Forest Ecology and Management 337 (2015) 41–47
Contents lists available at ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
Guild-specific responses of forest Lepidoptera highlight
conservation-oriented forest management – Implications
from conifer-dominated forests
Simon Thorn a,b,⇑, Hermann H. Hacker c, Sebastian Seibold a,b, Hans Jehl a, Claus Bässler a, Jörg Müller a,b
a
b
c
Bavarian Forest National Park, Freyunger Str. 2, 94481 Grafenau, Germany
Terrestrial Ecology, Department of Ecology and Ecosystem Management, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany
Bavarian State Collection of Zoology, Munich, Germany
a r t i c l e
i n f o
Article history:
Received 19 August 2014
Received in revised form 29 October 2014
Accepted 31 October 2014
Available online 20 November 2014
Keywords:
Natural disturbance
Ips typographus
Multi-layered forest stand
Single-layered forest stand
Salvage logging
Red list
a b s t r a c t
The loss of biodiversity in forest ecosystems has led to a discussion on conservation-oriented forest management, particularly in intensively managed coniferous forest of the northern hemisphere. Two conservation-oriented management strategies, namely advancement of multi-layered forests stands and benign
neglect of naturally disturbed stands, are currently being promoted over conventional management strategies of single-layered stands and salvage logging after natural disturbances. However, the effect of these
conservation-oriented strategies on nocturnal Lepidoptera has not yet been assessed, despite the high
contribution of this order to biodiversity. Here we used full assemblage data of forest-dwelling micromoths and macro-moths to compare species densities and relative abundance of moths of the larval feeding guilds in single-layered and multi-layered stands, and in naturally disturbed salvaged or unsalvaged
stands. We demonstrate that forest moth assemblages are sensitive to conservation-oriented forest management strategies. The relative abundance of moths of the saproxylic and detritus-feeding larval guilds
was higher in naturally disturbed unsalvaged stands and in multi-layered stands, whereas that of moths
of the moss-feeding larval guild was lower in multi-layered stands. These results corroborate the benefit
of a benign-neglect strategy in the management of naturally disturbed stands in conserving saproxylic
and detritus-feeding moths and in using natural disturbance to guide the enhancement of stand complexity. Our results demonstrate both the power of functional approaches to reveal slight changes in species
communities and the importance of including micro-moths (a frequently disregarded group) in studies
aimed at developing management implications for forest managers.
Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction
Key goals of conservation biology are to inform decision makers
of the identity of taxa of conservation concern and to develop
implications for the conservation of these taxa (Young, 2000). But
after the initial conservation strategies are defined, the efficacy of
these strategies for a broad range of taxa must be monitored and
evaluated (Hughey et al., 2003; Mansourian and Vallauri, 2014).
In this regard, it has to be considered that management implications for different focal taxa and conservation targets vary strongly
(Rost et al., 2013).
⇑ Corresponding author at: Bavarian Forest National Park, Freyunger Str. 2, 94481
Grafenau, Germany. Tel.: +49 8552 9600 179.
E-mail addresses: [email protected] (S. Thorn), hermann-heinrich.hacker@
t-online.de (H.H. Hacker), [email protected] (S. Seibold), hans.
[email protected] (H. Jehl), [email protected] (C. Bässler),
[email protected] (J. Müller).
http://dx.doi.org/10.1016/j.foreco.2014.10.031
0378-1127/Ó 2014 Elsevier B.V. All rights reserved.
Forest management has altered biodiversity of various taxonomic groups and across most forest biomes worldwide (Gardner
et al., 2009; Paillet et al., 2010). Over the past decades, controversial discussions of the ‘‘ifs and buts’’ of forest management in the
light of biodiversity conservation have risen (Donato et al., 2006;
Stokstad, 2006), and thus, a large variety of conservation-oriented
management strategies have been proposed (Götmark, 2013).
Among these strategies, particularly two are currently most often
promoted by conservationists for conifer-dominated forests of
the Northern Hemisphere. The first is a benign-neglect strategy
of forest stands naturally disturbed by fire, windthrow or insect
outbreaks (Angelstam, 1998; Lindenmayer et al., 2006). However,
despite increasing acknowledgement of the ecological values of
natural disturbances, salvage logging, i.e. the removal of fallen
and weakened trees, is still the most widespread strategy to mitigate economic losses (Burton, 2006; Lindenmayer et al., 2008;
Stadelmann et al., 2013). The second is the promotion of
42
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
horizontally and vertically heterogeneous, multi-layered forest
stands, which are assumed to be more natural and more resilient
against future disturbances (Carey, 2003; O’Hara et al., 2013;
Zenner et al., 2012). Nevertheless, most stands across a wide range
of temperate and boreal forests are single layered due to historical
silvicultural strategies and high economic efficiency (Nyland,
2003).
