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Linking forest management and biodiversity indicators to strengthen

sustainable forest management in Europe
Article in Ecological Indicators · December 2020

DOI: 10.1016/j.ecolind.2020.107275
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Ecological Indicators 122 (2021) 107275
Contents lists available at ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
Review
Linking forest management and biodiversity indicators to strengthen

sustainable forest management in Europe
Janine Oettel *, Katharina Lapin
Austrian Research Centre for Forests, Natural Hazards and Landscape (BFW), Seckendorff-Gudent-Weg 8, 1131 Vienna, Austria
A R T I C L E I N F O A B S T R A C T
Keywords: The accelerating global rate of species extinctions and the inevitable human impacts on biodiversity have
Europe increased the need to conserve, restore and use ecosystems sustainably. Indicators for biodiversity are the most
Nature conservation frequently used tool to monitor the status of biodiversity, changes to biodiversity, and the effects of management
Structural diversity
actions. In this study, we aim to assess the magnitude of studies on indicators for biodiversity (IB) in European
Forest protection
forest ecosystems, establish and analyze the link between IB and silvicultural management measures (MM), and
Forest management
Ecosystem management define indicators for management (IM), that aim to support biodiversity at the stand and landscape level. We
Umbrella species performed a systematic literature review and analyzed data from 162 studies. We identified 9 IB groups, cor
responding to 32 IB and linked them to 7 IM groups corresponding to 44 IM. Arthropods, birds, and plants are the
most frequently used IB in European managed forests. We found IB with clear links to specific IM, such as
saproxylic species and Collembola (collembolans) with deadwood, bird families (Passeriformes, Piciformes,
Accipitriformes) with links to microhabitats, and ground-dwelling species with links to regeneration. We iden
tified 17 species as proposed umbrella species based on the studies examined. This review shows that high
structural diversity is associated with an increase in diversity, especially with regard to vascular plants, birds and
ground-dwelling species. The adaptation of forest management for biodiversity requires regular active moni
toring of IM to assess the temporal and spatial changes and of IB to assess the effectiveness of measures.
1. Introduction Forests 2030 and its Global Forest Goal 2 target, underlines the contri
bution of all types of forests to biodiversity conservation (UN, 2017).
Forests provide multiple ecosystem services and contain a large The achievement of global biodiversity goals in managed forest eco
proportion of the Earth’s terrestrial biodiversity (Andren, 1994; Borie systems requires technically appropriate, economically viable and so
and Hulme, 2015; Kok et al., 2017). They provide habitats for many cially acceptable methods with well-defined criteria and indicators for
taxonomic groups including birds, vertebrates, invertebrates, and mi sustainable forest management at the local, regional, and national levels
crobes, which are impacted in different ways by current and past forest (FAO, 2020).
management practices (Douda et al., 2017; Lassauce et al., 2011; In Europe, the implementation of sustainable forest management has
Márialigeti et al., 2016). Forest management type and intensity are been emphasised in national strategies and implemented through legally
major drivers of structural diversity (Dieler et al., 2017; Gao et al., 2014; binding and non-binding instruments, such as the EU Habitats and Birds
Reise et al., 2019) and impact biodiversity in forest ecosystems (Dieler Directives, the EU Biodiversity Strategy, and various certification
et al., 2017; Schall and Ammer, 2013). Conservation and restoration of schemes (PEFC, 2020; FSC, 2020). Another common tool for the
forest ecosystems is one of the major critical tasks for the protection of implementation of measures supporting the development of forest
global ecosystems (Chazdon et al., 2017; Mancosu et al., 2018). To biodiversity in response to the global biodiversity targets is the forest
address the 21st century global biodiversity crisis, recent policy efforts management plan (FMP), which is a legal national instrument in most
at the international, regional, and local levels have focused on forest European countries (Lindenmayer et al., 2006; Schulze et al., 2014).
biodiversity and the contribution it can make to broader biodiversity Biodiversity considerations, including Natura 2000 conservation ob
conservation goals (Bayrak and Marafa, 2016; CBD, 2010; Forest jectives in FMPs, have been implemented by over 70% of EU-member
Europe, 2011). For example, the United Nations Strategic Plan for states (EU, 2018). Although the use of indicators is a widely supported
* Corresponding author.
E-mail address: [email protected] (J. Oettel).
https://doi.org/10.1016/j.ecolind.2020.107275
Received 25 June 2020; Received in revised form 24 October 2020; Accepted 11 December 2020
Available online 21 December 2020
1470-160X/© 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275
concept for biodiversity monitoring and assessment at all levels of 2. Methods

