FFGC 05 818474

SYSTEMATIC REVIEW
published: 08 July 2022

doi: 10.3389/ffgc.2022.818474
Tree-Related Microhabitats Are

Promising Yet Underused Tools for
Biodiversity and Nature
Conservation: A Systematic Review
for International Perspectives
Maxence Martin 1,2,3*, Yoan Paillet 4 , Laurent Larrieu 5,6 , Christel C. Kern 7 ,
Patricia Raymond 3,8 , Pierre Drapeau 3,9 and Nicole J. Fenton 1,3
1
Forest Research Institute, Université du Québec en Abitibi-Témiscamingue, Rouyn-Noranda, QC, Canada, 2 Département
des Sciences Fondamentales, Université du Québec à Chicoutimi, Saguenay, QC, Canada, 3 Centre for Forest Research,
Université du Québec à Montréal, Montréal, QC, Canada, 4 Université de Grenoble Alpes, INRAE, LESSEM, Saint Martin
Edited by: d’Hères, France, 5 Université de Toulouse, INRAE, UMR DYNAFOR, CS 52627, Castanet-Tolosan, France, 6 CNPF-CRPF
Pedro Álvarez-Álvarez, Occitanie, Tarbes, France, 7 U.S. Department of Agriculture (USDA) Forest Service Northern Research Station, Rhinelander,
University of Oviedo, Spain WI, United States, 8 Direction de la Recherche Forestière, Ministère des Forêts, de la Faune et des Parcs (MFFP), Québec,
QC, Canada, 9 Département des Sciences Biologiques and Chaire de Recherche, Université du Québec en
Reviewed by: Abitibi-Témiscamingue - Université du Québec à Montréal (UQAT-UQAM) en Aménagement Forestier Durable, Université du
Alan Feest, Québec à Montréal, Montréal, QC, Canada
University of Bristol, United Kingdom
Marco Basile,
Swiss Federal Institute for Forest, Sustainable management of forest ecosystems requires the use of reliable and easy to
Snow and Landscape Research
implement biodiversity and naturalness indicators. Tree-related microhabitats (TreMs) can
(WSL), Switzerland
fulfill these roles as they harbor specialized species that directly or indirectly depend
*Correspondence:
Maxence Martin on them, and are generally more abundant and diverse in natural forests or forests
[email protected] unmanaged for several decades. The TreM concept is however still recent, implying the
existence of many knowledge gaps that can challenge its robustness and applicability.
Specialty section:
This article was submitted to To evaluate the current state of knowledge on TreMs, we conducted a systematic review
Forest Management, followed by a bibliometric analysis of the literature identified. A total of 101 articles
a section of the journal
Frontiers in Forests and Global
constituted the final corpus. Most of the articles (60.3%) were published in 2017 or
Change after. TreM research presented a marked lack of geographical representativity, as the
Received: 19 November 2021 vast majority (68.3%) of the articles studied French, German or Italian forests. The main
Accepted: 21 June 2022 themes addressed by the literature were the value of TreMs as biodiversity indicators,
Published: 08 July 2022
the impact of forest management on TreMs and the factors at the tree- and stand-scales
Citation:
Martin M, Paillet Y, Larrieu L, Kern CC, favoring TreMs occurrence. Old-growth and unmanaged forests played a key role as a
Raymond P, Drapeau P and “natural” forest reference for these previous themes, as TreMs were often much more
Fenton NJ (2022) Tree-Related
Microhabitats Are Promising Yet
abundant and diverse compared to managed forests. Arthropods were the main phylum
Underused Tools for Biodiversity and studied for the theme of TreMs as biodiversity indicators. Other more diverse themes
Nature Conservation: A Systematic were identified, such as restoration, remote sensing, climate change and economy and
Review for International Perspectives.