Considering the increasing probability of natural disturbance
events in the future (Seidl et al., 2014) and the ongoing loss of biodiversity (Butchart et al., 2010), rigorous evaluations of the effect
of the above-mentioned conservation-oriented forest management
strategies on multiple taxa are urgently needed. The often contrasting responses of different species to forest management can
make it difficult to identify an optimal management strategy
(Paillet et al., 2010). By focusing on functional guilds within a set
of studied species, species abundance patterns and particular forest management strategies can be directly linked (Kroll et al.,
2012). Such a detailed understanding of functional links combined
with well-defined conservation targets is a valuable basis to mitigate negative effects of forest management on biodiversity.
Among forest-dwelling arthropods, Lepidoptera are a highly
diverse group whose species richness has dramatically decreased
over the last decades (Franzén et al., 2007). Thus, this order of
insects has become important for developing management strategies in various ecosystems (Fartmann et al., 2013; Kerr et al., 2000;
Rickert et al., 2012). Because of the large number of different functional groups, forest moth assemblages are regarded as useful indicators of changes in forest structures (Kerr et al., 2001; Merckx
et al., 2012; Summerville and Crist, 2002) and forest disturbance
(Beck et al., 2002; Kitching et al., 2000; Summerville et al., 2004).
Here, we sampled full assemblages of micro-moths and macromoths in a spruce–beech mountain forest to compare species densities and relative abundance of the moths in single-layered and
multi-layered stands, and in salvaged and unsalvaged stands disturbed by bark beetles. To evaluate the efficacy of conservationoriented forest management strategies for coniferous forests in
central Europe, we considered the species densities and abundance
of red-listed and non-red-listed forest moths as well as larval
feeding guilds.
2. Methods
2.1. Study area and study design
The study was conducted in the Bavarian Forest National Park in
south-eastern Germany. In this low mountain range, annual precipitation ranges from 1,300 to 1,800 mm, and annual mean air temperature ranges from 3.0 to 4.0 °C (Bässler et al., 2010). Within
the last three decades, the European spruce bark beetle (Ips typographus, L.) extensively infested stands of Norway spruce (Picea
abies, Karst) and mixed stands of spruce, silver fir (Abies alba, MILL.)
and European beech (Fagus sylvatica, L.) at a maximum of 800 ha in
one year (Müller et al., 2008). Owing to a benign-neglect strategy in
the core zones of the national park, these infested stands remained
unsalvaged; in the extension zones, infested stands were salvage
logged. Unsalvaged stands are characterized by a dead-wood
amount of about 300 m3 ha 1 and an initial natural regeneration
of spruce and frequently Calamagrostis villosa (CHAIX EX VILL.)
and F. sylvatica. In contrast, salvaged stands are similar to clearcuts, but with more dead wood from logging residuals (stumps
and branches) at about 50 m3 ha 1. The three most common plant
species are P. abies, C. villosa and Vaccinium myrtillus (L.).
Due to forest history, mature stands are characterized by different levels of structural complexity, ranging from single-layered
stands to multi-layered stands. Single-layered stands are even
aged, dominated by mature spruces with mixtures of beech and
poor understory vegetation, frequently with Dryopteris dilatata
(HOFFM), and a standing stock similar to that of unsalvaged disturbed stands. In multi-layered stands, the most frequent plant
species are spruce, beech, and fir of all age and size classes. Overall,
we recorded 185 species of plants (for more characteristics see
Table 1). The highest species density per plot was found in unsalvaged stands (17 ± 8.85), followed by salvage-logged stands
(13.88 ± 6.7), multi-layered stands (12.5 ± 8.38), and single-layered
stands (9 ± 3.5).
In each of these four stand types, we selected eight plots in
structurally typical stands of at least 5 ha, distributed from 666
to 1,327 m a.s.l. For details and photos of all plot types, see Mehr
et al. (2012). The minimum distance between two plots of the
same forest type was 800 m, and the largest distance between
two plots was 30 km (Fig. 1). Selected plots of salvage-logged
stands were naturally disturbed and subsequently salvage logged
2–8 years before the study.
2.2. Moth sampling
Moths were sampled using light traps consisting of a 12 V, 15 W
super-actinic ultraviolet light tube mounted above a plastic funnel.
Attracted moths were collected in a plastic container at the bottom
of the trap and killed by chloroform (Müller et al., 2012). Since light
traps of the type used here attract moths within a radius of up to
50 m (Truxa and Fiedler, 2012), we placed traps in the centre of
the plot to optimally reflect the structure of the surrounding forest
stands. All specimens of micro-moths and macro-moths were identified by one of us, if necessary by examining genital preparations
(HHH, with support by an expert for micro-moths, see Acknowledgements). For literature and reference lists of moths in Bavaria,
see Hacker and Müller (2006).
To acquire complete assemblages of forest moths, we set up
traps for seven consecutive nights on each plot throughout the
whole vegetation period from early May (shortly after snow melt)
to mid-September in 2009, comprising a total of 224 individual
trap nights. Sampling was only conducted on frostless nights with
low wind speeds. A maximum of ten traps could be set per night;
thus, two to three plots of each forest type were sampled at the
same time. All plots were completely sampled within a maximum
of ten consecutive days. After sampling, we pooled the data from
all seven trap nights to the plot level. Each moth species was
assigned to one of six larval feeding guilds according to Hacker
and Müller (2006): ‘‘herbs and grasses’’, ‘‘detritus’’, ‘‘trees and
Table 1
Vegetation characteristics of study plots in the Bavarian Forest National Park. Presented are means and standard deviances.
