has been found to fit rather well with dispersal patterns of animal species (Moilanen and
Nieminen 2002). We identified the scale that generated the minimum residual deviance for
the total statistical model by graphically comparing spatial scales (i.e. 1/a, in whole
meters) within an interval from 10–10,000 m. As an estimate of habitat amount, we used
the measure of dead birch wood which best explained species presence (‘‘Nr birch’’ in
2004, ‘‘Area birch’’ for U. ceramboides and ‘‘Density birch’’ for P. minus in 2010).
We obtained two different measures of connectivity for 2010 occurrence models, by
using data on habitat (dead wood) amount of occupied sites (Hj and p in Eq. 1) either from
2004 or 2010. Data that resulted in a better model fit were used in final analysis (Table 5).
The past habitat amount may better relate to occupancy if the species respond slowly to
changes in the landscape. To make the connectivity measures from the periphery of the
study area comparable with the centre, we took into account presumable occurrences of P.
minus outside the study area by creating a 2 km buffer zone around the study area and
including clearcuts in the buffer in the connectivity calculation. We assumed the same
frequency of species occurrence and dead wood amounts as within the landscape, so all
added clearcuts were given the average value for probability of occurrence and for dead
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457
wood amount. This was also done for the clearcuts within the landscape not surveyed in
2004 (both species). Due to the size of buffer, we used a 2 km distance limit (i.e. if
dij [ 2 km the clearcut j did not add to the connectivity in Eq. 1) for when calculating
connectivity for every clearcut.
Connectivity for U. ceramboides was calculated to all clearcuts within the landscape,
irrespective of distance. We assumed that U. ceramboides was absent from the buffer area.
The species has been searched for and has not been found outside the study area in
thorough surveys of the landscape by L. Wikars in 2003 and Olof Hedgren in 2009
(unpubl. data). It is therefore likely that the species was absent from the nearest surrounding landscape. In 2010, the species frequency in the landscape was so low that the
connectivity estimates would not be significantly affected by adding additional buffer area,
while in 2004 it might have some effect.
Analyses
All analyses were conducted in R version 2.14.0 (R Core Team 2012), using package lme4
(Bates et al. 2011). Continuous explanatory variables (clearcut level analyses) were logtransformed prior to analyses to improve skew distributions and minimise impact of
extreme values. To avoid multicollinearity, we calculated variation inflation factors (VIF)
for all models. Variables with VIF [3 were excluded from the models (Zuur et al. 2010);
this was ‘‘bark area’’ (correlated with length and diameter) on substrate level 2010.
Species presence/absence per clearcut was analysed with multiple logistic regression
(glm in R), with habitat characteristics and connectivity as explanatory variables (Table 2).
The model with the lowest AIC (Akaike information criterion) value was considered to
provide the best explanation of the data. We used backward elimination—all variables and
biologically relevant interactions were included in the initial model, then variables that
gave the largest decrease in AIC were dropped one at a time, until a model with the lowest
AIC was reached. Events of colonisation and extinction between the surveys were also
analyzed in relation to habitat characteristics in 2010. To test whether occupancy had
changed between 2004 and 2010, we used a generalised linear mixed effects model (glmer
in R), with survey year as a fixed categorical factor and clearcut identity as a random
factor.
Species presence/absence per substrate in 2004 (3 clearcuts, 231 substrates) was analyzed in relation to substrate properties (Table 3) and dead wood amount per transect with
a generalised linear mixed effects model (glmer). Clearcut identity and transect identity
were included as nested random factors. Due to many possible interactions, the models
were built by forward selection, i.e. adding one variable at a time, starting with the variable
that gave lowest AIC, until adding more variables no longer decreased AIC. Species
presence/absence on substrate level 2010 (110 clearcuts, 898 substrates) was analysed
similarly, with clearcut identity as random factor. The quadratic term of the decay class in
2010 was tested to account for non-linear response.
