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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 provide multiple ecosystem services and contain a large
proportion of the Earth’s terrestrial biodiversity (Andren, 1994; Borie
and Hulme, 2015; Kok et al., 2017). They provide habitats for many
taxonomic groups including birds, vertebrates, invertebrates, and mi­
crobes, which are impacted in different ways by current and past forest
management practices (Douda et al., 2017; Lassauce et al., 2011;
Márialigeti et al., 2016). Forest management type and intensity are
major drivers of structural diversity (Dieler et al., 2017; Gao et al., 2014;
Reise et al., 2019) and impact biodiversity in forest ecosystems (Dieler
et al., 2017; Schall and Ammer, 2013). Conservation and restoration of
forest ecosystems is one of the major critical tasks for the protection of
global ecosystems (Chazdon et al., 2017; Mancosu et al., 2018). To
address the 21st century global biodiversity crisis, recent policy efforts
at the international, regional, and local levels have focused on forest
biodiversity and the contribution it can make to broader biodiversity
conservation goals (Bayrak and Marafa, 2016; CBD, 2010; Forest
Europe, 2011). For example, the United Nations Strategic Plan for
Forests 2030 and its Global Forest Goal 2 target, underlines the contri­
bution of all types of forests to biodiversity conservation (UN, 2017).
The achievement of global biodiversity goals in managed forest eco­
systems requires technically appropriate, economically viable and so­
cially acceptable methods with well-defined criteria and indicators for
sustainable forest management at the local, regional, and national levels
(FAO, 2020).
In Europe, the implementation of sustainable forest management has
been emphasised in national strategies and implemented through legally
binding and non-binding instruments, such as the EU Habitats and Birds
Directives, the EU Biodiversity Strategy, and various certification
schemes (PEFC, 2020; FSC, 2020). Another common tool for the
implementation of measures supporting the development of forest
biodiversity in response to the global biodiversity targets is the forest
management plan (FMP), which is a legal national instrument in most
European countries (Lindenmayer et al., 2006; Schulze et al., 2014).
Biodiversity considerations, including Natura 2000 conservation ob­
jectives in FMPs, have been implemented by over 70% of EU-member
states (EU, 2018). Although the use of indicators is a widely supported

* Corresponding author.
E-mail address: janine.oettel@bfw.gv.at (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
concept for biodiversity monitoring and assessment at all levels of
biodiversity policy, it can be difficult for stakeholders as well as forest
and conservation managers to identify applicable indicators and to un­
dertake or recommend the appropriate forest management measures
(Bayrak and Marafa, 2016; CBD, 2010; Forest Europe, 2011).
Over time, the need for measurable, simple, financially feasible and
reliable indicators for biodiversity has increased, but their development
has resulted in an inhomogeneous landscape of quantitative and quali­
tative biodiversity indicators (Schall and Ammer, 2013; Van Ouden­
hoven et al., 2012). Indicators for biodiversity frequently refer to species
or groups of species that are characteristic for certain habitat features
and therefore often of high conservation value (Gao et al., 2015).
Furthermore, biodiversity indicators can also refer to structure-based
indicators such as heterogeneity and connectivity at the landscape
level. Indicators at landscape level are less frequently applied, however
(Lindenmayer et al., 2000).
Numerous single-species conservation concepts, for example con­
cepts focusing on keystone, flagship, or umbrella species (Simberloff,
1998), were developed to facilitate nature conservation management
and the planning of habitats (Barua, 2011; Hansson and Angelstam,
1991). The umbrella species concept has been recognized as a cost- and
time-effective tool following the logic that habitat protection and
management of a single species at a high trophic level also shelters a
large range of co-occurring species that require similar environmental
conditions (Ozaki et al., 2006; Roberge and Angelstam, 2004) and are
thus strongly related to the abundance of the umbrella species (Mills
et al., 1993). In forest ecosystems, specialized bird species such as the
white-backed woodpecker (Dendrocopos leucotos) are often selected as
umbrella species (Lešo et al., 2019; Roberge et al., 2016; Suter et al.,
2002). Such single-species conservation approaches have been criticized
for their bias in terminology and selection of charismatic species, as well
as with the regard to their effectiveness and applicability as indicators
for biodiversity in forests, however (Edman et al., 2011; Roberge et al.,
2008; Roberge and Angelstam, 2004; Runge et al., 2019). Almost all
indicators for biodiversity are positively or negatively impacted by
silvicultural measures (Dieler et al., 2017). Understanding the link be­
tween biodiversity indicators and silvicultural management measures
has been the focus of many comparative, descriptive, and experimental
research studies in previous decades, but the relationship to silvicultural
management measures has hitherto not been presented systematically.