Front. For. Glob. Change 5:818474. there was a lack of research related to the social sciences. Overall, current research
doi: 10.3389/ffgc.2022.818474 on TreMs has focused on assessing its robustness as an indicator of biodiversity and
Frontiers in Forests and Global Change | www.frontiersin.org 1 July 2022 | Volume 5 | Article 818474
Martin et al. Tree-Related Microhabitats Systematic Review
naturalness at the stand scale. The important geographical gap identified underscores
the importance of expanding the use of the TreMs in other forest ecosystems of the
world. The notable efforts made in recent years to standardize TreM studies are an
important step in this direction. The novelty of the TreM concept can partially explain the
thematic knowledge gaps. Our results nevertheless stress the high potential of TreMs for
multidisciplinary research, and we discuss the benefits of expanding the use of TreMs on
a larger spatial scale.
Keywords: biodiversity indicators, TreMs, habitat trees, biodiversity conservation, naturalness, monitoring, forest
inventory, wildlife habitat
INTRODUCTION are highly-dependant on specific TreMs. Some TreMs such as

cavities can host several hundred taxa, some of which can also
Forests play a key-role in solving the current global issue live in other TreMs or on deadwood. In contrast, dendrotelms
of biodiversity erosion, as they host about two-thirds of the (a cup-shaped concavity that retains water) host very few taxa;
world’s terrestrial biodiversity (World Commission on Forests however, most of these taxa are strictly associated with this type
Sustainable Development, 1999). However, assessing the ability of of TreM (Dajoz, 2007), and dendrotelms are more generally an
sustainable forest management strategies to maintain biodiversity important resource for hydration and nutrition of animal species
is complex (Drapeau et al., 2009; Blicharska et al., 2020) as (Gossner et al., 2020; Kirsch et al., 2021). For this reason, TreMs
exhaustive biodiversity surveys are generally time- and money- have proven to be indicators of forest biodiversity (Paillet et al.,
consuming. Consequently for practical purposes, and despite 2018; Larrieu et al., 2019; Basile et al., 2020), although the direct
contradictory evidence of cross-taxa congruent biodiversity links between TreMs and species occurrence at the stand scale
patterns in forests (Burrascano et al., 2018; Larrieu et al., are not always clear (Asbeck et al., 2021a). The richness and
2018a), biodiversity surveys are often focused on a small group diversity of TreMs, as well as the occurrence of specific types, are
of taxa, generally vertebrates and vascular plants. This limits also relevant indicators of naturalness or old-growthness (Winter
their applicability in forest management and conservation. and Möller, 2008; Michel and Winter, 2009; Vuidot et al., 2011;
Reliable biodiversity proxies for undersurveyed taxa, which Larrieu et al., 2012; Paillet et al., 2017; Asbeck et al., 2021b).
can be easily monitored, are therefore critically required to While some TreMs have been studied for a long time, such as
assess the sustainability of the current anthropogenic impacts dendrotelms (Kitching, 1971) or cavities (Wesołowski, 2007),
on biodiversity in forest ecosystems. Forest management the concept of a list of different microhabitats that represent a
for timber production, and more generally anthropogenic significant part of the forest biodiversity is more recent. Indeed,
disturbances, have caused an important degradation of forests the novelty with the current “TreM concept” is to consider TreMs
worldwide (Puettmann et al., 2009), threatening the habitats, at the stand scale, as a key set of resources for a much wider range
functions, and services forest ecosystems provide. Hence, of taxa, which are functionally linked to each other as well as to
remnant natural forests now play a key role as references for other elements such as deadwood. This more holistic approach
naturalness in degraded forest landscapes, providing knowledge therefore aims at, among other purposes, assessing and orienting
on development processes of critical habitat elements to be forest management strategies that conserve biodiversity.