Results
Landscape level
We observed different trends in occupancy per clearcut for the two study species. Upis
ceramboides showed a decrease from 29 % in 2004 to 7 % in 2010 (glmer:
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Platysoma minus
Upis ceramboides
Absence
Presence 2004
Presence 2004+2010
Presence 2010
Fig. 2 Presence/absence of U. ceramboides (a) and P. minus (b) in the studied landscape, size 20 9 20 km
Table 4 Species occupancy per clearcut (%), colonisation (Col) and extinction (Ext) rates as % of all
clearcuts where colonisation/extinction was possible; colonisations if only new clearcuts are considered in
parentheses
Species
Occupancy
Col
Ext
2004
2010
U. ceramboides
31
7
3
70
P. minus
32
60
62 (60)
57
R. mordax
54
38
36 (39)
63
T. fasciatus
48
55
48 (45)
37
The two other species, R. mordax and T. fasciatus, are shown for comparison
coefficientyear = -9.82; p = 0.057; Fig. 2; Table 4), while P. minus increased its occupancy from 30 to 60 % (glmer: coefficientyear = 1.17, p \ 0.001; Fig. 2; Table 4). In
comparison to the common species R. mordax and T. fasciatus, we observed very few
colonisations and many extinctions of U. ceramboides. Clearcuts with required habitat
amount for this species appears to be rare, as more than 90 % of all surveyed clearcuts had
low amounts of dead birch wood (‘‘Area birch’’) and consequently low species occupancy
(Fig. 3).
Clearcut level
On clearcut level, occurrence of both species depended mainly on the habitat amount (dead
wood) and clearcut age (Table 5; Fig 4). The frequency of U. ceramboides increased with
the number of substrates (2004) and area with dead wood (2010), while dead wood
aggregation density had strongest effect on the probability of occurrence of P. minus. Upis
ceramboides was most frequent 8–9 years after clearcutting, while P. minus occurred most
frequently on older clearcuts (12–14 years). Connectivity did not predict presence/absence
for any of the species. However, the geographical gradients were important for P. minus,
with higher probability of occurrence and colonisation towards the northern part of the
landscape (Table 5). Also, we found no effect of burning on species occurrence. Exinctions
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0.7
Frequency
Fig. 3 Relationship between
area with birch dead wood per
clearcut and (i) occupancy of
U. ceramboides (grey columns),
and (ii) proportion of all clearcuts
in the landscape in 2010 (black
columns). Of all existing
clearcuts, \10 % have the
amount of habitat needed to
achieve a high occupancy of
U. ceramboides
459
0.6
clearcuts
0.5
U. ceramboides
0.4
0.3
0.2
0.1
0
<1
1-2
2-3
>3
Area with dead wood/clearcut (ha)
Table 5 Final logistic regression models explaining species presence/absence on clearcut level
Independent
variable
U. ceramboides
P. minus
2004
2010
P. minus
a
2010
Col
P. minus
Ext
Area
–
–
–
–
-4.02
Age cat 2
3.46*
–
-0.97
-0.81
–
Age cat 3
4.69*
–
1.42
1.95#
–
#
Age cat 4
4.52*
–
1.83
na
–
Age cat 5
na
–
0.49
na
–
Nr Birch
7.92**
na
na
na
na
Area Birch
na
6.5*
4.04*
3.57#
-18.1#
Density Birch
na
–
2.15**
–
1.82#
–
1.8 9 10 **
1.9 9 10-4*
–
-4
South-North
–
West-East
-1.5 9 10-4#
–
–
–
–
Presence 2004
na
3.04**
-1.75*
na
na
Connectivity
29.8
–
-0.95#
-3.15#
na
a (Eq. 1)
20
–
480
20
na
Hj (Eq. 1)
Nr Birch
–
Nr Birch
Density Birch
na
Explained variation
60 %
33 %
29 %
25 %
47 %
‘‘na’’ indicates that the factor was not measured/tested and ‘‘–’’ that the factor was tested but not a part of the
final model. Age category 1 was reference category. Coefficients and significance codes (#0.1 \ p \0.05,
*0.05 \ p\0.01, **0.01 \ p \0.001, *** p \ 0.001) are shown. Connectivity was excluded from the
model for U. ceramboides in 2010 due to too few species occurrences
a
colonisations of sites inventoried 2004 were not included in the analyses
of U. ceramboides could not be explained by any habitat property (adding habitat variables
gave no improvement in AIC compared to intercept-only model). Due to only three
observed colonisations by U. ceramboides, no meaningful analysis could be done.