To identify and facilitate these links and make them exploitable, we
defined indicators for biodiversity (IB) of organisms or structural ele­
ments that represent biodiversity in forests. We also specified the di­
versity level of each IB: genetic, species, or ecosystem diversity level.
The conservation and positive development of IB are related to silvi­
cultural management measures (MM), which affect biodiversity in
managed forests. To assess the successful implementation and effec­
tiveness of MM, we defined management indicators (IM) measurable
units and scales of forest structure and management that are used to
monitor human interference. The difference between IB and IM has
never been clearly delineated in previous studies, and therefore we
highlight the importance of distinguishing between IB, which represent
trends in biodiversity and IM, which represent changes in forest man­
agement associated with an IB.
The aim of this review was therefore to investigate and systemati­
cally analyze the numerous links between indicators for biodiversity (IB)
and indicators for forest management (IM), in order to support the
integration of biodiversity conservation into sustainable forest man­
agement of European forests by determining silvicultural management
measures (MM). The specific objectives were to (1) systematically re­
view the existing literature on applied IB in European forests, (2)
establish and analyze the links between IB and IM, (3) identify umbrella
species for European forest types and (4) suggest MM, that are related to
IM and linked with IB.
2
Ecological Indicators 122 (2021) 107275
2. Methods
2.1. Literature review
We identified relevant studies on silvicultural management measures
related to biodiversity by searching the databases Scopus and ISI Web of
Knowledge (20.03.2020) through March 2020 using the search string
“biodiversity” AND “indicator*” AND “forest management”. This search
string was formatted using ‘TS =’ added for ‘topic’ at the beginning of
the search string. The search resulted in 607 references. We then
reviewed the titles, abstracts and keywords of these studies to select
those conducted in European forest ecosystems and excluded review
articles and papers in languages besides English. These specifications
narrowed the list down to 450 references, which were carefully read in
detail. We selected 162 studies matching the following criteria for
further analysis: (1) original study including field data or field obser­
vations focusing on biodiversity patterns related to occurrence, abun­
dance, cover, diversity, composition, or richness, (2) conducted in
European forests, (3) in English language, and (4) linking organisms
and/or structural elements representing biodiversity at any level with
forest management. No restrictions were applied regarding the year of
publication.
2.2. Data processing
We systematically extracted all relevant information on bibliog­
raphy, geographic location, forest ecosystems and stand descriptors,
such as forest type and dominant tree species, silvicultural information,
investigated organisms and structural elements representing biodiver­
sity, related forest structural components as well as recommended and
applied silvicultural management measures (MM). On this basis, we
established a systematic of biodiversity indicators (IB) based on the
taxonomic information of organisms or the functional group. Forest
structural components ware categorized into management indicators
(IM) based on the investigated variables, such as tree height, deadwood
amount or levels of management intensity. To process the magnitude of
both, IB and IM, we assigned indicator groups. In addition, all site de­
scriptions were classified based on forest type (EEA, 2006).
2.3. Statistical analysis
To determine the relative importance of forest management for
biodiversity, we investigated the relationships between IB and IM. These
relationships are well known for some IB, while for many others there is
uncertainty regarding a clear correlation with a particular IM and thus
regarding the influence of silvicultural management measures. Flow
chart diagrams were used to visualize the proportion and strength of
correlation between IB and IM, resulting in MM. Sankey plots were
created using SankeyMATIC (Bogart, 2014). We used the Chord diagram
visualizations of the R package Circlize (Gu, 2019). Visualizations were
created using ggplot2 for the analysis of the relationship between IB
groups and IM groups (Wickham, 2016).
On the base of the determined relationships, we summarized the
frequency with which each of the identified IB is related to each of the
IM and IM groups, respectively. Fisher’s exact test was computed to
evaluate whether the IB are significantly related to the IM groups. The
decision to use Fisher’s exact test was made because it allows low fre­
quencies of observation, which was the case for some of the links. The p-
value (p = 0.05) was computed using Monte Carlo simulation (based on
2000 replicates). Following this test, correspondence analysis (CA) was
performed based on the frequency of relationships between IB and IM
groups. CA allows us to evaluate correlations among IB in their response
to the same IM groups and to graphically visualize the in­
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).