biodiversity policy, it can be difficult for stakeholders as well as forest
and conservation managers to identify applicable indicators and to un 2.1. Literature review
dertake or recommend the appropriate forest management measures
(Bayrak and Marafa, 2016; CBD, 2010; Forest Europe, 2011). We identified relevant studies on silvicultural management measures
Over time, the need for measurable, simple, financially feasible and related to biodiversity by searching the databases Scopus and ISI Web of
reliable indicators for biodiversity has increased, but their development Knowledge (20.03.2020) through March 2020 using the search string
has resulted in an inhomogeneous landscape of quantitative and quali “biodiversity” AND “indicator*” AND “forest management”. This search
tative biodiversity indicators (Schall and Ammer, 2013; Van Ouden string was formatted using ‘TS =’ added for ‘topic’ at the beginning of
hoven et al., 2012). Indicators for biodiversity frequently refer to species the search string. The search resulted in 607 references. We then
or groups of species that are characteristic for certain habitat features reviewed the titles, abstracts and keywords of these studies to select
and therefore often of high conservation value (Gao et al., 2015). those conducted in European forest ecosystems and excluded review
Furthermore, biodiversity indicators can also refer to structure-based articles and papers in languages besides English. These specifications
indicators such as heterogeneity and connectivity at the landscape narrowed the list down to 450 references, which were carefully read in
level. Indicators at landscape level are less frequently applied, however detail. We selected 162 studies matching the following criteria for
(Lindenmayer et al., 2000). further analysis: (1) original study including field data or field obser
Numerous single-species conservation concepts, for example con vations focusing on biodiversity patterns related to occurrence, abun
cepts focusing on keystone, flagship, or umbrella species (Simberloff, dance, cover, diversity, composition, or richness, (2) conducted in
1998), were developed to facilitate nature conservation management European forests, (3) in English language, and (4) linking organisms
and the planning of habitats (Barua, 2011; Hansson and Angelstam, and/or structural elements representing biodiversity at any level with
1991). The umbrella species concept has been recognized as a cost- and forest management. No restrictions were applied regarding the year of
time-effective tool following the logic that habitat protection and publication.
management of a single species at a high trophic level also shelters a
large range of co-occurring species that require similar environmental 2.2. Data processing
conditions (Ozaki et al., 2006; Roberge and Angelstam, 2004) and are
thus strongly related to the abundance of the umbrella species (Mills We systematically extracted all relevant information on bibliog
et al., 1993). In forest ecosystems, specialized bird species such as the raphy, geographic location, forest ecosystems and stand descriptors,
white-backed woodpecker (Dendrocopos leucotos) are often selected as such as forest type and dominant tree species, silvicultural information,
umbrella species (Lešo et al., 2019; Roberge et al., 2016; Suter et al., investigated organisms and structural elements representing biodiver
2002). Such single-species conservation approaches have been criticized sity, related forest structural components as well as recommended and
for their bias in terminology and selection of charismatic species, as well applied silvicultural management measures (MM). On this basis, we
as with the regard to their effectiveness and applicability as indicators established a systematic of biodiversity indicators (IB) based on the
for biodiversity in forests, however (Edman et al., 2011; Roberge et al., taxonomic information of organisms or the functional group. Forest
2008; Roberge and Angelstam, 2004; Runge et al., 2019). Almost all structural components ware categorized into management indicators
indicators for biodiversity are positively or negatively impacted by (IM) based on the investigated variables, such as tree height, deadwood
silvicultural measures (Dieler et al., 2017). Understanding the link be amount or levels of management intensity. To process the magnitude of
tween biodiversity indicators and silvicultural management measures both, IB and IM, we assigned indicator groups. In addition, all site de
has been the focus of many comparative, descriptive, and experimental scriptions were classified based on forest type (EEA, 2006).
research studies in previous decades, but the relationship to silvicultural
management measures has hitherto not been presented systematically. 2.3. Statistical analysis
To identify and facilitate these links and make them exploitable, we
defined indicators for biodiversity (IB) of organisms or structural ele To determine the relative importance of forest management for
ments that represent biodiversity in forests. We also specified the di biodiversity, we investigated the relationships between IB and IM. These
versity level of each IB: genetic, species, or ecosystem diversity level. relationships are well known for some IB, while for many others there is
The conservation and positive development of IB are related to silvi uncertainty regarding a clear correlation with a particular IM and thus
cultural management measures (MM), which affect biodiversity in regarding the influence of silvicultural management measures. Flow
managed forests. To assess the successful implementation and effec chart diagrams were used to visualize the proportion and strength of
tiveness of MM, we defined management indicators (IM) measurable correlation between IB and IM, resulting in MM. Sankey plots were
units and scales of forest structure and management that are used to created using SankeyMATIC (Bogart, 2014). We used the Chord diagram
monitor human interference. The difference between IB and IM has visualizations of the R package Circlize (Gu, 2019). Visualizations were
never been clearly delineated in previous studies, and therefore we created using ggplot2 for the analysis of the relationship between IB
highlight the importance of distinguishing between IB, which represent groups and IM groups (Wickham, 2016).
trends in biodiversity and IM, which represent changes in forest man On the base of the determined relationships, we summarized the
agement associated with an IB. frequency with which each of the identified IB is related to each of the
The aim of this review was therefore to investigate and systemati IM and IM groups, respectively. Fisher’s exact test was computed to
cally analyze the numerous links between indicators for biodiversity (IB) evaluate whether the IB are significantly related to the IM groups. The
and indicators for forest management (IM), in order to support the decision to use Fisher’s exact test was made because it allows low fre
integration of biodiversity conservation into sustainable forest man quencies of observation, which was the case for some of the links. The p-
agement of European forests by determining silvicultural management value (p = 0.05) was computed using Monte Carlo simulation (based on
measures (MM). The specific objectives were to (1) systematically re 2000 replicates). Following this test, correspondence analysis (CA) was
view the existing literature on applied IB in European forests, (2) performed based on the frequency of relationships between IB and IM
establish and analyze the links between IB and IM, (3) identify umbrella groups. CA allows us to evaluate correlations among IB in their response
species for European forest types and (4) suggest MM, that are related to to the same IM groups and to graphically visualize the in
IM and linked with IB. terdependencies. Computation and interpretation of the CA was per
formed using the R packages FactoMineR (Husson et al., 2020) and
factoextra (Kassambara and Mundt, 2020).
2
In addition, we investigated the relationship between IB and the 3. Results