Substrate level
An important factor determining species presence/absence on substrate level was wood
decay class. Platysoma minus was frequent in far decayed wood, while U. ceramboides
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R. mordax
R. mordax
10
50
Occupancy (%)
Occupancy (%)
60
40
30
20
10
0
3-6
7-10
11-14
8
6
4
2
0
15-20
2
Clearcut age (years)
U. ceramboides
Occupancy (%)
Occupancy (%)
30
20
10
3-6
7-10
8
4
0
11-14
2
3
P. minus
Occupancy (%)
Occupancy (%)
30
60
40
20
3-6
7-10
11-14
20
10
0
15-20
2
Occupancy (%)
Occupancy (%)
30
40
20
3-6
7-10
11-14
15-20
Clearcut age (years)
3
4
5
Substrate decay class
T. fasciatus
60
0
5
P. minus
Clearcut age (years)
80
4
Substrate decay class
80
0
5
12
Clearcut age (years)
100
4
U. ceramboides
16
40
0
3
Substrate decay class
T. fasciatus
20
10
0
2
3
4
5
Substrate decay class
Fig. 4 Occupancy per clearcut and per dead wood object (%) of four beetle species on clearcuts of different
age and in substrates of different decay stage in 2010 (except U. ceramboides, for which 2004 data were
used), illustrating patterns of succession
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461
Table 6 Final models explaining species presence/absence on substrate level
Variable
U. ceramboides
2004
P. minus
2010
2010
Diameter
–
–
0.06***
Bark area
0.47
na
na
Birch vol/transect
5.63**
na
na
Decay class*
na
–
0.82***
Decay class 3
1.47*
na
na
Decay class 4
0.16
na
na
Decay class 5
-0.71
na
na
Decay class 6
-14.9
na
na
White rot
1.77**
na
na
Contact
na
2.25#
–
Intact tree
na
2.1#
1.04***
‘‘na’’ indicates that the factor was not measured/tested and ‘‘–’’ that the factor was tested but not part of the final
model. Decay class 2 was reference category; *continuous variable for decay class used in 2010. Coefficients and
significance codes (#0.1 \ p \0.05, *0.05 \ p \0.01, **0.01 \ p \0.001, ***p \ 0.001) are shown
was associated with intermediate decay stages (Fig. 4; Table 6). Platysoma minus was
strongly associated with large-diameter dead wood objects. Both species were more frequent in intact trees compared to cut wood like tops, branches and stem fragments.
Occupancy of U. ceramboides per substrate increased if substrates were aggregated within
clearcuts (Volume/transect, 2004; Table 6) and in direct contact with other substrates
(Contact 2010; Table 6).
Discussion
We show that clearcuts in managed forest landscapes constitute important habitat for earlysuccessional forest species. We have observed that species track the dynamics of their
habitat—they colonise clearcuts, remain during the time when conditions are suitable and
go locally extinct as forest and dead wood succession proceeds. During the open-habitat
stage of clearcuts, there is a species succession driven by the decay of dead wood (Fig. 4).
For the species of this study, amount and quality of dead wood is important, and that is
strongly affected by forestry operations. The observed occurrence patterns and changes in
occupancy of P. minus were clearly associated with habitat dynamics on landscape scale,
as we predicted. The species effectively colonised newly established habitats with suitable
properties (age, dead wood amount). The observed decline of U. ceramboides, however,
cannot be attributed to habitat succession on landscape scale.
Occupancy changes in the landscape
We observed different occupancy patterns over time for the main study species; U. ceramboides decreased in occupancy while P. minus showed a strong increase between 2004
and 2010. It is difficult to determine whether the observed changes are long-term trends or
caused by annual fluctuations of population sizes. However, the long development time of
U. ceramboides (Pettersson and Ehnström 2010) should reduce large fluctuations in the
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larval population. This suggests that the population of U. ceramboides is indeed
decreasing, which is consistent with the long-term decrease of the distribution area for this
species in Sweden (Gärdenfors 2010).
The low number of occurrences and colonisations by U. ceramboides (Table 4) is a
strong indication that the species is at risk of extinction in the studied landscape. Many
apparently suitable clearcuts were not occupied, e.g. 49 % of the clearcuts were of the
most suitable age (8–9 years) and 43 % of the substrates were of the most suitable decay
stage (suitability according to Fig. 4). Even among clearcuts with the highest amounts of
dead wood, less than 40 % were occupied (Fig. 3). Intensified forest management during
the last century has resulted in, among other, decreased abundance of old and large
deciduous trees, and it is likely that this has caused a decline of U. ceramboides. Species
usually track changes in habitat amount with a time lag, resulting in an extinction debt in
recently fragmented or degraded landscapes (Hanski and Ovaskainen 2002). It has been
estimated that in Finland, which has rather similar conditions to central and northern
Sweden, about 1000 species constitute an extinction debt, which in the long run will go
regionally extinct unless habitat is restored (Hanski 2000). Species that are specialised on
a very particular type of habitat, like U. ceramboides, can be expected to suffer earlier
than more generalistic species (e.g. Henle et al. 2004). In this study we used R. mordax
and T. fasciatus as more generalistic species for comparison, since they occur in forest of
various successional stages and can use dead wood of other tree species. Occupancy of
these species appears quite stable (Table 4), suggesting that habitat amount in the
landscape is sufficient for successful reproduction and colonisation by common generalist
species.