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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
J. Oettel and K. Lapin
links between IB, IM, and MM were identified (hereinafter: links). The
results also showed that 30% of the studies were conducted in deciduous
forests, 28% in mixed forests and 22% in coniferous forests, while 11%
of the studies were conducted in coniferous and deciduous forests and
for 7% did not specify the forest type. According to the classification of
European forest types (EEA, 2006), most studies referred to beech forests
(18%), plantations and self-sown exotic forests (14.8%), and moun­
tainous beech forests (12%). In total, 361 links (representing 75% of the
studies) with managed forests, 41 links (8.5%) with unmanaged forests,
and 81 links (16.8%) with forests whose management type was not
specified.
3.1. Identification of indicators
We identified 32 IB and 44 IM, which result in 14 silvicultural
management measures for biodiversity in forests. The IB were assigned
to nine IB groups, and the IM were assigned to seven IM groups.
The most frequently investigated IB groups were ‘arthropods’ (n =
129 links), ‘birds’ (n = 94), ‘plants’ (n = 94) and ‘habitats’ (n = 76), the
latter referring to ecosystem biodiversity indicators, such as ‘tree mi­
crohabitats’ (n = 26), ‘deadwood’ (n = 9), ‘forest structure’ (n = 10),
and ‘habitats at landscape level’ (n = 15) or ‘protected habitats’ (n =
16). All other IB referred to species as indicators for biodiversity (n =
396). Within the IB group ‘arthropods’ we identified ‘ground-dwelling
species’ (n = 35) and ‘saproxylic species’ (n = 61) as most important IB.
The IB group ‘birds’ mainly consisted of IB ‘multi taxa birds’ (n = 52)
and ‘Piciformes (woodpeckers)’ (n = 15) and the IB group ‘plants’ mainly
referred to IB ‘vascular plants’ (n = 76).
The most frequently investigated IM groups were ‘stand structure
and size’ (n = 153 links), ‘management intensity’ (n = 102) and
‘deadwood’ (n = 85) (Table 1). By far the fewest examined IM group is
‘regeneration’ (n = 16). The IM ‘stand diversity’ (n = 63) within the IM
group ‘stand structure and size’, the IM ‘management type’ (n = 25)
within the IM group ‘management intensity’ and the IM ‘deadwood
amount’ within the IM group ‘deadwood’ showed the highest number of
links to biodiversity indicators.
The most frequently investigated MMs were ‘provide unmanaged
forest patches (n = 70 links)’, ‘provide horizontal and structural het­
erogeneity’ (n = 67), ‘promote deadwood quality and quantity’ (n = 66).
Fewer investigated MM include ‘perform active monitoring’ (n = 19),
‘provide habitat structures’ (n = 17) and ‘reduce understory density’ (n
= 6). A list of MM including short definitions is provided in Table 2.
3.2. Links between indicator groups
Among the 483 identified links, the strongest links between IB and
IM were observed for the IM group ‘stand structure and size’ (n = 153,
31.6%) which included IM ‘stand diversity’ (n = 63) and IM ‘forest/tree
age’ (n = 39) (Fig. 3, Table 1). After the IM ‘management intensity’ (n =
102, 21%), IM ‘deadwood’ is the third largest IM group (n = 85, 17.7%),
which is mostly quantified in deadwood amount (n = 44) or deadwood
dimension (n = 12). The related silvicultural management measures
include ‘promotion of deadwood quantity and quality’ (MM3), which
influences the IM group ‘deadwood’ linked to the IB group ‘arthropods’,
while the ‘provision of horizontal and structural heterogeneity’ (MM1)
which influences the IM group ‘stand structure and size’ being linked to
the IB groups ‘arthropods’, IB ‘birds’ and IB ‘plants’. The ‘provision of
unmanaged forest patches’ (MM9) influences the IM group ‘manage­
ment intensity’ and thus the IB groups ‘plants’ and IB ‘habitats’ (Fig. 3).
Fig. 4 illustrates the differences in link assemblage among conif­
erous, deciduous, and mixed forest types. In general, the number of
investigated links was higher in deciduous (n = 148) and mixed forests
(n = 140) compared to coniferous forests (n = 108). The three categories
show different investigation priorities and link combinations between
IM groups and IB groups. While in mixed forest the IM groups ‘dead­
wood’ and ‘stand structure and size’ are of main interest, the IM group
4
Ecological Indicators 122 (2021) 107275
‘deadwood’ seems to be less investigated in deciduous forests. In
coniferous forests the IM group ‘management intensity’ is added with
equal importance. In mixed forests the strongest link is visible between
IM group ‘deadwood’ and IB group ‘arthropods’, while in coniferous
forests the link of IM group ‘deadwood’ to IB group ‘fungi’ is as high as to
IB group ‘arthropods. In deciduous forests the link between IM group
‘stand structure and size’ and IB groups ‘arthropods’, ‘birds’ and ‘plants’
is dominant. The IB group ‘plants’, however, is more strongly linked to
the IM groups ‘tree species composition and diversity’ in coniferous
forests and ‘management intensity’ in mixed forests.