different forest types according to EEA (2006). Based on the frequency of
IB investigations in the different forest types, we determined whether The empirical studies for the 162 analyzed peer-reviewed papers
they are specifically associated with one forest type. If this relationship were carried out in 32 countries (Appendix A). Most studies on biodi
is significant, the IB could represent a potential indicator of the versity indicators were conducted in Germany, Italy and France (Fig. 1),
respective forest type. We performed indicator species analysis and their number increased from 1995 to 2020 (Fig. 2). In total, 483
measuring the indicator value of the IB in relation to a forest type based
on its specificity and fidelity. Specificity refers to the proportion of forest
types in which an IB was investigated and fidelity refers to the propor
tion of IB per forest type. The statistical significance was tested using a
permutation test. We chose the number of random permutations
required for the permutational test (nperm = 999, p = 0.05). Analysis of
indicator species was performed using ‘multipatt’ command in the R
package indicspecies (Cáceres et al., 2020).
Finally, we examined the studies with regard to their consideration
of potential umbrella species among the IB as well as the provision of
relevant information on habitat threshold values or recommendations
on how these species can be promoted and conserved through targeted
management. For this purpose, we searched for the terminology ‘um
brella species’, ‘keystone species’ or ‘flagship species’ in the studies. We
summarized the number of studies investigating a particular umbrella
species and supplemented the management-related information.
Microsoft Excel 2010 was used for data management and data con
trol, and R version 3.4.2 (R Core Team, 2017) was used for further Fig. 2. Number of studies per year. N Number of studies per year included in
the analysis. The trend line [pink] shows an increase in studies between 1995
analyses.
and 2020. (For interpretation of the references to colour in this figure legend,
the reader is referred to the web version of this article.)
Fig. 1. Map of studies in 32 countries. Geographic spread and number of case studies included in the systematic literature review at the country level (n = 162
case studies).
3
links between IB, IM, and MM were identified (hereinafter: links). The ‘deadwood’ seems to be less investigated in deciduous forests. In
results also showed that 30% of the studies were conducted in deciduous coniferous forests the IM group ‘management intensity’ is added with
forests, 28% in mixed forests and 22% in coniferous forests, while 11% equal importance. In mixed forests the strongest link is visible between
of the studies were conducted in coniferous and deciduous forests and IM group ‘deadwood’ and IB group ‘arthropods’, while in coniferous
for 7% did not specify the forest type. According to the classification of forests the link of IM group ‘deadwood’ to IB group ‘fungi’ is as high as to
European forest types (EEA, 2006), most studies referred to beech forests IB group ‘arthropods. In deciduous forests the link between IM group
(18%), plantations and self-sown exotic forests (14.8%), and moun ‘stand structure and size’ and IB groups ‘arthropods’, ‘birds’ and ‘plants’
tainous beech forests (12%). In total, 361 links (representing 75% of the is dominant. The IB group ‘plants’, however, is more strongly linked to
studies) with managed forests, 41 links (8.5%) with unmanaged forests, the IM groups ‘tree species composition and diversity’ in coniferous
and 81 links (16.8%) with forests whose management type was not forests and ‘management intensity’ in mixed forests.
specified. Fisher’s exact test showed that IB were associated with different IM
groups (p < 0.001) based on the frequency of relationships. This is
3.1. Identification of indicators visualized in detail in CA results in Fig. 5 and Table 3 (see also Table 4).
The first and second axes of the CA explained 39% and 21% of the
We identified 32 IB and 44 IM, which result in 14 silvicultural variation in IB across IM groups. The first axis defines a gradient of forest
management measures for biodiversity in forests. The IB were assigned structural components. The variables that best explained the ordination
to nine IB groups, and the IM were assigned to seven IM groups. of IB along axis 1 were the IM groups ‘deadwood’ and ‘stand structure
The most frequently investigated IB groups were ‘arthropods’ (n = and size’. The second axis defines a gradient of related components to
129 links), ‘birds’ (n = 94), ‘plants’ (n = 94) and ‘habitats’ (n = 76), the management intensity, indicated by the IM groups ‘regeneration’ in the
latter referring to ecosystem biodiversity indicators, such as ‘tree mi lower and ‘habitat provisioning’ as well as ‘management intensity’ in the
crohabitats’ (n = 26), ‘deadwood’ (n = 9), ‘forest structure’ (n = 10), upper section of the graph (Fig. 5). Several IB show clear relationships to
and ‘habitats at landscape level’ (n = 15) or ‘protected habitats’ (n = certain IM groups, for example ‘saproxylic species’ and ‘Collembola
16). All other IB referred to species as indicators for biodiversity (n = (collembolans)’ with ‘deadwood’, bird families (‘Passeriformes’, ‘Pici
396). Within the IB group ‘arthropods’ we identified ‘ground-dwelling formes’, ‘Accipitriformes’) with ‘habitat provisioning’, or ‘ground-
species’ (n = 35) and ‘saproxylic species’ (n = 61) as most important IB. dwelling species’ with ‘regeneration’. However, there is also a large
The IB group ‘birds’ mainly consisted of IB ‘multi taxa birds’ (n = 52) group of IB which are generally linked to ‘management intensity’ or
and ‘Piciformes (woodpeckers)’ (n = 15) and the IB group ‘plants’ mainly ‘stand structure and size’. The structural IB ‘protected habitats’ and
referred to IB ‘vascular plants’ (n = 76). ‘deadwood’ are strongly linked to IM group ‘management intensity’,
The most frequently investigated IM groups were ‘stand structure while IB ‘microhabitats’ is linked to IM group ‘habitat provisioning’ and
and size’ (n = 153 links), ‘management intensity’ (n = 102) and IB ‘forest structure’ is strongly linked to IM group ‘stand structure and
‘deadwood’ (n = 85) (Table 1). By far the fewest examined IM group is size’.
‘regeneration’ (n = 16). The IM ‘stand diversity’ (n = 63) within the IM
group ‘stand structure and size’, the IM ‘management type’ (n = 25) 3.3. Correlation between IB and European forest types
within the IM group ‘management intensity’ and the IM ‘deadwood
amount’ within the IM group ‘deadwood’ showed the highest number of The frequency of links between 32 IB and 10 forest types were
links to biodiversity indicators. likewise investigated to identify significant correlations. We identified
The most frequently investigated MMs were ‘provide unmanaged several IB associated with forest types, but only four IB were found to be
forest patches (n = 70 links)’, ‘provide horizontal and structural het significant indicators (p = 0.05) of a particular forest type based on the
erogeneity’ (n = 67), ‘promote deadwood quality and quantity’ (n = 66). permutational test. The IB ‘Rodentia’ (rodents) and ‘Galliformes’
Fewer investigated MM include ‘perform active monitoring’ (n = 19), (gamebirds) (p < 0.05) were found to be indicators for boreal forest,
‘provide habitat structures’ (n = 17) and ‘reduce understory density’ (n ‘Chiroptera’ (bats) (p < 0.01) for broadleaf evergreen forest and ‘Diptera’
= 6). A list of MM including short definitions is provided in Table 2. (dipterans) (p < 0.05) for plantation and self-sown exotic forest.
3.2. Links between indicator groups 3.4. Umbrella species
Among the 483 identified links, the strongest links between IB and Among the IB, we found 17 umbrella species according to the
IM were observed for the IM group ‘stand structure and size’ (n = 153, investigated studies (Table 5). They correspond to the IB groups ‘birds’
31.6%) which included IM ‘stand diversity’ (n = 63) and IM ‘forest/tree (n = 10), ‘arthropods’ (n = 5), ‘fungi’ (n = 1) and ‘mammals’ (n = 1).
age’ (n = 39) (Fig. 3, Table 1). After the IM ‘management intensity’ (n = The most abundant umbrella species were Tetrao urogallus (western
102, 21%), IM ‘deadwood’ is the third largest IM group (n = 85, 17.7%), capercaillie) and Bonasa banasia (hazel grouse) in boreal and alpine
which is mostly quantified in deadwood amount (n = 44) or deadwood coniferous forests, and Picoides tridactylus (three-toed woodpecker) in
dimension (n = 12). The related silvicultural management measures boreal forests. From 17 umbrella species, 12 (71%) linked to general
include ‘promotion of deadwood quantity and quality’ (MM3), which forest management related recommendations, however, only for 6 of
influences the IM group ‘deadwood’ linked to the IB group ‘arthropods’, them (35%) clear threshold values were provided. These include dead
while the ‘provision of horizontal and structural heterogeneity’ (MM1) wood amounts of 62–76 m3 ha− 1 and a forest age of 50 years for Den
which influences the IM group ‘stand structure and size’ being linked to drocopus leucotos (white-backed woodpecker). For Tetrao urogallus
the IB groups ‘arthropods’, IB ‘birds’ and IB ‘plants’. The ‘provision of (western capercaillie) and Periparus ater (coal tit), minimum forest ages
unmanaged forest patches’ (MM9) influences the IM group ‘manage were defined as 70 and 100 years respectively.
ment intensity’ and thus the IB groups ‘plants’ and IB ‘habitats’ (Fig. 3).
Fig. 4 illustrates the differences in link assemblage among conif 4. Discussion
erous, deciduous, and mixed forest types. In general, the number of
investigated links was higher in deciduous (n = 148) and mixed forests The aims of this study were to determine indicators for biodiversity
(n = 140) compared to coniferous forests (n = 108). The three categories in different forest ecosystems and link them to measurable silvicultural
show different investigation priorities and link combinations between management measures by reviewing a total of 162 peer reviewed,
IM groups and IB groups. While in mixed forest the IM groups ‘dead empirical studies conducted in Europe. The findings emphasize that
wood’ and ‘stand structure and size’ are of main interest, the IM group biodiversity in European forests (represented through species or
4
Table 1
Indicators for management and related management measures. Table of indicators for management (IM) in seven IM groups showing number of determined links (n),
the scale, and the link to each of the 14 silvicultural management measures (MM) for biodiversity in forests in Europe: Provide horizontal and vertical structural
heterogeneity (MM-1), adapt tree species composition (MM-2), promote deadwood quantity and quality (MM-3), provide habitat structures (MM-4), increase tree
species diversity (MM-5), conserve habitat trees and veteran trees (MM-6), provide spatial heterogeneity at the landscape level (MM-7), reduce understory density
(MM-8), provide unmanaged forest patches (MM-9), increase rotation period (MM-10), provide uneven-aged forests under continuous forest cover (MM-11), avoid
forest fragmentation and habitat isolation (MM-12), adapt habitat management for indicator species (MM-13), perform active monitoring (MM-14); n = 162 studies
from the time period 1995–2020 reviewed. No. signifies the number assigned to IM used in Table A.1.
IM group No. Indicator for n Scales Management measures (MM)
management
1 2 3 4 5 6 7 8 9 10 11 12 13 14
Regeneration 1 litter cover 1 proportion, thickness ✔