Stand type
Salvaged
Unsalvaged
Single-layered
Multi-layered
Species richness
13.9 ± 6.7
17 ± 9.8
9 ± 3.5
12.5 ± 8.4
Total vegetation cover in percentage
Herb layer
Shrub layer
Tree layer (1–15 m)
Tree layer (>15 m)
68.6 ± 28.2
79.4 ± 21.8
25.6 ± 30.4
40.1 ± 40.1
12.9 ± 13.8
12.8 ± 14
5.1 ± 7
15.6 ± 22
23.9 ± 33.6
16.9 ± 24.1
75 ± 31.5
40.9 ± 36.7
6.9 ± 16.4
12.1 ± 13.9
13.8 ± 14.9
39.1 ± 33.2
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
43
Fig. 1. Spatial arrangement of study plots of salvaged and unsalvaged naturally disturbed stands, and single-layered and multi-layered stands within conifer-dominated
forests of the Bavarian Forest National Park (outlined in black) in central Europe (inset).
shrubs’’; ‘‘moss’’, ‘‘omnivores’’ and ‘‘saproxylic’’, whereas lichenfeeders where assigned to ‘‘saproxylic’’.
3. Results
3.1. Moth assemblages
2.3. Data analysis
All analyses were carried out in the statistical software R (R
Development Core Team, 2014). The moth data were generated
with a standardized sampling effort and therefore represent species densities but not species richness (Gotelli and Colwell,
2001). To control for the completeness of the moth species
recorded, we used an individual-based rarefaction approach to
estimate the rate of increase in species richness with increasing
number of trapped moth individuals (Colwell et al., 2012).
An index for illustrating moth response to forest disturbance is
the relationship of the abundance of Geometridae to that of Arctiidae plus Noctuidae per plot; relatively high values of the calculated
disturbance index reflect less-disturbed forests (Kitching et al.,
2000). We followed this approach and calculated a disturbance
index by dividing the 100-fold abundance of Geometridae per plot
by the pooled abundance of Arctiidae and Noctuidae per plot. To
model the effects of disturbance and silvicultural management,
we calculated generalized linear models with either abundance
(micro-moths and macro-moths pooled together and considered
separately), species density, disturbance index or relative abundance of moths of the various larval feeding guilds as response variable (Venables and Ripley, 2002). Since elevation can seriously
affect forest Lepidopteran assemblages, we included plot elevation
(m a.s.l.) as a covariable in our models (Highland et al., 2013). Abundance and species density were modelled using a Poisson distribution, and relative abundance of moths of the larval feeding guilds
was modelled with binomial distribution. To compare each of the
two management alternatives (salvaged/unsalvaged and multi-layered/single-layered), we calculated post hoc tests with adjusted
pairwise p-values using the function glht in the add-on package
multicomp (Hothorn et al., 2008). All models were repeated with
the standardized species richness, and results were similar.
We trapped 15,504 specimens for a total of 291 species of
macro-moths (12,791 specimens) and 137 species of micro-moths
(2713 specimens); 97 species were represented only by singletons.
Individual-based rarefaction indicated high sample completeness
for all forest stand types with exception of salvage-logged stands
Rarefaction curves with confidence intervals given by bootstrap
replicates (Fig. 2) revealed the highest standardized species richness on salvage-logged areas, and no difference between the other
three types of plots. Geometridae and Noctuidae were the most
abundant families of moths, representing more than half of the
trapped individuals (Fig. 3).
Fig. 2. Individual-based rarefaction (solid lines) and extrapolation (dotted lines, up
to twice the sample size actually taken) of forest moth species richness, along with
95% unconditional confidence intervals (grey shading).
44
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
Fig. 3. Total abundance of moth families and larval feeding guilds on salvaged and unsalvaged plots and on single-layered and multi-layered plots in the Bavarian Forest
National Park.
The disturbance index according to Kitching et al. (2000) was
significantly lower on naturally disturbed salvaged plots
(76.65 ± 54.03) than on naturally disturbed unsalvaged plots
(87.13 ± 33.83), which accounted for the higher similarity of naturally disturbed unsalvaged plots to both types of undisturbed forest plots. In contrast, we found no significant differences in the
disturbance index between multi-layered stands (129.74 ± 41.05)
and single-layered stands (134.02 ± 22.53), which indicated a similar relationship of the abundances of Geometridae to that of
Arctiidae plus Noctuidae in both forest types. The species density
of all moths together and that of red-listed moths considered separately did not significantly differ (mean species density per plot:
naturally disturbed salvaged, 69.75 ± 21.42; naturally disturbed
unsalvaged, 75.25 ± 38.54; single-layered stands, 96.75 ± 32.45;
multi-layered stands, 98.25 ± 33.19). Also, consideration of
micro-moths and macro-moths separately did not reveal significant differences. Within disturbed stands, unsalvaged plots hosted
significantly higher abundances of moths than salvaged plots. Differences between silvicultural managements (single-layered and
multi-layered stands) had no significant effect on moth abundance.