Fisher’s exact test showed that IB were associated with different IM
groups (p < 0.001) based on the frequency of relationships. This is
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
variation in IB across IM groups. The first axis defines a gradient of forest
structural components. The variables that best explained the ordination
of IB along axis 1 were the IM groups ‘deadwood’ and ‘stand structure
and size’. The second axis defines a gradient of related components to
management intensity, indicated by the IM groups ‘regeneration’ in the
lower and ‘habitat provisioning’ as well as ‘management intensity’ in the
upper section of the graph (Fig. 5). Several IB show clear relationships to
certain IM groups, for example ‘saproxylic species’ and ‘Collembola
(collembolans)’ with ‘deadwood’, bird families (‘Passeriformes’, ‘Pici­
formes’, ‘Accipitriformes’) with ‘habitat provisioning’, or ‘ground-
dwelling species’ with ‘regeneration’. However, there is also a large
group of IB which are generally linked to ‘management intensity’ or
‘stand structure and size’. The structural IB ‘protected habitats’ and
‘deadwood’ are strongly linked to IM group ‘management intensity’,
while IB ‘microhabitats’ is linked to IM group ‘habitat provisioning’ and
IB ‘forest structure’ is strongly linked to IM group ‘stand structure and
size’.
3.3. Correlation between IB and European forest types
The frequency of links between 32 IB and 10 forest types were
likewise investigated to identify significant correlations. We identified
several IB associated with forest types, but only four IB were found to be
significant indicators (p = 0.05) of a particular forest type based on the
permutational test. The IB ‘Rodentia’ (rodents) and ‘Galliformes’
(gamebirds) (p < 0.05) were found to be indicators for boreal forest,
‘Chiroptera’ (bats) (p < 0.01) for broadleaf evergreen forest and ‘Diptera’
(dipterans) (p < 0.05) for plantation and self-sown exotic forest.
3.4. Umbrella species
Among the IB, we found 17 umbrella species according to the
investigated studies (Table 5). They correspond to the IB groups ‘birds’
(n = 10), ‘arthropods’ (n = 5), ‘fungi’ (n = 1) and ‘mammals’ (n = 1).
The most abundant umbrella species were Tetrao urogallus (western
capercaillie) and Bonasa banasia (hazel grouse) in boreal and alpine
coniferous forests, and Picoides tridactylus (three-toed woodpecker) in
boreal forests. From 17 umbrella species, 12 (71%) linked to general
forest management related recommendations, however, only for 6 of
them (35%) clear threshold values were provided. These include dead­
wood amounts of 62–76 m3 ha− 1 and a forest age of 50 years for Den­
drocopus leucotos (white-backed woodpecker). For Tetrao urogallus
(western capercaillie) and Periparus ater (coal tit), minimum forest ages
were defined as 70 and 100 years respectively.
4. Discussion
The aims of this study were to determine indicators for biodiversity
in different forest ecosystems and link them to measurable silvicultural
management measures by reviewing a total of 162 peer reviewed,
empirical studies conducted in Europe. The findings emphasize that
biodiversity in European forests (represented through species or
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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.
Within the large number of studies, we identified 32 IB and established
483 links to 44 IM. A differentiation of applied IB with more detailed
ecosystem information (for example forest stand age, successional stage,
and other relevant parameters) was not possible, however. We rarely
found information on the effectiveness of biodiversity related manage­
ment measures, required financial resources actual or potential side
effects, or acceptability to stakeholders, which should be included in
future studies with an adapted approach, including grey literature,
expert opinions and practitioners’ experiences. Nevertheless, our anal­
ysis uncovers the magnitude of links between IM and IB and provides
insights into options for silvicultural management measures for sup­
porting biodiversity in forests.
4.1. Habitat provisioning
There is an increasing number of studies recognizing the importance
of habitat structures for biodiversity, especially in recent years (e.g.