restored in managed forests (Watson et al., 2018). Forest management and biodiversity conservation both
Evaluating the success of “closer to nature” forest management benefit from exchanges among researchers and practitioners,
strategies (Messier et al., 2015; Puettmann et al., 2015) requires and more generally from the transferability of concepts and the
the use of reliable yet easily applicable indicators. Tree-related assessment of their robustness in different contexts. A quick
microhabitats (TreMs) can fulfill the roles of biodiversity and look at the literature on TreMs suggests, however, that the
naturalness indicators. They are defined as “all distinct and well- concept has developed mainly in Europe, and particularly in the
delineated structures occurring on living or standing dead trees, temperate and Mediterranean regions of that continent (Kraus
that constitute a particular and essential substrate or life site for et al., 2016; Larrieu et al., 2018b). Trees and forests in this
species or species communities during at least a part of their life area demonstrate certain characteristics (e.g., tree size, TreM
cycle to develop, feed, shelter or breed” (Larrieu et al., 2018b). They development dynamics, history of anthropogenic disturbance)
can be regrouped in seven main forms, based on morphological that may differ from other territories and current knowledge
characteristics, and use by the associated taxa: (i) cavities, (ii) on TreMs may not be directly applicable outside the regions
tree injuries and exposed wood, (iii) crown deadwood, (iv) where they are currently studied. For example, Martin et al.
excrescences, (v) fruiting bodies of saproxylic fungi and fungi- (2021a) highlighted that the TreMs size thresholds commonly
like organisms, (vi) epiphytic, epixylic, and parasitic structures used to survey TreMs in temperate forests may not be easily
(e.g., nest), and (vii) exudates (Figure 1; Larrieu et al., 2018b). applicable in some boreal regions due to the smaller tree
They thus represent a wide variety of structures, necessary for size. Evaluations of the applicability of the TreM concept by
many animal, vegetal or fungal species, and several species comparing new territories (United Sates, Iran) with European
FIGURE 1 | Illustration of the seven TreM forms defined by Larrieu et al. (2018b), and link between TreM forms and taxa in European temperate and Mediterranean
forests. Italic text in brackets indicates the specific TreM types represented here. Taxa pictures indicates that several species of the taxonomic group occur; these
species are not necessarily strictly associated with the TreM group. Adapted from Larrieu et al. (2018b) and Bütler et al. (2020). Tree drawing by Valentina Buttò and
taxa drawings by Celine Emberger.
forests have however been conducted in recent years (Asbeck MATERIALS AND METHODS
et al., 2020a; Jahed et al., 2020). In line with these efforts, this
article conducts a systematic review of the scientific literature Systematic Review
on TreMs to identify research gaps, for example in terms of The systematic review was conducted in three steps.
geographical coverage or themes. Identification of the scope and First, we performed a search on the specialized search
limits of the current knowledge on TreMs will facilitate the engines Scopus (www.scopus.com) and Web of Science
prioritization of research objectives and the application of this (www.webofscience.com) to find literature referring to TreMs.
concept in sustainable management of forest ecosystems. We Identifying the relevant keywords for the search is a key part
assumed that (1) the study of TreMs currently covers a limited of this step (Atkinson and Cipriani, 2018; Foo et al., 2021).
geographical area and few studies are available outside of Europe, A wide diversity of terms, however, has been used to refer to
and that (2) due to the recent nature of this concept, the majority TreMs before the terminology became more homogenized
of studies on TreMs have focused on validating their role as an in recent years. We therefore relied on the literature already
indicator of biodiversity and naturalness. known by the authors to identify the different terms that have
been used to refer to TreMs, here presented in the singular Winter, 2009; Michel et al., 2011; Vuidot et al., 2011; Larrieu and
form: TreM (Jahed et al., 2020), tree related microhabitat Cabanettes, 2012; Regnery et al., 2013a; Larrieu et al., 2014a,b,
(Larrieu et al., 2021), tree microhabitat (Paillet et al., 2015), bark 2017; Winter et al., 2015). We considered these ten articles as
microhabitat (Michel et al., 2011), microhabitat (Winter and landmark research, because they were more likely to synthetize
Möller, 2008), microhabitat-bearing tree (Regnery et al., 2013b), current knowledge of their time on a wide diversity of TreMs, and
dendromicrohabitat (Madera et al., 2017), special tree structure to be cited by further TreM-studies. The backward and forward
(Winter et al., 2005) or structural diversity characteristic (Lilja search led to the identification of 1,133 articles, including 543
and Kuuluvainen, 2005). We used wildcards (∗ ) to account for articles that were absent from the first step. We used the same
various word spellings. Because some of the identified terms method and criteria as before to make the article selection. A total
were relatively generic (e.g., “microhabitat”) or can be a part of of 19 articles were added to the corpus at the end of the second
another word (e.g., “TreM”), we also add as a constraint a 5- step (total number of articles in the corpus = 99; Figure 2).