Total abundance of non-red-listed moths on naturally disturbed
salvaged plots and naturally disturbed unsalvaged plots differed
significantly; the relative abundances of red-listed moths were
higher in single-layered stands than in multi-layered stands
(Fig. 4). The plot elevation (m a.s.l., included as co-variable) had
a significantly negative effect on abundance and species density
of forest moths.
3.2. Guild composition
The most abundant moths were of the larval feeding guild that
depended on trees and shrubs (188 species; Fig. 3), followed by
moths of the guild that depended on herbs and grasses (140 species), the guild of omnivores (67 species), the guild of saproxylic
species (19 species), the guild feeding on detritus (10 species)
and the guild feeding on moss (4 species). Both silvicultural (single-layered and multi-layered stands) and disturbance management (salvaged and unsalvaged) had a strong significant effect on
the relative abundance of moths of several larval feeding guilds.
Moths of the saproxylic larval guild were relatively more abundant
on unsalvaged plots than on salvaged plots and in multi-layered
stands than in single-layered stands. Unsalvaged plots harboured
relatively more moths of the detritus-feeding larval guild than salvaged plots. The relative abundance of moths of the omnivorous
larval guild was significantly higher in multi-layered stands than
in single-layered stands, and the relative abundance of moths with
moss-feeding larvae was relatively more abundant in singlelayered stands than in multi-layered stands (Fig. 5).
4. Discussion
Fig. 4. Mean abundance of non-red-listed moths and red-listed moths on salvaged
naturally disturbed stands, unsalvaged naturally disturbed stands, single-layered
stands, and multi-layered stands based on 224 individual light-trapping nights in
the Bavarian Forest National Park (log scale).
Our study revealed higher overall abundances of moths in naturally disturbed unsalvaged forest stands than in naturally disturbed salvaged stands, but no significant effect of silvicultural
management aiming at multi-layered stands as compared to
single-layered stands. The abundance and species density of
red-listed moth species were not affected by either disturbance
or silvicultural managements. However, the standardized species
richness was highest on salvage-logged plots, which underlines
that mass effect (living and dead biomass) mainly drives higher
species richness in disturbed and unsalvaged stands and
undisturbed mature forest stands. In general, moth communities
in temperate forest ecosystems more likely respond to an alteration of environment or stand structure with a shift in abundance
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
45
Fig. 5. Dependence of t-values of the relative abundance of larval feeding guilds on disturbance and silvicultural managements provided by generalized linear models with
elevation as a co-variable based on light-trap catches in the Bavarian Forest National Park. Black bars on the right illustrate the abundance of trapped moth specimens within
specific guilds (log scale).
of subgroups than with a shift in species richness (Kitching et al.,
2000; Merckx et al., 2012; Summerville and Crist, 2005). Species
richness, in turn, is strongly governed by elevation and study season (Highland et al., 2013). Individual-based rarefaction and the
significant negative effect of plot elevation on abundance and species density in the present study confirmed these earlier findings.
Individual-based rarefaction reveals also relatively steep incline
of standardized species richness at our current sampling intensity
for salvaged stands. This effect could be caused by relatively small
attraction radii of light traps in open habitats (Merckx and Slade,
2014), which may biased the total sampled species densities. However, we focus our main analysis on relative abundance which is
unbiased by the total abundance.
Examinations of functional traits and guilds of birds (Kroll et al.,
2012) and saproxylic beetles (Thorn et al., 2014) have been
attested to provide a deeper understanding of assemblage response
to the management of naturally disturbed coniferous forests. Our
results of the contrasting response of moths of the different larval
feeding guilds confirmed these earlier conclusions. The relative
abundances of moth species whose larvae are dependent on dead
wood, including larval lichen feeders, were significantly higher in
naturally disturbed unsalvaged stands and multi-layered forests
than in naturally disturbed salvaged stands and single-layered forests. Moths with detritus-feeding larvae benefitted as well from
benign neglect of naturally disturbed stands, and the relative abundances of moths with omnivorous larvae were higher in multilayered forest stands than in single-layered stands. In contrast,
the relative abundances of moths with moss-feeding larvae were
significantly higher in single-layered forests.