Augustynczik et al., 2019; Kozák et al., 2018; Nagel et al., 2017). Habitat
structures include standing and lying deadwood at different stages of
decay (Floren et al., 2014; Lassauce et al., 2011; Parisi et al., 2016), as
well as old and veteran trees providing microhabitats or big branches,
holes, cavities and water bodies (e.g. Larrieu et al., 2018; Sever and
Nagel, 2019; Winter et al., 2015). Such structures have been discussed as
monitoring surrogates for related species (Larrieu et al., 2018; Lassauce
et al., 2011). Although monitoring them will not provide direct evidence
of presence of species (Dudley et al., 2005) it may help to prioritize areas
for conservation efforts (Barton et al., 2014; Ikauniece et al., 2012).
Species related to such habitats are numerous, and include fungi, li­
chens, arthropods, birds, bats and bryophytes. Many of them have
highly specialized habitat requirements often associated with unman­
aged natural and old growth forests (Nagel et al., 2017; Sitzia et al.,
2017). However, providing sufficient habitat structures in managed
forests remains a challenge for many forest managers due to the
resulting loss of profitability (Sever and Nagel, 2019).
We identified several options for silvicultural management measures
aimed at increasing habitat structures, such as ‘promoting deadwood
quantity and quality’ (MM-3), ‘conserving potential habitat trees and
veteran trees’ (MM-6) by retaining single trees or groups of trees as
potential refuges (Perhans et al., 2009), ‘increasing the rotation period’
(MM-10) (Lange et al., 2014; Triviño et al., 2017) or ‘providing un­
managed forest patches’ (MM-9) (Banaś et al., 2019; Blattert et al.,
2018). In doing so, the provision of habitat structures for specialized
species can be facilitated.
Another approach is to specifically ‘adapt habitat management for
indicator species’ (MM-13) which often refers to the umbrella species
concept. Romero-Calcerrada and Luque (2006) describe an improve­
ment to habitat quality for the three-toed woodpecker (Picoides tri­
dactylus) with an increasing number of habitat trees. It still remains
unclear for how many and for which ecosystems umbrella species can be
defined, however (Dudley et al., 2005; Simberloff, 1999), and it may
thus be appropriate to focus on functional indicator groups with similar
habitat preferences instead of individual species (de Groot et al., 2016;
Koivula, 2011; Thorn et al., 2016). Gregory et al. (2007) also suggest
using multiple species (focal species concept) in order to reflect the
overall health and functioning of forest ecosystems based on species
trends.
For a comprehensive evaluation of the condition and quality of forest
ecosystems, as well as the connectivity opportunities at the landscape
level (Mitchell et al., 2008), ‘adapting forest management to avoid forest
fragmentation’ (MM-12) is essential (Gregory et al., 2007). There are
numerous studies reporting habitat degradation caused by forest frag­
mentation or isolation (Angelstam et al., 2018; Maleque et al., 2006;
Sverdrup-Thygeson and Lindenmayer, 2003). The impacts are alarming,
ranging from altered species composition and loss of species to a
reduction in genetic variation (Appolorio Passilongo, 2017; Van Rossum
et al., 2002) affecting not only non-mobile and low-mobility species, but
birds and mammals as well (Andren, 1994; Lešo et al., 2019; Maleque

6
J. Oettel and K. Lapin
Table 2
Management measures for biodiversity. Summary of the 14 silvicultural
management measures (MM) with explanatory descriptions.
No. Categories managment measure for biodiverstiy in forests (MM)
1 Provide horizontal and vertical
structural heterogeneity
The structural heterogeneity
refers to a differentiation in
diameter at breast height (dbh)
and tree height. It assures the
establishment of diversely
structured forests with trees of
different dimensions and ages.
Increasing structural
heterogeneity is an important
tool for promoting stable forests
that are resistant to natural
hazards.
2 Adapt tree species composition
Tree species composition can be
adjusted by selectively
promoting tree species by way of
harvesting measures. Desired
species are left standing in order
to increase their share in favour
of other tree species. In doing so,
tree species composition can be
oriented in a certain direction.
Further adaptation can further be
achieved by planting and
regulating mixed growth.
3 Promote deadwood quantity and
quality
Deadwood promotion refers to
the quantity of deadwood,
expressed in volume per hectare
or number of trees, and to
quality. Deadwood quality is
defined by its dimension,
decomposition and the type,
which can be differentiated into
standing, lying or stumps. The
latter are usually present due to
frequent timber harvesting
measures.
4 Provide habitat structures
Habitat structures can be various
structural elements providing
microhabitats, such as wet and
dry biotopes, piles of branches, or
cairns. They increase structural
diversity and provide habitats for
numerous organisms. Habitat
structures that are present should
be left in place and unaffected by
forestry measures, if not present,
they can be actively created.
5 Increase tree species diversity
A variety of tree species and their
composition increase tree species
diversity of a forest area.