words proximity with “tree∗ ” or “forest∗ ,” Similarly, for the terms As a third step, we finally compared the results of the
“special tree structure” and “structural diversity characteristics,” corpus with the literature related to TreMs already known by
constrained these words as a single expression rather than the authors and fulfilling our selection criterion. We identified
individual words. The literature search was conducted the two articles that were absent from the corpus (Larrieu et al.,
27th September 2021 using the following query, here written 2019; Gosselin and Larrieu, 2020), probably because TreMs were
following the Scopus syntax: studied through the Index of Biodiversity Potential (Larrieu and
[TITLE-ABS-KEY ((trem OR trems) W/5 (tree∗ OR forest∗ )) Gonin, 2008), an index that considers TreMs among other forest
OR TITLE-ABS-KEY (tree W/5 microhabitat∗ ) OR TITLE-ABS- attributes (Figure 2). These articles were consequently added to
KEY (dendromicrohabitat∗ ) OR TITLE-ABS-KEY (bark W/5 the corpus (total number of articles in the corpus = 101).
microhabitat∗ ) OR TITLE-ABS-KEY (microhabitat W/1 bearing
W/1 tree∗ ) OR TITLE-ABS-KEY (structural W/1 diversity
W/1 characteristic∗ ) OR TITLE-ABS-KEY (special W/1 tree Bibliometric Analysis
W/1 structure∗ )]. To better highlight the general context of TreMs-related
Once the duplicates removed, a total of 626 articles were literature we conducted a bibliometric analysis (Donthu et al.,
identified at this stage (Figure 2). We then read the title and 2021) on the 101 articles selected for our corpus. For each article,
the abstract, as well as the full text if necessary, of each articles we extracted the authors name, the date of publication, the
to determine if they fulfilled the following criteria (hereafter, “Keywords Plus” (i.e., the keywords defined by the publisher)
“selection criterion”): (i) research article; we nevertheless as well as the countries covered by the data. We consider the
identified literature reviews related to TreMs for a subsequent countries covered by the data rather than the country of the
step, (ii) TreMs had to be studied, not just mentioned, (iii) at least corresponding author, which is commonly used in bibliometric
2 TreM forms following the typology of Larrieu et al. (2018b) analyses, because the latter is not necessarily the same as the
were considered, although without any size or abundance limits; country studied and several countries can be covered by the
this criterion serves to remove all articles focusing specifically same study. Further, we chose to use the Keywords Plus rather
on one type of TreM [e.g., cavities Remm and Lõhmus (2011)], than the authors’ Keywords because the former are considered
without considering TreMs as concepts, (iv) all TreM forms to better describe the articles than the latter (Zhang et al., 2016).
studied are recognized as TreMs as defined by Larrieu et al. There were also fewer articles in the corpus from which keywords
(2018b), and not as an element without its own habitat value. A plus were unavailable (n = 14) compared to authors keywords
single researcher (M. Martin) reviewed all the articles, but articles (n = 22).
for which the correspondence to the criteria was uncertain were The manual creation of a thesaurus based on the keywords
identified so that the final selection was made among all the plus also allows a better grouping of the themes that revolve
authors. A total of 80 articles constituted the corpus at the end around a subject (Yang et al., 1998). First, we identified and
of the first step (Figure 2). grouped keywords whose difference was only due to spelling
It was possible that some relevant articles related to TreMs (e.g., “tree” and “trees,” “Abies alba” and “Abies alba Mill”).