4.1. Response of moths to post-disturbance management
In our study, salvaged and unsalvaged naturally disturbed
stands differed significantly in the relationship of the abundance
of Geometridae to that of Arctiidae plus Noctuidae, which indicated a shift in community composition. Considering the disturbance index of Kitching et al. (2000), moth assemblages on
unsalvaged naturally disturbed sites were more similar to assemblages of forest stands than to assemblages of salvaged naturally
disturbed sites. Although the value of Geometridae abundance as
an indicator of forest disturbance has been demonstrated (Beck
et al., 2002), investigations of indicators or subfamilies may not
reflect slight changes within the complete community or functional structure of forest moth assemblages (Hawksworth et al.,
2006). In general, dead-wood-dependent species are negatively
affected by intense forest management (Paillet et al., 2010). This
pattern is visible throughout larval feeding guilds of moth assemblages; for example, Summerville and Crist (2002) have found significantly lower species richness and of moths with fungi/lichen/
moss-feeding and detritus-feeding larvae in clear-cuts than in
unlogged or selectively logged stands in oak–hickory forests of
North America. Similarly, we found significantly higher relative
abundances of moths with saproxylic and detritus-feeding larvae
in unsalvaged forest stands killed by bark beetles. This increase
in relative abundance is probably governed by the generally higher
amount of dead wood on unsalvaged sites than on salvaged sites
(270 m3/ha vs. 70 m3/ha; Priewasser et al., 2013). Similarly, moths
with saproxylic and detritus-feeding larvae clearly benefit from
high resource amount on unsalvaged disturbed plots (see also
Fig. 2).
Besides the differences in the supply of dead wood, forest
stands affected by disturbance are characterized by lower canopy
closure and a shift in ground and shrub-layer vegetation communities compared to that of undisturbed stands (Lain et al., 2008). Canopy gaps created by bark beetle outbreaks in particular can
promote an extensive growth of European blueberry and hairy
reed grass in the early successional stages (Kirchner et al., 2011).
The increasing biomass of such herbaceous plants in turn promotes
the relative abundance of species such as riband wave (Idaea aversata, L., Geometridae) or grey pug (Eupithecia subfuscata, Haworth,
Geometridae), whose larvae feed polyphagously on dried or dead
leaves (detritivorous feeding guild).
4.2. Response of moths to silvicultural management
Coarse woody debris in spruce forests is independent of stand
structural characteristics but increases with amount and volume
of living trees (Motta et al., 2006). However, multi-layered stands
of coniferous trees often develop under the influence of natural
disturbance and canopy openings on local scales (Svoboda and
Pouska, 2008; Svoboda et al., 2012). Such canopy gaps in our study
area were created mainly by small and localized outbreaks of the
spruce bark beetle, and most of the resulting dead wood remained
in the stands (Müller et al., 2010). This natural stand development
and the resulting dead wood may account for relatively higher
abundances of moth species with saproxylic larvae in multilayered stands compared to that of single-layered stands. In turn,
a reduced canopy density enables the growth of European blueberries and non-spruce-dominated natural regeneration (Kirchner
et al., 2011), which are favourite feeding crops for the larvae of
the abundant omnivorous species in our study, e.g. the mottled
beauty (Alcis repandata, L., Geometridae).
46
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
In contrast to moth species with saproxylic or omnivorous larvae, which benefit from multi-layered stands, the abundance of
moths with moss-feeding larvae in multi-layered stands was significantly lower than in conventional, single-layered stands. This
result was surprising because species richness of mosses is higher
in less intensely managed forests and unsalvaged disturbed forests
(Bradbury, 2006; Ranius et al., 2014). However, the most abundant
species with moss-feeding larvae in our study was the micro-moth
Eudonia truncicolella STAINTON (Crambidae), which develops preferably within mosses in the basal trunk region of mature trees. This
microhabitat appears to be more frequent in single-layered stands,
which contain a higher number of mature trees per ha than multilayered stands and thus host higher numbers of moss feeders
(Bardat and Aubert, 2007; Motta et al., 2006; Schmalholz et al.,
2011).
In general, single-layered stands across Europe not only have an
even-aged tree layer but also tend to consist of a specific tree species, such as spruce in our study area, with only nominal admixtures of beeches (Carey, 2003; Nyland, 2003). Such pure
coniferous stands contain higher abundances of mosses and more
diverse moss communities than mixed or deciduous stands
(Ewald, 2000). Hence the lower relative abundance of moths with
moss-feeding larvae in our study could likewise be caused indirectly by considerable proportions of beech in the multi-layered
stands.
4.3. Implications for forest management and conservation
Although a benign-neglect strategy of naturally disturbed forest
stands began decades ago (Angelstam, 1998; Lindenmayer et al.,
2006), salvage logging is still the most widespread strategy to mitigate economic losses (Lindenmayer et al., 2008). Our study
focused on a diverse, but mostly phytophagous group of insects
not associated with dead wood, and the results again justify a
benign-neglect strategy in conserving forest moths of the saproxylic and detritus-feeding larval guilds. Hence, naturally disturbed
forest stands should not be salvaged, particularly in protected
areas, to warrant natural succession accompanied by specific species assemblages (Lehnert et al., 2013; Müller et al., 2008).
Our comparison of multi-layered forest stands and singlelayered forest stands revealed a contrasting response of moths of
the saproxylic/detritus-feeding larval guild and moths of the
moss-feeding guild. This suggests that a mixture of both stands
types should be promoted at the landscape level to conserve the
functional guild diversity of forest moths. Earlier results have
confirmed the importance of mature old trees in general, which
provide also suitable habitats for epiphytic mosses, within multilayered stands (Lindenmayer et al., 2012). A feasible management
approach of providing both single-layered and multi-layers stand
types would be allowing natural disturbances in single-layered
stands to form sections of multi-layered stands.