2 natural 3 abundance ✔ ✔
regeneration
3 ground 6 gap size, height, proportion ✔ ✔ ✔ ✔
vegetation
cover
4 vegetation 5 presence/absence of indicator species, ✔ ✔ ✔ ✔ ✔
diversity temporal heterogeneity, vegetation
degradation
5 soil disturbance 1 duration of soil openess ✔
Tree species 6 share of alien 1 proportion ✔
species
composition 7 share of 8 proportion ✔
broadleaves
and diversity 8 share of native 1 abundance ✔
species
9 share of 3 proportion, spruce abundance ✔ ✔
coniferous
10 tree species 20 abundance, composition, mingling index, ✔ ✔ ✔ ✔
composition proportion, richness, species profile index,
spruce mortality
11 tree species 8 abundance, alpha/gamma, diversity, ✔ ✔ ✔ ✔
diversity Shannon index
deadwood 12 deadwood 9 decay stages ✔ ✔
decomposition
13 deadwood 12 diameter, type ✔ ✔
dimension
14 deadwood 2 diversity, mingling index ✔
diversity
15 deadwood 46 volume, type ✔ ✔ ✔ ✔ ✔ ✔
amount
16 lying deadwood 6 abundance, presence, diversity, presence/ ✔ ✔
absence of disturbance, volume
17 standing 10 abundance, proportion, volume, diameter ✔ ✔ ✔ ✔ ✔
deadwood
Habitat 18 branchiness 1 Abundance ✔
provisioning
19 cavities 4 Abundance ✔ ✔ ✔
20 characteristic 3 abundance, elevation, ocurrence ✔
species
21 microhabitats 8 abundance, habitat quality, T, relative ✔ ✔ ✔ ✔ ✔ ✔
humidity
22 old/veteran/ 26 abundance, abundance-age. Abundance- ✔ ✔ ✔ ✔ ✔ ✔
habitat trees basal area, abundance-diameter, area,
diameter, distance to nearest neighbour,
net present value, proportion, volume,
volume-diameter
23 protected 1 occurrence, abundance ✔
species
24 waterbodies 1 abundance, distribution ✔
Canopy 25 canopy cover 35 gap size leaf volume presence/absence of ✔ ✔ ✔ ✔
structure indicator species proportion
26 canopy 2 diversity, gap size ✔
diversity
27 tree height 5 stand height ✔ ✔ ✔
Stand 28 basal area 12 basal area, stemnumber ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔
structure
and stand size 29 diameter 18 diameter distribution, diameter ✔ ✔ ✔ ✔ ✔ ✔
diversity distribution-age
30 distance to 4 distance ✔ ✔ ✔ ✔
forest edge
31 forest/tree age 39 rotation period, stand age, tree age ✔ ✔ ✔ ✔ ✔ ✔ ✔
32 forest area 10 area, area -proportion ✔ ✔ ✔
33 growing stock 7 timber harvest proportion, volume, ✔ ✔ ✔ ✔ ✔
volume-rotation period
34 stand diversity 63 ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔
(continued on next page)
5
Table 1 (continued )
IM group No. Indicator for n Scales Management measures (MM)
management
1 2 3 4 5 6 7 8 9 10 11 12 13 14
alpha/gamma diversity, forest types,