were not identified in the previous step. For this reason, Foo Second, we selected only the keywords that occurred at least three
et al. (2021) suggest to perform a backward and forward search times in the corpus. Preliminary tests showed that lowering this
based on pertinent reviews and landmark articles, i.e., a review threshold strongly increased the occurrence of unique themes,
of the references that are cited or that cite these selected articles. causing noise in the subsequent analyses. Third, we indexed
We thus performed a backward and forward search as a second the keywords when deemed relevant to avoid synonyms and
step of our review. We identified three relevant literature reviews to highlight explicit links [e.g., “Abies alba” = “Species/Genera
that specifically study TreMs (Larrieu et al., 2018b; Asbeck et al., (Tree), “Arthropod” = “Fauna (Invertebrate),” Aitchison et al.
2021a; Kõrkjas et al., 2021a). For other landmark articles that (2000)]. Depending on the quality of the links between words,
were not reviews, we selected ten research articles presenting different degrees of clustering were given to the keywords. For
a detailed TreM typology [i.e., more than four different TreM example, the word fauna was treated separately because it is
forms, so more than half of the seven forms identified by a very generic word. On the contrary, the words arthropod,
Larrieu et al. (2018b)] and published before Larrieu et al. (2018b) beetle, coleopteran, or diptera were associated with the group
homogenized typology (Winter and Möller, 2008; Michel and Fauna (Invertebrate).
FIGURE 2 | PRISMA diagram of the systematic review conducted.
To analyze the co-occurrence of the different themes identified

in the thesaurus, we performed a Non-metric Multidimensional
Scaling (NMDS) analysis based on the theme occurrence
within the articles. To limit the noise caused by rare or
very frequent themes we first removed themes for which the
frequency in the corpus was below the 20th percentile or
above the 80th percentile of theme frequency. We applied a
NDMS on two dimensions using the Jaccard distance and 1,000
iterations, with the metaMDS function of the vegan R-package
(Oksanen et al., 2018).
To analyze the authors co-occurrence, we first identified the
numbers of articles published by each author in the corpus. For
this analysis we kept only the authors that published at least three
articles in the corpus, as we considered that a lower number
of articles published meant low or no co-occurrence. The co- FIGURE 3 | Number of articles from the corpus by publication year. The year
2021 was still incomplete at the time the bibliometric study was conducted
occurrence of the selected authors was identified using Veech’s (27th September 2021), which may partly explain a lower value. One article
probabilistic model of species co-occurrence (Veech, 2013). The already available at the date of the bibliometric study belongs to an issue for
analysis was performed using the cooccur function of the cooccur which the publication year is 2022 (Przepióra and Ciach, 2022), explaining the
R-package (Griffith et al., 2016). All the analyses were performed unique value observed for this year.
using the R programming language (R Core Team, 2019).
RESULTS extent (11.8%) (Figure 4). For all of the 26 remaining countries,
we identified between 1 and 6 articles studying TreMs on
The oldest article identified in the corpus was published in their territory.
2000 (Lindenmayer et al., 2000; Figure 3). The number of A total of 351 authors contributed to the articles from
articles published annually remained low (<4 articles/year) the corpus. Among them, 45 authors published at least
until 2013, where it progressively increased to reach a three articles (12.8% of the total number of authors;
maximum in 2020 (20 articles published). The study areas Table 1). Using Veech’s probabilistic model of species
of the articles from the corpus were located in 30 different co-occurrence, we identified three author groups: (A)
countries (Supplementary Material 1). The dominant countries Larrieu L, Cabanettes A, Bouget C, and Deconchat M (all
were France (32.6%), Germany (30.6%) and Italy to a lower authors main affiliations located in France), (B) Asbeck
FIGURE 4 | Map of the number of articles from the corpus covering world countries. Gray fill indicates no article identified for the country, blue indicates seas and
oceans.