5. Conclusions
Larval feeding guilds of forest moth assemblages were found to
be sensitive to silvicultural management and post-disturbance
management, but without detectable changes in species richness.
However, standardized species richness was highest on salvagelogged plots, which accounted for the mass effect of larval food
resources in unsalvaged naturally disturbed stands and mature forest stands. However, abundances of moths of the saproxylic larval
guild tended to be higher in unsalvaged naturally disturbed stands
than in salvage-logged naturally disturbed stands. Our functional
approaches detected slight changes in functional guild composition of forest moth assemblages, including often disregarded
micro-moths. Based on our results, we endorse the benign-neglect
strategy of naturally disturbed forest stands to support moths of
the saproxylic and detritus-feeding larval guilds and to develop
multi-layered stands.
Acknowledgements
S.T. and S.S. were financially supported by the Scholarship
Programme of the German Federal Environmental Foundation.
We thank Milenka Mehr for field work and Karen A. Brune for
linguistic revision. We thank Georg Derra for the identificaton of
numerous micro-moths.
References
Angelstam, P.K., 1998. Maintaining and restoring biodiversity in European boreal
forests by developing natural disturbance regimes. J. Veg. Sci. 9, 593–602.
Bardat, J., Aubert, M., 2007. Impact of forest management on the diversity of
corticolous bryophyte assemblages in temperate forests. Biol. Conserv. 139, 47–
66.
Bässler, C., Müller, J., Dziock, F., 2010. Detection of climate-sensitive zones and
identification of climate change indicators: a case study from the Bavarian
Forest National Park. Folia Geobot. 45, 163–182.
Beck, J.A.N., Schulze, C.H., Linsenmair, K.E., Fiedler, K., 2002. From forest to
farmland: diversity of geometrid moths along two habitat gradients on
Borneo. J. Trop. Ecol. 18, 33–51.
Bradbury, S.M., 2006. Response of the post-fire bryophyte community to salvage
logging in boreal mixedwood forests of northeastern Alberta, Canada. For. Ecol.
Manage. 234, 313–322.
Burton, P.J., 2006. Restoration of forests attacked by mountain pine beetle:
misnomer, misdirected, or must-do? BC. J. Ecosyst. Manage. 7, 1–10.
Butchart, S.H.M., Walpole, M., Collen, B., van Strien, A., Scharlemann, J.P.W., Almond,
R.E.A., Baillie, J.E.M., Bomhard, B., Brown, C., Bruno, J., Carpenter, K.E., Carr, G.M.,
Chanson, J., Chenery, A.M., Csirke, J., Davidson, N.C., Dentener, F., Foster, M.,
Galli, A., Galloway, J.N., Genovesi, P., Gregory, R.D., Hockings, M., Kapos, V.,
Lamarque, J.-F., Leverington, F., Loh, J., McGeoch, M.A., McRae, L., Minasyan, A.,
Morcillo, M.H., Oldfield, T.E.E., Pauly, D., Quader, S., Revenga, C., Sauer, J.R.,
Skolnik, B., Spear, D., Stanwell-Smith, D., Stuart, S.N., Symes, A., Tierney, M.,
Tyrrell, T.D., Vié, J.-C., Watson, R., 2010. Global biodiversity: indicators of recent
declines. Science 328, 1164–1168.
Carey, A.B., 2003. Biocomplexity and restoration of biodiversity in temperate
coniferous forest: inducing spatial heterogeneity with variable-density
thinning. Forestry 76, 127–136.
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S., Mao, C.X., Chazdon, R.L., Longino, J.T.,
2012. Models and estimators linking individual-based and sample-based
rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5, 3–21.
Development Core Team, R., 2014. R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna, Austria.
Donato, D.C., Fontaine, J.B., Campbell, J.L., Robinson, W.D., Kauffman, J.B., Law, B.E.,
2006. Post-wildfire logging hinders regeneration and increases fire risk. Science
311, 352.
Ewald, J., 2000. The influence of coniferous canopies on understorey vegetation and
soils in mountain forests of the northern Calcareous Alps. Appl. Veg. Sci. 3, 123–
134.
Fartmann, T., Müller, C., Poniatowski, D., 2013. Effects of coppicing on butterfly
communities of woodlands. Biol. Conserv. 159, 396–404.
Franzén, M., Johannesson, M., Franze, M., Johannesson, Æ.M., 2007. Predicting
extinction risk of butterflies and moths (Macrolepidoptera) from distribution
patterns and species characteristics. J. Insect Conserv. 11, 367–390.
Gardner, T.A., Barlow, J., Chazdon, R., Robert, M., Harvey, C.A., Ewers, R.M., Peres,
C.A., Sodhi, N.S., 2009. Prospects for tropical forest biodiversity in a humanmodified world. Ecol. Lett. 12, 561–582.
Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in
the measurement and comparison of species richness. Ecol. Lett. 4, 379–391.
Götmark, F., 2013. Habitat management alternatives for conservation forests in the
temperate zone: review, synthesis, and implications. For. Ecol. Manage. 306,
292–307.
Hacker, H., Müller, J., 2006. Die Schmetterlinge der Bayerischen Naturwaldreservate
eine Charakterisierung der Süddeutschen Waldlebensraumtypen Anhand der
Lepidoptera. Verlag Werner Wolf, Bindlach.
Hawksworth, D., Bull, A., Beck, J., Kitching, I., Linsenmair, K.E., 2006. Effects of
habitat disturbance can be subtle yet significant: biodiversity of hawkmothassemblages (Lepidoptera: Sphingidae) in Southeast-Asia. Biodivers. Conserv.
451–472.
Highland, S.A., Miller, J.C., Jones, J.A., 2013. Determinants of moth diversity and
community in a temperate mountain landscape: vegetation, topography, and
seasonality. Ecosphere 4, 1–22.
Hothorn, T., Bretz, F., Westfall, P., 2008. Simultaneous inference in general
parametric models. Biometrical J. 50, 346–363.
Hughey, K.F.D., Cullen, R., Moran, E., 2003. Integrating economics into priority
setting and evaluation in conservation management. Conserv. Biol. 17, 93–103.
S. Thorn et al. / Forest Ecology and Management 337 (2015) 41–47
Kerr, J.T., Sugar, A., Packer, L., 2000. Indicator taxa, rapid biodiversity assessment,
and nestedness in an endangered ecosystem. Conserv. Biol. 14, 1726–1734.
Kerr, J.T., Southwood, T.R.E., Cihlar, J., 2001. Remotely sensed habitat diversity
predicts butterfly species richness and community similarity in Canada. Proc.
Natl. Acad. Sci. 98, 11365–11370.
Kirchner, K., Kathke, S., Bruelheide, H., 2011. The interaction of gap age and
microsite for herb layer species in a near-natural spruce forest. J. Veg. Sci. 22,
85–95.
Kitching, R.L., Orr, A.G., Thalib, L., Mitchell, H., Hopkins, M.S., Graham, A.W., 2000.
Moth assemblages as indicators of environmental quality in remnants of upland
Australian rain forest. J. Appl. Ecol. 37, 284–297.
Kroll, A.J., Giovanini, J., Jones, J.E., Arnett, E.B., Altman, B., Nr, W., Box, P.O., Way, F.,
2012. Effects of salvage logging of beetle-killed forests on avian species and
foraging guild abundance. J. Wildlife Manage. 76, 1188–1196.
Lain, E.J., Haney, A., Burris, J.M., Burton, J., 2008. Response of vegetation and birds to
severe wind disturbance and salvage logging in a southern boreal forest. For.
Ecol. Manage. 256, 863–871.
Lehnert, L.W., Bässler, C., Brandl, R., Burton, P.J., Müller, J., Bassler, C., Muller, J., 2013.
Conservation value of forests attacked by bark beetles: highest number of
indicator species is found in early successional stages. J. Nat. Conserv. 21, 97–
104.
Lindenmayer, D.B., Franklin, J.F., Fischer, J., 2006. General management principles
and a checklist of strategies to guide forest biodiversity conservation. Biol.
Conserv. 131, 433–445.
Lindenmayer, D., Burton, P.J., Franklin, J.F., 2008. Salvage Logging and its Ecological
Consequences. Island Press, Washington.
Lindenmayer, D.B., Laurance, W.F., Franklin, J.F., 2012. Global decline in large old
trees. Science 338, 1305–1306.
Mansourian, S., Vallauri, D., 2014. Restoring forest landscapes: important lessons
learnt. Environ. Manage. 53, 241–251.
Mehr, M., Brandl, R., Kneib, T., Müller, J., 2012. The effect of bark beetle infestation
and salvage logging on bat activity in a national park. Biodivers. Conserv. 21,
2775–2786.
Merckx, T., Slade, E.M., 2014. Macro-moth families differ in their attraction to light:
implications for light-trap monitoring programmes. Insect Conserv. Divers. 7,
453–461.
Merckx, T., Feber, R.E., Hoare, D.J., Parsons, M.S., Kelly, C.J., Bourn, N.a.D.D.,
Macdonald, D.W., 2012. Conserving threatened Lepidoptera: towards an
effective woodland management policy in landscapes under intense human
land-use. Biol. Conserv. 149, 32–39.
Motta, R., Berretti, R., Lingua, E., Piussi, P., 2006. Coarse woody debris, forest
structure and regeneration in the Valbona Forest Reserve, Paneveggio, Italian
Alps. For. Ecol. Manage. 235, 155–163.
Müller, J., Bussler, H., Gossner, M., Rettelbach, T., Duelli, P., Duelli, Æ.P., 2008. The
European spruce bark beetle Ips typographus in a national park: from pest to
keystone species. Biodivers. Conserv. 17, 2979–3001.
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.