Depending on the local
conditions, preference should be
given to natural regeneration.
Furthermore, additional tree
species can be planted. Mixed
tree species should also be left in
the stand during harvesting
operations in order to ensure
their natural regeneration in the
long term.
6 Conserve habitat trees and
veteran trees
8 Reduce understory density
The reduction of the density in
the undergrowth can be achieved
by reducing stemnumber and
controlling mixed growth. This
measure promotes the stand
stabilization as well as an
increase in growth and can
promote the tree species mixture.
9 Provide unmanaged forest
patches
Forest areas that constitute
habitats worth protecting or
habitats for protected species
should be left undisturbed. This
may relate to either general or
seasonal management
abandonment. In addition, in
unmanaged forest areas, the
decay phase, which does not
usually occur under
management, may be allowed in
unmanaged forest areas.
10 Increase rotation period
The rotation period refers to the
age of the stand up before
harvesting. For uneven-aged
forests it refers to the age of the
individual tree. Increasing stand
age provides habitats for species
that depend on mature forests
and allows the provision of large
scale deadwood.
11 Provide uneven-aged forests
under continuous forest cover
Adaptation of forest management
to ensure uneven forest structures
and continuous forest cover is
achieved through single tree
harvesting. Natural regeneration
can occur simultaneously in small
gaps and soil disturbances are
reduced due to low management
intensity.
12 Avoid forest fragmentation and
habitat isolation
Forest loss, clear cutting and
extensive forest road construction
can lead to fragmentation of the
forests. This should be avoided in
order to maintain the stability of
a forest and ensure the habitat
connectivity.
13 Adapt habitat management for
indicator species
7
Ecological Indicators 122 (2021) 107275
Table 2 (continued )
No. Categories managment measure for biodiverstiy in forests (MM)
Habitat trees are living or dead Forest management should
trees of high ecological value. consider and actively promote
They may have various types of the protection and conservation
holes, rotten parts, many and of indicator species and protected
coarse branches, epiphytic habitats. Protected habitats refer
vegetation such as mosses or to the Habitats Directive or
lichens, or they may be a rare tree national nature conservation
species in the surrounding forest. legislation. Indicator species can
Veteran or mature trees are older be umbrella species or protected
than the rest of the stand. They species according to the Habitats
provide potential habitats and and Birds Directives or national
are left to natural development. nature conservation law.
The use of a group of habitat trees Umbrella species are species that
or veteran trees significantly are selected for conservation
increases the ecological value. decisions, because their
protection implies the protection
of many other species that form
the ecological community of the
respective habitat.
7 Provide spatial heterogeneity at 14 Perform active monitoring
landscape level
At the landscape level, the Active monitoring in forests
structural diversity of forests and refers to the continuous
forest edges refers to varying tree observation of different species
species composition, age classes and processes. It forms the basis
and development stages. This for detecting changes over time.
may include gaps with low forest Forest management can be
cover or different management adapted according to these
intensities and management changes. Monitoring is also used
systems. to evaluate the success of
adaptation measures.
et al., 2009). Possible silvicultural measures to avoid habitat fragmen­
tation and isolation include avoidance of clear cutting (Česonienė et al.,
2019; Iordan et al., 2018; Vangansbeke et al., 2017) and the enabling of
habitat connectivity (Dyderski et al., 2017).
4.2. Canopy and stand structure diversity
Our study shows that a high structural diversity is linked to high
levels of biodiversity, especially in regard to vascular plants, birds and
ground-dwelling species. Silvicultural management measures can
impact the following aspects of forest structure: basal area, canopy cover
and diversity, deadwood, tree species diversity, diameter distribution,
tree age and height, and tree species composition. At the landscape level,
structural diversity of forests and forest edges refers to varying tree
species composition and development stages. This may include forest
areas with varying forest cover or differing management intensities and
management systems. It is also important to integrate adjacent land
cover types, such as agriculture, taking related management intensity
and spatial–temporal changes into consideration. At stand level, struc­
tural diversity can be achieved by ‘reducing stem number and control­
ling mixed growth’ (MM-8), ‘increasing rotation periods’ (MM-10) and
‘providing horizontal and vertical heterogeneity’ (MM-1). These man­
agement measures aimed at the creation of structurally diverse forests
with trees of various ages, diameters and heights, which in turn are
positively associated with an increase in bird, insect and fungi abun­
dance (Standovár et al., 2016).