T and Bauhus J (all authors main affiliations located in DISCUSSION

Germany), and (C) Paillet Y, Gosselin F, and Archaux F
(all authors main affiliations located in France) (Table 1, Tree-Related Microhabitats: A Recent and
Supplementary Material 2). For all the 35 remaining authors, Developing Ecological Concept
we identified no significant associations. Research on TreMs is concentrated in a narrow number of
We indexed the Keywords Plus in a total of 40 themes countries and research groups from Western Europe, supporting
(Table 2, Supplementary Material 3), with four of them our first assumption. This small geographic range of the TreM
occurring in more than half of the articles from the corpus concept is consistent with its relatively young age, as the oldest
for which keyword plus were available (Management (Forest), study identified was published in 2000 (Lindenmayer et al., 2000)
Biodiversity, Microhabitat and Country/Territory) and five and more than half of the articles from the corpus were published
of them occurring in three articles or less (Climate, Lichen, in 2017 or after. The lack of consistent TreM terminology before
Natural, Climate change and Economy). A total of 26 themes, 2008, e.g., special tree structure (Winter et al., 2005) or structural
identified in 76 articles were kept for the NMDS (Figure 5). diversity characteristic (Lilja and Kuuluvainen, 2005), illustrates
We observed that the NMDS1 axis distributed the themes well the juvenile character of this concept. Admittedly, numerous
in two main groups: general forest attributes for the positive research projects on individual TreM forms existed before 2000,
values [e.g., Heterogeneity, Dynamics (Forest)], and forest forming the foundations of what will become the TreM concept.
species or their monitoring [e.g., Fauna (Vertebrate), Flora, For example, Ricarte et al. (2009) in Mediterranean forest or
Fauna, Survey] for the negative values. This suggest that this Ranius and Jansson (2000) in Sweden provided detailed reviews
axis distinguishes studies focused on different scales, from the of the different TreMs individually used by saproxylic beetles and
landscape (positive values) to local habitat (negative values). hoverflies. During the literature search, we also identified articles
For the NMDS2 axis, positive values regrouped themes related studying one specific TreM form in regions for which there was
to the methodology (e.g., Prediction/Probability, Methodology, little or no other TreM research, such as Africa (Pringle et al.,
Survey) while negatives values grouped more ecological concepts 2015), South America (Whitfield et al., 2005; Ibarra et al., 2020)
(e.g., Ecology, Community, Disturbance). This suggests that this or Asia (Patel et al., 2021). Ecological research generally suffers
second axis discriminates studies related to the methodological from an important lack of representativeness at the global scale,
aspects of TreMs research (positive values) from those that with Global North countries being dramatically overrepresented
are more centered on the ecological perspective. As a result, in part because of better access to funding sources (Martin et al.,
the combination of the two NMDS axes divides the themes 2012; Wohner et al., 2021). The fact that most TreM-related
in four main groups: forest complexity and heterogeneity research comes from Western European countries is therefore
(positive NDMS1 and NDMS2 values), general ecological consistent with this global trend.
concepts (positive NDMS1 and negative NDMS2 values), Current research on TreMs focuses primarily on the themes
methodological approaches (negative NDMS1 and positive of the value of TreMs as biodiversity indicators (37.6% of
NDMS2 values), and biodiversity (negative NDMS1 and the corpus; Table 3) or the effect of forest management on
NDMS2 values). TreMs abundance and diversity (34.5% of the corpus; Table 3),
TABLE 1 | Authors that published at least three articles in the corpus and TABLE 2 | Number and frequency of articles presenting themes identified from
co-occurrence group. the Keywords plus.