habitat complexity score, net present
value, shrub proportion, stand
heterogeneity index, stand productivity,
structural diversity, vertical structure
Management 35 area-no/low 33 abundance area, distance between ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔
intensity management patches, forest quality, net present value,
patch characteristics, presence/absence of
disturbance, proportion, Shannon index
of land cover size, size and proportion,
timber harvest area
36 distance to 1 distance to forest road ✔
forest road
37 forest road 1 width ✔
width
38 harvesting 4 categories, thinning frequency ✔ ✔ ✔
method
39 management 1 past landuse ✔
history
40 management 23 categories, forest loss per year, ✔ ✔ ✔ ✔ ✔ ✔ ✔
intensity management intensity index, naturalness,
presence/absence of disturbance, rotation
period, timber harvest area, timber
harvest volume
41 management 25 categories, net present value ✔ ✔ ✔ ✔ ✔ ✔ ✔
type
42 nr of visitors 1 abundance ✔
43 harvesting 11 site productivity, timber harvest revenue, ✔ ✔ ✔ ✔ ✔
intensity timber harvest volume
44 long-term 2 past landuse, structural diversity, ✔ ✔
changes presence/absence of disturbance
Total 44 483
structural indicators) is linked to silvicultural management measures. resulting loss of profitability (Sever and Nagel, 2019).
Within the large number of studies, we identified 32 IB and established We identified several options for silvicultural management measures
483 links to 44 IM. A differentiation of applied IB with more detailed aimed at increasing habitat structures, such as ‘promoting deadwood
ecosystem information (for example forest stand age, successional stage, quantity and quality’ (MM-3), ‘conserving potential habitat trees and
and other relevant parameters) was not possible, however. We rarely veteran trees’ (MM-6) by retaining single trees or groups of trees as
found information on the effectiveness of biodiversity related manage potential refuges (Perhans et al., 2009), ‘increasing the rotation period’
ment measures, required financial resources actual or potential side (MM-10) (Lange et al., 2014; Triviño et al., 2017) or ‘providing un
effects, or acceptability to stakeholders, which should be included in managed forest patches’ (MM-9) (Banaś et al., 2019; Blattert et al.,
future studies with an adapted approach, including grey literature, 2018). In doing so, the provision of habitat structures for specialized
expert opinions and practitioners’ experiences. Nevertheless, our anal species can be facilitated.
ysis uncovers the magnitude of links between IM and IB and provides Another approach is to specifically ‘adapt habitat management for
insights into options for silvicultural management measures for sup indicator species’ (MM-13) which often refers to the umbrella species
porting biodiversity in forests. concept. Romero-Calcerrada and Luque (2006) describe an improve
ment to habitat quality for the three-toed woodpecker (Picoides tri
4.1. Habitat provisioning dactylus) with an increasing number of habitat trees. It still remains
unclear for how many and for which ecosystems umbrella species can be
There is an increasing number of studies recognizing the importance defined, however (Dudley et al., 2005; Simberloff, 1999), and it may
of habitat structures for biodiversity, especially in recent years (e.g. thus be appropriate to focus on functional indicator groups with similar
Augustynczik et al., 2019; Kozák et al., 2018; Nagel et al., 2017). Habitat habitat preferences instead of individual species (de Groot et al., 2016;
structures include standing and lying deadwood at different stages of Koivula, 2011; Thorn et al., 2016). Gregory et al. (2007) also suggest
decay (Floren et al., 2014; Lassauce et al., 2011; Parisi et al., 2016), as using multiple species (focal species concept) in order to reflect the
well as old and veteran trees providing microhabitats or big branches, overall health and functioning of forest ecosystems based on species
holes, cavities and water bodies (e.g. Larrieu et al., 2018; Sever and trends.
Nagel, 2019; Winter et al., 2015). Such structures have been discussed as For a comprehensive evaluation of the condition and quality of forest
monitoring surrogates for related species (Larrieu et al., 2018; Lassauce ecosystems, as well as the connectivity opportunities at the landscape
et al., 2011). Although monitoring them will not provide direct evidence level (Mitchell et al., 2008), ‘adapting forest management to avoid forest
of presence of species (Dudley et al., 2005) it may help to prioritize areas fragmentation’ (MM-12) is essential (Gregory et al., 2007). There are
for conservation efforts (Barton et al., 2014; Ikauniece et al., 2012). numerous studies reporting habitat degradation caused by forest frag
Species related to such habitats are numerous, and include fungi, li mentation or isolation (Angelstam et al., 2018; Maleque et al., 2006;
chens, arthropods, birds, bats and bryophytes. Many of them have Sverdrup-Thygeson and Lindenmayer, 2003). The impacts are alarming,
highly specialized habitat requirements often associated with unman ranging from altered species composition and loss of species to a
aged natural and old growth forests (Nagel et al., 2017; Sitzia et al., reduction in genetic variation (Appolorio Passilongo, 2017; Van Rossum
2017). However, providing sufficient habitat structures in managed et al., 2002) affecting not only non-mobile and low-mobility species, but
forests remains a challenge for many forest managers due to the birds and mammals as well (Andren, 1994; Lešo et al., 2019; Maleque
6
Table 2 Table 2 (continued )