Müller, J., Mehr, M., Bässler, C., Fenton, M.B., Hothorn, T., Pretzsch, H., Klemmt, H.-J.,
Brandl, R., Brandl, H.K.R., 2012. Aggregative response in bats: prey abundance
versus habitat. Oecologia 169, 673–684.
Nyland, R.D., 2003. Even- to uneven-aged: the challenges of conversion. For. Ecol.
Manage. 172, 291–300.
O’Hara, K.L., Ramage, B.S., International, A., Hara, K.L.O., Hall, M., 2013. Silviculture
in an uncertain world: utilizing multi-aged management systems to integrate
disturbance. Forestry 86, 401–410.
47
Paillet, Y., Berges, L., Hjalten, J., Odor, P., Avon, C., Bernhardt-Romermann, M.,
Bijlsma, R.J., De Bruyn, L., Fuhr, M., Grandin, U., Kanka, R., Lundin, L., Luque, S.,
Magura, T., Matesanz, S., Meszaros, I., Sebastia, M.T., Schmidt, W., Standovar, T.,
Tothmeresz, B., Uotila, A., Valladares, F., Vellak, K., Virtanen, R., 2010.
Biodiversity differences between managed and unmanaged forests: metaanalysis of species richness in Europe. Conserv. Biol. 24, 101–112.
Priewasser, K., Brang, P., Bachofen, H., Bugmann, H., Wohlgemuth, T., 2013. Impacts
of salvage-logging on the status of deadwood after windthrow in Swiss forests.
Eur. J. For. Res. 132, 231–240.
Ranius, T., Caruso, A., Jonsell, M., Juutinen, A., Thor, G., Rudolphi, J., 2014. Dead wood
creation to compensate for habitat loss from intensive forestry. Biol. Conserv.
169, 277–284.
Rickert, C., Fichtner, A., Van Klink, R., Bakker, J.P., van Klink, R., 2012. A- and bdiversity in moth communities in salt marshes is driven by grazing
management. Biol. Conserv. 146, 24–31.
Rost, J., Hutto, R.L., Brotons, L., Pons, P., 2013. Comparing the effect of salvage
logging on birds in the mediterranean basin and the rocky mountains: common
patterns, different conservation implications. Biol. Conserv. 158, 7–13.
Schmalholz, M., Hylander, K., Frego, K., 2011. Bryophyte species richness and
composition in young forests regenerated after clear-cut logging versus after
wildfire and spruce budworm outbreak. Biodivers. Conserv. 20, 2575–2596.
Seidl, R., Schelhaas, M.-J., Rammer, W., Verkerk, P.J., 2014. Increasing forest
disturbances in Europe and their impact on carbon storage. Nat. Clim. Change
4, 806–810.
Stadelmann, G., Bugmann, H., Meier, F., Wermelinger, B., Bigler, C., 2013. Effects of
salvage logging and sanitation felling on bark beetle (Ips typographus L.)
infestations. For. Ecol. Manage. 305, 273–281.
Stokstad, E., 2006. Ecology: salvage logging research continues to generate sparks.
Science 311, 761.
Summerville, K.S., Crist, T.O., 2002. Effects of timber harvest on forest Lepidoptera:
community, guild, and species response. Ecol. Appl. 12, 820–835.
Summerville, K.S., Crist, T.O., 2005. Temporal patterns of species accumulation in a
survey of lepidoptera in a beech-maple forest. Biodivers. Conserv. 14, 3393–
3406.
Summerville, K.S., Ritter, L.M., Crist, T.O., 2004. Forest moth taxa as indicators of
lepidopteran richness and habitat disturbance: a preliminary assessment. Biol.
Conserv. 116, 9–18.
Svoboda, M., Pouska, Vã¡, 2008. Structure of a Central-European mountain spruce
old-growth forest with respect to historical development. For. Ecol. Manage.
255, 2177–2188.
Svoboda, M., Janda, P., Nagel, T.A., Fraver, S., Rejzek, J., Bac, R., Bace, R., 2012.
Disturbance history of an old-growth sub-alpine Picea abies stand in the
Bohemian Forest, Czech Republic. J. Veg. Sci. 23, 86–97.
Thorn, S., Bässler, C., Gottschalk, T., Hothorn, T., Bussler, H., Raffa, K., Müller, J., 2014.
New insights into the consequences of post-windthrow salvage logging
revealed by functional structure of saproxylic beetles Assemblages. PLoS ONE
9, e101757.
Truxa, C., Fiedler, K., 2012. Attraction to light – from how far do moths (Lepidoptera)
return to weak artificial sources of light? Eur. J. Entomol. 109, 77–84.
Venables, W.N., Ripley, B.D., 2002. Modern Applied Statistics with S. Springer, New
York.
Young, T.P., 2000. Restoration ecology and conservation biology. Biol. Conserv. 92,
73–83.
Zenner, E.K., Peck, J.E., Lahde, E., Laiho, O., 2012. Decomposing small-scale structural
complexity in even- and uneven-sized Norway spruce-dominated forests in
southern Finland. Forestry 85, 41–49.