Canopy cover was identified as an important indicator for manage­
ment, and is measured by the gap size, leaf volume, stand height, and
relative proportion of cover in the landscape. Particularly in coniferous
forests, canopy cover is a confirmed indicator for structural diversity
(Coote et al., 2013). Overall vascular plant species richness increases
and plant species composition changes with the increase of light avail­
ability in the herbaceous layer provided by canopy openness (French
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
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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
of forest management to create uneven forest structures and continuous
forest cover’ (MM-11) can contribute to reducing forest fragmentation,
as well as increasing structural diversity at a larger scale. Sustainable
forest management should therefore seek to mimic natural processes in
order to enhance structural diversity (Doyon et al., 2008; Moretti et al.,
2010). Insect and plant biodiversity in particular benefit from measures
such as retaining part of the deadwood and delaying planting after
harvesting (Müller et al., 2008).
4.3. The ‘no-management‘ approach
Forest management intensity is associated with harvesting intensity
and forest stand management activities focused on wood supply (Levers
et al., 2014). In our review, forest management intensity measures
include the lowering of harvesting intensity, the adaptation of harvest­
ing and forest management methods, and the creation of forest areas
with no management. ‘Providing unmanaged forest patches’ (MM-9)
mainly targets forest habitats with high levels of naturalness that are of
interest for nature conservation, e.g. biodiversity hotspots (Schröter
et al., 2017). Management abandonment may vary in space and time
depending on the objectives and associated species. Bird species survival
and breeding success is increases as a result of seasonal abandonment
and the creation of quiet zones during breeding season (Fernandez-
Juricic and Jokimaki, 2001), while long-term unmanaged forests are
needed to increase macrofungal diversity (Dvořák et al., 2017).
Furthermore, specifications and demands for patch sizes vary greatly.
While Sánchez-Almendro et al. (2018) suggest a favorable unmanaged
forest patch size of above 10 ha, Dyderski et al. (2017) recommend the
preservation of any areas between 0.1 and 10 ha, and Perhans et al.
(2009) argue that even small unmanaged patches between 0.01 and 0.5
ha can represent a “life-boat” for endangered species.
We conclude that the strong link between the IM ‘area with no or low
management’ to IB groups ‘arthropods’, ‘birds’ and ‘fungi’ indicates a
positive effect on the overall biodiversity of forests. The positive effect of
forest abandonment in large forest patches is not confirmed across all
taxa, however (Sever and Nagel, 2019). In fact, many organisms func­
tioning as IB require active management measures for positive devel­
opment (Augustynczik et al., 2019; Cistrone et al., 2015; Hlásny et al.,
2017). Cistrone et al. (2015) report increasing foraging activity of bats in
sustainably managed forests compared to unmanaged forests. Vascular
plant diversity is positively linked to climate induced changes in the tree
species composition of formerly monocultural spruce forests (Hlásny
et al., 2017). Further research and sampling efforts are thus required to
investigate ecological processes in unmanaged versus managed forests
with respect to changing climatic conditions (Sitzia et al., 2017).
4.4. Implications for biodiversity monitoring
The adaptation of management measures for biodiversity requires
‘regular active monitoring’ (MM-14) to assess the effectiveness of
measures, as well as temporal and spatial changes in indicator values
(Table 2). Several different approaches show that the established na­
tional forest inventories (NFI) can provide information related to
biodiversity conservation (Crecente-Campo et al., 2016; Reise et al.,
2019; Thakur et al., 2018). In particular, indicators for the IM group
‘deadwood’ have been monitored and compared over large landscape
scales using NFI data (Rondeux et al., 2012). The comparison of other IM
or IB monitored in NFIs requires careful harmonization efforts, however
(Chirici et al., 2012).

8
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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

Fig. 5. Correlation between indicators for biodiversity and management indi­
cator groups. Ordination (CA) of 32 indicators for biodiversity (IB) based on 7
management indicator groups (IM groups). Plot shows correlation between the
variables and the first two ordination axes based on the length and direction of
vectors. Biodiversity indicators are coloured according to the respective
biodiversity indicator groups (IB groups). Biodiversity indicator numbers and
bi-plot scores are presented in Table 4.
Existing studies have so far focused mainly on structural and species
indicators relating to ecosystem or species diversity. Very few studies
refer to indicators concerning genetic diversity. Nevertheless, the
agement of forest genetic resources will increase in future (Filippos,
2016). The investigation of genetic indicators in sustainable forest
management needs to be explored in future research, especially with
regard to climate change adaptation measures in forests (Loo et al.,
2014). However, such efforts face challenges such as expenses, taxo­
nomic expertise, representativeness and comparability at the national
and international level, depending on the chosen methodology (Bar­
soum et al., 2019). Therefore, monitoring has been commonly applied to
surrogates, such as taxa or habitats, as they can be assessed more easily
and quickly. Nevertheless, applicability is hampered by a lack of infor­
mation, as many of the indicators have not been tested across different
forest types so far.