Management measures for biodiversity. Summary of the 14 silvicultural No. Categories managment measure for biodiverstiy in forests (MM)
management measures (MM) with explanatory descriptions.
Habitat trees are living or dead Forest management should
No. Categories managment measure for biodiverstiy in forests (MM) trees of high ecological value. consider and actively promote
1 Provide horizontal and vertical 8 Reduce understory density They may have various types of the protection and conservation
structural heterogeneity holes, rotten parts, many and of indicator species and protected
The structural heterogeneity The reduction of the density in coarse branches, epiphytic habitats. Protected habitats refer
refers to a differentiation in the undergrowth can be achieved vegetation such as mosses or to the Habitats Directive or
diameter at breast height (dbh) by reducing stemnumber and lichens, or they may be a rare tree national nature conservation
and tree height. It assures the controlling mixed growth. This species in the surrounding forest. legislation. Indicator species can
establishment of diversely measure promotes the stand Veteran or mature trees are older be umbrella species or protected
structured forests with trees of stabilization as well as an than the rest of the stand. They species according to the Habitats
different dimensions and ages. increase in growth and can provide potential habitats and and Birds Directives or national
Increasing structural promote the tree species mixture. are left to natural development. nature conservation law.
heterogeneity is an important The use of a group of habitat trees Umbrella species are species that
tool for promoting stable forests or veteran trees significantly are selected for conservation
that are resistant to natural increases the ecological value. decisions, because their
hazards. protection implies the protection
2 Adapt tree species composition 9 Provide unmanaged forest of many other species that form
patches the ecological community of the
Tree species composition can be Forest areas that constitute respective habitat.
adjusted by selectively habitats worth protecting or 7 Provide spatial heterogeneity at 14 Perform active monitoring
promoting tree species by way of habitats for protected species landscape level
harvesting measures. Desired should be left undisturbed. This At the landscape level, the Active monitoring in forests
species are left standing in order may relate to either general or structural diversity of forests and refers to the continuous
to increase their share in favour seasonal management forest edges refers to varying tree observation of different species
of other tree species. In doing so, abandonment. In addition, in species composition, age classes and processes. It forms the basis
tree species composition can be unmanaged forest areas, the and development stages. This for detecting changes over time.
oriented in a certain direction. decay phase, which does not may include gaps with low forest Forest management can be
Further adaptation can further be usually occur under cover or different management adapted according to these
achieved by planting and management, may be allowed in intensities and management changes. Monitoring is also used
regulating mixed growth. unmanaged forest areas. systems. to evaluate the success of
3 Promote deadwood quantity and 10 Increase rotation period adaptation measures.
quality
Deadwood promotion refers to The rotation period refers to the
the quantity of deadwood, age of the stand up before et al., 2009). Possible silvicultural measures to avoid habitat fragmen
expressed in volume per hectare harvesting. For uneven-aged tation and isolation include avoidance of clear cutting (Česonienė et al.,
or number of trees, and to forests it refers to the age of the 2019; Iordan et al., 2018; Vangansbeke et al., 2017) and the enabling of
quality. Deadwood quality is individual tree. Increasing stand
defined by its dimension, age provides habitats for species
habitat connectivity (Dyderski et al., 2017).
decomposition and the type, that depend on mature forests
which can be differentiated into and allows the provision of large
4.2. Canopy and stand structure diversity
standing, lying or stumps. The scale deadwood.
latter are usually present due to
frequent timber harvesting Our study shows that a high structural diversity is linked to high
measures. levels of biodiversity, especially in regard to vascular plants, birds and
4 Provide habitat structures 11 Provide uneven-aged forests ground-dwelling species. Silvicultural management measures can
under continuous forest cover
Habitat structures can be various Adaptation of forest management
impact the following aspects of forest structure: basal area, canopy cover
structural elements providing to ensure uneven forest structures and diversity, deadwood, tree species diversity, diameter distribution,
microhabitats, such as wet and and continuous forest cover is tree age and height, and tree species composition. At the landscape level,
dry biotopes, piles of branches, or achieved through single tree structural diversity of forests and forest edges refers to varying tree
cairns. They increase structural harvesting. Natural regeneration
species composition and development stages. This may include forest
diversity and provide habitats for can occur simultaneously in small
numerous organisms. Habitat gaps and soil disturbances are areas with varying forest cover or differing management intensities and
structures that are present should reduced due to low management management systems. It is also important to integrate adjacent land
be left in place and unaffected by intensity. cover types, such as agriculture, taking related management intensity
forestry measures, if not present, and spatial–temporal changes into consideration. At stand level, struc
they can be actively created.
5 Increase tree species diversity 12 Avoid forest fragmentation and
tural diversity can be achieved by ‘reducing stem number and control
habitat isolation ling mixed growth’ (MM-8), ‘increasing rotation periods’ (MM-10) and
A variety of tree species and their Forest loss, clear cutting and ‘providing horizontal and vertical heterogeneity’ (MM-1). These man
composition increase tree species extensive forest road construction agement measures aimed at the creation of structurally diverse forests
diversity of a forest area. can lead to fragmentation of the
with trees of various ages, diameters and heights, which in turn are
Depending on the local forests. This should be avoided in
conditions, preference should be order to maintain the stability of positively associated with an increase in bird, insect and fungi abun
given to natural regeneration. a forest and ensure the habitat dance (Standovár et al., 2016).
Furthermore, additional tree connectivity. Canopy cover was identified as an important indicator for manage
species can be planted. Mixed ment, and is measured by the gap size, leaf volume, stand height, and
tree species should also be left in
the stand during harvesting
relative proportion of cover in the landscape. Particularly in coniferous
operations in order to ensure forests, canopy cover is a confirmed indicator for structural diversity
their natural regeneration in the (Coote et al., 2013). Overall vascular plant species richness increases
long term. and plant species composition changes with the increase of light avail
6 Conserve habitat trees and 13 Adapt habitat management for
ability in the herbaceous layer provided by canopy openness (French
veteran trees indicator species
et al., 2008; Kelemen et al., 2014; Lehnert et al., 2013). Burrascano et al.
(2009) concluded that plant diversity in forest ecosystems is highly
affected by decisions in forest management, which should be based on
7
Fig. 3. Links between indicators for biodiversity, indicators for management, and the related management measures. Sankey diagram quantifying the number of
links (relative values, n = 483) between indicators for biodiversity (IB) groups on the left side, indicators for forest management (IM) in the middle bar, and the 14
recommended silvicultural management measures (MM) on the right bar: Provide horizontal and vertical structural heterogeneity (MM-1), adapt tree species
composition (MM-2), promote deadwood quantity and quality (MM-3), provide habitat structures (MM-4), increase tree species diversity (MM-5), conserve habitat
trees and veteran trees (MM-6), provide spatial heterogeneity at landscape level (MM-7), reduce understory density (MM-8), provide unmanaged forest patches (MM-
9), increase rotation period (MM-10), provide uneven-aged forests under continuous forest cover (MM-11), avoid forest fragmentation and habitat isolation (MM-12),
adapt habitat management for indicator species (MM-13), perform active monitoring (MM-14).
the knowledge of natural stand dynamics. Furthermore, ‘the adaptation (2009) argue that even small unmanaged patches between 0.01 and 0.5
of forest management to create uneven forest structures and continuous ha can represent a “life-boat” for endangered species.
forest cover’ (MM-11) can contribute to reducing forest fragmentation, We conclude that the strong link between the IM ‘area with no or low
as well as increasing structural diversity at a larger scale. Sustainable management’ to IB groups ‘arthropods’, ‘birds’ and ‘fungi’ indicates a
forest management should therefore seek to mimic natural processes in positive effect on the overall biodiversity of forests. The positive effect of
order to enhance structural diversity (Doyon et al., 2008; Moretti et al., forest abandonment in large forest patches is not confirmed across all
2010). Insect and plant biodiversity in particular benefit from measures taxa, however (Sever and Nagel, 2019). In fact, many organisms func
such as retaining part of the deadwood and delaying planting after tioning as IB require active management measures for positive devel
harvesting (Müller et al., 2008). opment (Augustynczik et al., 2019; Cistrone et al., 2015; Hlásny et al.,
2017). Cistrone et al. (2015) report increasing foraging activity of bats in
4.3. The ‘no-management‘ approach sustainably managed forests compared to unmanaged forests. Vascular
plant diversity is positively linked to climate induced changes in the tree
Forest management intensity is associated with harvesting intensity species composition of formerly monocultural spruce forests (Hlásny
and forest stand management activities focused on wood supply (Levers et al., 2017). Further research and sampling efforts are thus required to
et al., 2014). In our review, forest management intensity measures investigate ecological processes in unmanaged versus managed forests
include the lowering of harvesting intensity, the adaptation of harvest with respect to changing climatic conditions (Sitzia et al., 2017).
ing and forest management methods, and the creation of forest areas
with no management. ‘Providing unmanaged forest patches’ (MM-9) 4.4. Implications for biodiversity monitoring
mainly targets forest habitats with high levels of naturalness that are of
interest for nature conservation, e.g. biodiversity hotspots (Schröter The adaptation of management measures for biodiversity requires
et al., 2017). Management abandonment may vary in space and time ‘regular active monitoring’ (MM-14) to assess the effectiveness of
depending on the objectives and associated species. Bird species survival measures, as well as temporal and spatial changes in indicator values
and breeding success is increases as a result of seasonal abandonment (Table 2). Several different approaches show that the established na
and the creation of quiet zones during breeding season (Fernandez- tional forest inventories (NFI) can provide information related to
Juricic and Jokimaki, 2001), while long-term unmanaged forests are biodiversity conservation (Crecente-Campo et al., 2016; Reise et al.,
needed to increase macrofungal diversity (Dvořák et al., 2017). 2019; Thakur et al., 2018). In particular, indicators for the IM group
Furthermore, specifications and demands for patch sizes vary greatly. ‘deadwood’ have been monitored and compared over large landscape
While Sánchez-Almendro et al. (2018) suggest a favorable unmanaged scales using NFI data (Rondeux et al., 2012). The comparison of other IM
forest patch size of above 10 ha, Dyderski et al. (2017) recommend the or IB monitored in NFIs requires careful harmonization efforts, however
preservation of any areas between 0.1 and 10 ha, and Perhans et al. (Chirici et al., 2012).
8
Fig. 4. Links between indicators for biodi