Rather surprisingly, P. minus increased its occupancy in the landscape, despite that it is
a red-listed species and generally thought to be negatively affected by forest management.
On the one hand, this may be because it is a predator species and is therefore not directly
dependent on dead wood quality, but indirectly through prey abundance. On the other
hand, predatory species belong to a higher trophic level than consumers and might thereby
be more sensitive to habitat loss or degradation (Davies et al. 2000). Platysoma minus
appears to be colonising newly established clearcuts throughout the landscape. The high
frequency of colonisation for P. minus, which was independent on connectivity, indicates
that the species is not dispersal limited and highly mobile on landscape level. We could not
explain extinction rates with clearcut age for any of the species, likely because clearcuts
that were old enough ([20 years) were by intention not surveyed. However, extinction of
early-successional species could be expected to occur in old clearcuts with high shading
and most of the dead wood decayed.
Unexpectedly, we did not find a significant effect of connectivity on species occurrence.
However, Hodgson et al. (2009) have shown that although connectivity affects colonisation
and is consequently important for persistence of a species, effect of connectivity on
occupancy might not be apparent in short-lived habitats. Other studies have found that
connectivity is indeed important for colonisation of saproxylic beetles in short-lived dead
wood objects (e.g. Ranius et al. 2011), including a species inhabiting high-stumps on
clearcuts (Schroeder et al. 2006). In accordance with our study, Sahlin and Schroeder (2010)
found that habitat patch size, but not connectivity, increased saproxylic beetle occupancy
per dead wood object. Generally, the amount and quality of breeding habitats are relatively
more important for species persistence than the habitat spatial arrangement (Hodgson et al.
2011). Nevertheless, we found higher occurrence and colonisation of P. minus towards the
north of the landscape (Table 5). This geographical pattern may be due to variation in forest
history, i.e. that modern forestry started later in the north of the study landscape.
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463
Clearcut quality
We have shown that different species that share the same post-disturbance habitat are
associated with somewhat different stages of clearcut age and dead wood decay (Fig 4).
The main part of the dead wood is created during harvesting, and more dead wood is
supplied by death of retained living trees during the following years. Thereby, dead wood
of various decay stages can be found on young as well as old clearcuts (in our data, clearcut
age and average substrate decay stage are moderately correlated, Pearson correlation
coefficient = 0.55). This makes it possible for early-successional species to use the habitats over longer period of time, provided that the dead wood stays sun-exposed. However,
planting of conifers shortens the time of sun-exposed conditions on clearcuts. This affects
less species which use dead wood of early decay stages, e.g. the Rhagium species, but for
many species adapted to sun-exposed dead wood of intermediate or late decay stages,
conditions within the dense young stands are probably poor.
Upis ceramboides and P. minus represent a species community that has historically been
favoured by forest fires. In this study, the species were not more frequent in burned wood
and on burned clearcuts compared to unburned clearcuts. Our results are in accordance
with earlier findings that most early-successional species do not need fire or burned wood
itself, but a habitat with sufficient amounts and diversity of sun-exposed dead wood (Kaila
et al.1997; Johansson et al. 2007). Positive effect of burning on saproxylic beetles has been
found by Toivanen and Kotiaho (2007) and Hyvärinen et al. (2009). The effect was,
however, only studied early in succession (1–2 years after burning). Both U. ceramboides
and P. minus colonise clearcuts several years after the disturbance, and such species might
not respond strongly to burning.
Dead wood quality and aggregation
Our results show that whole dead trees were more frequently occupied by P. minus and U.
ceramboides than cut logs and fragments. This may be because the time-window for
possible use by beetles is longer in an intact tree, because it contains parts of a variety of
dimensions, with a faster decay in small-diameter parts compared to the stem. Also, the
dead wood created during harvesting might be of lower quality compared to naturally
down trees, e.g. because of size difference and bark damage (mean bark area 6.4 m2 per
whole tree, compared to 1.6 m2 for other substrates). Importance of large diameter trees
that supply high-quality substrate for rare beetles has been shown by Similä et al. (2003).