9
J. Oettel and K. Lapin Ecological Indicators 122 (2021) 107275

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
J. Oettel and K. Lapin
We therefore summarize that the most appropriate indicator species
or groups are those which: (1) have a strong link to a management in­
dicator, (2) are sensitive to changes, and (3) are not related to similar
habitat needs in order to cover different gradients of management in­
fluences. Additionally, further research should focus on biodiversity
indicators that have not yet been studied (or not been studied in depth)
but show high potential through a strong link to a certain management
indicator.
4.5. Application of indicators
In the 162 studies, apart from various general management recom­
mendations, only 6 thresholds for forest management were reported
(Table 5). We thus recognize the need to define evidence-based
threshold levels for biodiversity gains with respect to regional differ­
ences (Humphrey and Bailey, 2012). We highlight that no single indi­
cator approach is sufficient for guaranteeing successful biodiversity
protection in forests. Furthermore, our findings suggest that the selec­
tion of indicators for biodiversity should take three major aspects into
consideration: (1) What are the long-term conservation goals at the local
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
can the forest management be adapted and its success be monitored?
In practice, the formulation of sustainable forest management goals
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
practitioners with an overview of links between different indicators of
biodiversity (IB), associated forest structural components expressed in
management indicators (IM) and corresponding management measures
(MM). In accordance with local and regional conservation goals,
implementation of appropriate measures and monitoring of their success
using IM is possible. In addition, IB should be monitored on a small scale
for control purposes.
Although we focused on the identification of links at the forest stand
level, our results contribute to the discussion on the appropriate level of
management intensity in conservation areas. Forest management can
have positive and negative effects on biodiversity. In the case of certain
biodiversity indicators, such as plants, forest type specific management
was found to be positively linked to occurrence and diversity. It should
to be kept in mind, however, that we lack a comprehensive picture of the
natural dynamics and natural appearance of most European forest types,
and that natural forest dynamics of unmanaged forests may have been
disrupted especially given the lack of knowledge of the primary forest
conditions which are often impossible to reconstruct after centuries of
forest management.
5. Conclusion
This review identified indicator groups for biodiversity and forest
management, revealed their links to silvicultural management mea­
sures, and analyzed the strength of these relationships. The links differ in
evidence and strength; for example, the links between the abundance of
deadwood and saproxylic species or between the stand structure and
birds are very well established, while other taxonomic groups are
underrepresented.
We therefore suggest conducting further research on soil biota, pte­
ridophytes, reptiles, or other potential indicators to close knowledge
gaps on unexplored taxa that may inhibit the attributes of applicable
indicators. Furthermore, the determined links indicate the need to learn
more about the complex interactions of organisms under different
management regimes. First attempts to develop multi-taxa indicators
show reasonable pathways for future applied studies.
Future policy discussions should consider the link between IM and IB
in different forest ecosystems, as well as forest dynamics under the
impact of climate change. This goes hand in hand with the need to
11
Ecological Indicators 122 (2021) 107275
promote interdisciplinary research on indicators for biodiversity and
forest management. We conclude that there is an urgent need for more
precise biodiversity guidelines for forest and conservation practitioners.
Management practices need to reflect the latest scientific outputs, in
order to avoid mismanagement of biodiversity in forest ecosystems.
On the basis of our findings, we identify four important issues for
future research:
• Studies on biodiversity indicators and specific management related
threshold values
• Research on the influence of changing climatic conditions and
associated adaptation measures with regard to biodiversity
indicators
• Investigation of habitat connectivity at the landscape level, taking
other land use types and limiting factors into consideration
• Analysis of the effectiveness of biodiversity management measures,
including financial resources, actual or potential side effects, and
acceptance by stakeholders.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This study was supported by the Austrian Federal Ministry for
Agriculture, Regions and Tourism under the Austrian Rural Develop­
ment Programme 2014-2020 [7.6.1c-III4-40/18]. We would like to
thank Silvio Schüler for his valuable support during the last month and
fruitful discussions, Isabel Georges for her technical assistance, and
Stephan Stockinger for his comments on English language and style that
significantly improved this manuscript. We also greatly appreciate the
constructive comments by two anonymous reviewers.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ecolind.2020.107275.
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