versity and indicators for management in
different forest types. Chord diagrams
showing the direct links in relative propor
tion from IM groups (canopy [structure],
deadwood, habitat [provisioning], manag
[ement intensity], reg[eneration], stand
[structure and size], tree [species composi
tion and diversity]) to IB groups (am[phi
bians], arthropods, birds, fungi, habitats,
mam[mals], multi [taxa], NA, plants and rep
[tilians]) for all data assembled (n = 483),
and for the forest types: deciduous forests (n
= ), coniferous forests (n = 108), and mixed
forests (n = 140).
Table 3
Scores of the Correspondence Analysis. Axes 1 and 2 scores of the CA based on
7 forest management indicator groups (IM groups).
CA axes 1 CA axes 2
Eigenvalue 0.27 0.15

Percent of Variance 39% 21%
Deadwood − 1.03 − 0.15
Habitat provisioning − 0.35 0.69
Canopy structure − 0.08 − 0.29
Species composition and diversity 0.31 0.07
Management intensity 0.32 0.47
Stand structure and size 0.34 − 0.26
Regeneration 0.46 − 0.94
importance of genetic monitoring as a tool for conservation and man

agement of forest genetic resources will increase in future (Filippos,
2016). The investigation of genetic indicators in sustainable forest
Fig. 5. Correlation between indicators for biodiversity and management indi
management needs to be explored in future research, especially with
cator groups. Ordination (CA) of 32 indicators for biodiversity (IB) based on 7
regard to climate change adaptation measures in forests (Loo et al.,
management indicator groups (IM groups). Plot shows correlation between the
2014). However, such efforts face challenges such as expenses, taxo
variables and the first two ordination axes based on the length and direction of
vectors. Biodiversity indicators are coloured according to the respective nomic expertise, representativeness and comparability at the national
biodiversity indicator groups (IB groups). Biodiversity indicator numbers and and international level, depending on the chosen methodology (Bar
bi-plot scores are presented in Table 4. soum et al., 2019). Therefore, monitoring has been commonly applied to
surrogates, such as taxa or habitats, as they can be assessed more easily
Existing studies have so far focused mainly on structural and species and quickly. Nevertheless, applicability is hampered by a lack of infor
indicators relating to ecosystem or species diversity. Very few studies mation, as many of the indicators have not been tested across different
refer to indicators concerning genetic diversity. Nevertheless, the forest types so far.
9
Table 4
Biodiversity indicator numbers and bi-plot scores of the correspondence analysis. Indicators for biodiversity (IB) consisting of ten IB groups showing the number
of determined links (n), the scale and the IB species scores used in the CA bi-plot (Fig. 5). No. signifies the number assigned to IB used in Table A.1.
IB group No. Indicator for biodiversity N Scales Axis 1 species score Axis 2 species score
Amphibians 1 Amphibia 1 richness 0.62 1.21