Large-diameter dead wood present before harvesting is often damaged and fragmented by
machinery (Hautala et al. 2004). Bark-free dead wood is useless to the studied species.
Therefore, the best habitat for P. minus and U. ceramboides is provided when retained
green trees of birch die soon after clearcutting.
Occupancy of both species increased when substrate was aggregated within clearcuts,
but on different scales. Upis ceramboides appeared to benefit from high densities of birch
wood on substrate level in 2004. Also in 2010, the species was more frequent in substrates
in direct contact with other dead wood objects. Occurrence probability of P. minus
increased with a higher wood aggregation density on clearcut level. Also in an earlier
study, a positive effect of small-scaled aggregation of dead wood on diversity of saproxylic
insects has been suggested (Schiegg 2000). We can merely speculate about the underlying
mechanisms behind these observations; possibilities include species movement behaviour
(e.g. walking rather than flying between substrates) and search behaviour during dispersal.
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The observed patterns nevertheless suggest that substrates close to each other are more
valuable for biodiversity than evenly dispersed substrates.
Conservation and management implications
Current reserve networks are dominated by old-growth forests and have limited benefit for
early-successional species, if natural disturbances are not reintroduced. Protection in
reserves should, therefore, be complemented with improved habitats in surrounding
managed landscapes (Kouki et al. 2001; Franklin and Lindenmayer 2009; Kuuluvainen
2009). Clearcuts and young forests with retention in landscapes dominated by dense
managed forest have high potential for conservation of disturbance-favoured species
(Kouki et al. 2001; Lundström et al. 2011), since high quality early-successional stages can
be created with relatively low cost and little effort compared to, e.g., burning protected
mature forest to create early-successional habitats. However, there is a need to a larger
extent restore natural forest characteristics, e.g. number of large living trees and volume
and diversity of dead wood (Similä et al. 2002, Similä et al. 2003). By applying appropriate
management, the population size of threatened species can indeed increase even in managed forests (Djupström et al. 2012).
Importance of green-tree and dead wood retention at clearcutting is highlighted by our
finding that species are more frequent in naturally created dead wood than in wood from
the clearcutting (Table 6). Creation of dead wood should be done by cutting or injuring
whole trees after soil preparation to avoid damage from machinery. Already existing and
newly created dead wood could be aggregated in some parts of each clearcut and avoided
during soil preparation, e.g. along edges of retention groups of living trees. Trees that are
retained alive will provide substrate in the future. Living trees may also to some extent
locally set back regeneration of the new stand (Jacobsson and Elfving 2004), whereby dead
wood close to living trees stays sun-exposed for a longer period. In combination with
allowing natural regeneration instead of planting in these aggregations, the time when
natural-like early-successional conditions prevail on parts of clearcuts could be prolonged.
Any other measures that delay densification of young stands, such as pre-commercial
thinning, would also be beneficial.
To ensure a continuous supply of habitat for our study species, which depend on
deciduous wood in conifer-dominated landscapes, landscape scale planning of living tree
and dead wood retention in forest management is essential. The specialised species U.
ceramboides occupies only clearcuts with the highest amounts of dead wood, and the
current amount of such habitat is low on landscape level (Fig 3). Therefore, instead of
retaining dead wood of different tree species on each clearcut, it is better to focus on one tree
species per clearcut, given the volume of wood to be retained is constant. This applies even
to retention on landscape scale, as concentrating efforts to improve habitat quality to some
areas is more useful for threatened species compared to spreading them out evenly but thinly
over an entire forest landscape (Hanski 2000). Many dead-wood associated forest species
can successfully use natural early-successional habitats (Kouki et al. 2001). Thus, creating
networks of natural-like early-successional habitats of high quality in managed forest
landscapes may substantially counteract the loss of biodiversity from such landscapes.
Acknowledgments We thank Martin Schroeder for advice during project planning and together with the
Smart Tree Retention research group for useful discussion and comments on the manuscript, and Mikael
Andersson for statistical support. Also, thanks to Carola Orrmalm for sharing data from her project and Lisa
Karlsson for assistance with field work. This research was funded by the Swedish Research Council Program
FORMAS (grant no. 215-2009-569 and 215-2008-539).
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