Arthropods 2 Coleoptera 16 abundance, cover, occurrence, richness, diversity 0.32 − 0.09
3 Collembolla 3 richness − 1.10 − 0.48
4 Diptera 3 occurrence, abundance, richness − 0.07 0.75
5 Ground-dwelling species 35 occurrence, abundance, richness, diversity, composition 0.53 − 0.72
6 Heteroptera 2 occurrence, abundance − 0.03 1.49
7 Hymenoptera 3 occurrence, abundance, richness 0.63 0.58
8 Lepidoptera 1 occurrence 0.62 1.21
9 Multi taxa 5 occurrence, abundance, richness, diversity 0.64 − 0.50
10 Saproxylic species 61 occurrence, abundance, richness, diversity, composition − 1.03 − 0.03
Birds 11 Accipitriformes 10 occurrence, abundance 0.24 0.51
12 Ciconniiformes 4 abundance 0.30 0.62
13 Galliformes 9 occurrence, abundance 0.63 0.26
14 Multi.taxa 52 occurrence, abundance, richness, diversity, composition, cover 0.09 − 0.05
15 Passeriformes 4 occurrence, abundance − 0.34 0.48
16 Piciformes 15 occurrence, abundance, richness, composition − 0.23 0.41
Fungi 17 Fungi 21 occurrence, abundance, richness, diversity, composition − 0.62 − 0.58
18 Lichens 12 occurrence, mass, richness, diversity 0.31 0.25
Mammals 19 Chiroptera 16 occurrence, abundance, richness, diversity 0.15 − 0.35
20 Multi taxa 1 richness 0.62 1.21
21 Rodentia 2 occurrence, abundance 0.64 0.27
Multi taxa 22 multi taxa 25 occurrence, abundance, richness, diversity − 0.29 − 0.03
Plants 23 Bryophyta 15 occurrence, abundance, richness, diversity, composition, cover, mass 0.18 0.10
24 Pteridophyta 1 occurrence − 0.15 − 0.74
25 multi Taxa 2 occurrence, abundance 0.62 − 0.25
26 vascular plants 76 occurrence, abundance, richness, diversity, composition., cover 0.44 − 0.11
Reptilians 27 Reptilia 1 richness 0.62 1.21
Habitats 28 Deadwood 9 abundance, amount, diversity 0.34 0.61
29 forest structure 10 abundance, cover, diversity 0.47 − 0.14
30 Habitats 15 occurrence, type, composition, richness, diversity 0.05 0.36
31 protected Habitats 16 occurrence, area, composition 0.25 0.81
32 tree microhabitats 26 occurrence, abundance, diversity − 0.42 0.23
Total 32 483
Table 5
List of umbrella species including recommendations for forest management. 17 umbrella species by biodiversity indicator group, showing recommendations and
thresholds for forest management (if provided), the related forest types, the number of studies and the respective references. Abbreviated names of forest types ac
cording to EEA (2006): alpine – alpine coniferous forests, beech – beech forest, boreal – boreal forest, evergreen – broadleaved evergreen forest, conif_med – coniferous
forest of the Mediterranean, Anatolian and Macronesian regions, mixed - hemiboreal forest and nemoral coniferous and mixed broadleaved-coniferous, deciduous –
mesophytic deciduous forest, mountain – mountainous beech forests, not_spec – not specified, plantation - plantations and self sown exotic forest, thermo - ther
mophilous deciduous forest.
IB group umbrella threshold/recommendation forest type n References
species
Arthropods Atypus piceus open forest stands, dry conditions deciduous 1 (Košulič et al., 2016)
Camponotus old growth conditions conif-med 1 (Arnan et al., 2009)
herculeanus
Formica lugubris even-aged managed forest conif-med 1 (Arnan et al., 2009)
Ips typographus mixed 2 (Lehnert et al., 2013; Müller et al., 2008)
Tapinoma old growth conditions conif-med 1 (Arnan et al., 2009)
erraticum
Birds Aegithalos boreal 2 (Peura et al., 2018; Triviño et al., 2017)
caudatus
Bonasa bonasia min. 20% forest cover per 1 km2 boreal, 3 (Naumov et al., 2018; Peura et al., 2018;
alpine Triviño et al., 2017)
Ciconia nigra min. 5% of trees with age >= 150 years 1 (Banaś et al., 2019)
Dendrocopos deadwood amount: 62–76m3ha − 1, 20% of growing stock as beech, boreal 2 (Lešo et al., 2019; Naumov et al., 2018)
leucotos deadwood;forest age > 50 years; >= 15% forest cover per 20 km2
Dryobates minor boreal 2 (Peura et al., 2018; Triviño et al., 2017)
Leiocopus medius old growth conditions deciduous 1 (Dorresteijn et al., 2013)
Periparus ater forest age > 100 years plantation 1 (Vangansbeke et al., 2017)
Picoides tree dbh >=30–40 cm boreal 3 (Naumov et al., 2018; Peura et al., 2018;
tridactylus Triviño et al., 2017)
Picus canus old growth conditions deciduous 1 (Dorresteijn et al., 2013)
Tetrao urogallus forest age >=70 years, min 25% forest cover per 16 km2 boreal, 4 (Lõhmus et al., 2017; Naumov et al., 2018;
alpine Peura et al., 2018; Triviño et al., 2017)
Ffungi Lobaria therm, 3 (Fačkovcová et al., 2019; Nascimbene et al.,
pulmonaria mountain 2010)
Mammals Pteromys volans boreal 2 (Peura et al., 2018; Triviño et al., 2017)
10
We therefore summarize that the most appropriate indicator species promote interdisciplinary research on indicators for biodiversity and
or groups are those which: (1) have a strong link to a management in forest management. We conclude that there is an urgent need for more
dicator, (2) are sensitive to changes, and (3) are not related to similar precise biodiversity guidelines for forest and conservation practitioners.
habitat needs in order to cover different gradients of management in Management practices need to reflect the latest scientific outputs, in
fluences. Additionally, further research should focus on biodiversity order to avoid mismanagement of biodiversity in forest ecosystems.
indicators that have not yet been studied (or not been studied in depth) On the basis of our findings, we identify four important issues for
but show high potential through a strong link to a certain management future research:
indicator.
• Studies on biodiversity indicators and specific management related
4.5. Application of indicators threshold values
• Research on the influence of changing climatic conditions and
In the 162 studies, apart from various general management recom associated adaptation measures with regard to biodiversity
mendations, only 6 thresholds for forest management were reported indicators
(Table 5). We thus recognize the need to define evidence-based • Investigation of habitat connectivity at the landscape level, taking
threshold levels for biodiversity gains with respect to regional differ other land use types and limiting factors into consideration
ences (Humphrey and Bailey, 2012). We highlight that no single indi • Analysis of the effectiveness of biodiversity management measures,
cator approach is sufficient for guaranteeing successful biodiversity including financial resources, actual or potential side effects, and
protection in forests. Furthermore, our findings suggest that the selec acceptance by stakeholders.
tion of indicators for biodiversity should take three major aspects into
consideration: (1) What are the long-term conservation goals at the local
Declaration of Competing Interest
and regional level to increase the level of biodiversity?; (2) Which in
dicators for biodiversity can be used to achieve these goals?, and (3) how
The authors declare that they have no known competing financial
can the forest management be adapted and its success be monitored?
interests or personal relationships that could have appeared to influence
In practice, the formulation of sustainable forest management goals
the work reported in this paper.
and the selection of indicators is complex and multidisciplinary, and
forest managers may need to make challenging decisions in this respect
(Schall and Ammer, 2013). This study provides forest and conservation Acknowledgements
practitioners with an overview of links between different indicators of
biodiversity (IB), associated forest structural components expressed in This study was supported by the Austrian Federal Ministry for
management indicators (IM) and corresponding management measures Agriculture, Regions and Tourism under the Austrian Rural Develop
(MM). In accordance with local and regional conservation goals, ment Programme 2014-2020 [7.6.1c-III4-40/18]. We would like to
implementation of appropriate measures and monitoring of their success thank Silvio Schüler for his valuable support during the last month and
using IM is possible. In addition, IB should be monitored on a small scale fruitful discussions, Isabel Georges for her technical assistance, and
for control purposes. Stephan Stockinger for his comments on English language and style that
Although we focused on the identification of links at the forest stand significantly improved this manuscript. We also greatly appreciate the
level, our results contribute to the discussion on the appropriate level of constructive comments by two anonymous reviewers.
management intensity in conservation areas. Forest management can
have positive and negative effects on biodiversity. In the case of certain Appendix A. Supplementary data
biodiversity indicators, such as plants, forest type specific management
was found to be positively linked to occurrence and diversity. It should Supplementary data to this article can be found online at https://doi.
to be kept in mind, however, that we lack a comprehensive picture of the org/10.1016/j.ecolind.2020.107275.
natural dynamics and natural appearance of most European forest types,
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Linking forest management and biodiversity indicators to strengthen

Article in Ecological Indicators · December 2020

Janine Oettel Katharina Lapin

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Linking forest management and biodiversity indicators to strengthen

concept for biodiversity monitoring and assessment at all levels of 2. Methods

In addition, we investigated the relationship between IB and the 3. Results

3.2. Links between indicator groups 3.4. Umbrella species

Regeneration 1 litter cover 1 proportion, thickness ✔

alpha/gamma diversity, forest types,

Table 2 Table 2 (continued )

Fig. 4. Links between indicators for biodi­

Eigenvalue 0.27 0.15

importance of genetic monitoring as a tool for conservation and man­

Amphibians 1 Amphibia 1 richness 0.62 1.21

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Fig. 4. Links between indicators for biodi

importance of genetic monitoring as a tool for conservation and man