Rank Author # Articles Group Rank Theme # Articles Frequency (%)
1 Larrieu L 20 A 1 Management (forest) 60 59.4

2 Bouget C 13 A 2 Biodiversity 59 58.4
3 Paillet Y 12 C 3 Microhabitat 57 56.4
4 Asbeck T 10 B 4 Country/territory 53 52.5
5 Cabanettes A 10 A 5 Species/genera (tree) 49 48.5
6 Bauhus J 9 B 6 Indicator 48 47.5
7 Marchetti M 9 7 Ecosystem 43 42.6
8 Winter S 9
8 Protection/conservation 42 41.6
9 Gosselin F 7 C
9 Fauna (invertebrate) 28 27.7
10 Lombardi F 7
10 Deadwood 27 26.7
11 Tognetti R 7
11 Structure (forest) 23 22.8
12 Archaux F 6 C
12 Methodology 20 19.8
13 Muller J 6
13 Tree 20 19.8
14 Svoboda M 6
14 Tree (characteristics) 19 18.8
15 Basile M 5
16 Deconchat M 5 A 15 Fauna (vertebrate) 17 16.8
17 Parisi F 5 16 Land use 17 16.8

18 Parmain G 5 17 Saproxylic 14 13.9
19 Gilg O 4 18 Fungi 13 12.9
20 Kozak D 4 19 Structure (landscape) 10 9.9
21 Pyttel P 4 20 Old-growth 9 8.9
22 Augustynczik ALD 3 21 Prediction/probability 9 8.9
23 Campanaro A 3 22 Disturbance 8 7.9
24 Chirici G 3 23 Dynamics (forest) 8 7.9
25 Courbaud B 3 24 Flora 8 7.9
26 Debaive N 3 25 Community 7 6.9
27 Frey J 3 26 Ecology 7 6.9
28 Guilbert E 3 27 Habitat 7 6.9
29 Janda P 3 28 Plant (general) 7 6.9
30 Jonker M 3
29 Survey 7 6.9
31 Kameniar O 3
30 Article 5 5.0
32 Kraus D 3
31 Fauna 5 5.0
33 Lachat T 3
32 Restoration 5 5.0
34 Lasserre B 3
33 Forest 4 4.0
35 Martin M 3
34 Heterogeneity 4 4.0
36 Michel AK 3
35 Remote sensing 4 4.0
37 Mikolas M 3
36 Climate 3 3.0
38 Nagel TA 3
39 Nusillard B 3 37 Lichen 3 3.0
40 Sarthou JP 3 38 Natural 3 3.0
41 Schuck A 3 39 Climate change 2 2.0
42 Storch I 3 40 Economy 2 2.0
43 Svitok M 3
The frequency was calculated using the total number of articles for which Keywords plus
44 Synek M 3 were available (n = 84 articles), and not the total number of articles in the corpus.
45 Trotsiuk V 3
A same letter indicates a same co-occurrence group.

European managed forests (Stokland et al., 2012; Burrascano
et al., 2013). It is also consistent with the lack of knowledge
supporting our second assumption. These main themes are regarding invertebrate populations compared to vertebrates
consistent with the core concept of TreMs, which has been and vascular plants (Newbold, 2010; Feldman et al., 2020).
developed as an indicator of forest biodiversity that can be Interestingly, themes related to fungi, bryophytes and epiphytes
integrated into routine forest surveys (Larrieu et al., 2018b, (here regrouped under the theme “Flora”) as well as lichen were
2021; Reise et al., 2019; Asbeck et al., 2021a). The importance far less abundant. This implies that knowledge linking these
of the themes “Conservation/protection,” “Fauna (invertebrate),” taxa with TreMs is still scarce. It is important to note, however,
and “Deadwood” is congruent with both the current threats that research on the relationship between deadwood (standing
to many species caused by the depletion of deadwood in or downed) and fungi or lichens is abundant (Stokland et al.,
2012). It seems likely that much of this knowledge could be at The important cultural and social values of very large trees and
least partially applied to the TreM concept. Similarly, lichens and natural forests, i.e., tree and forests more likely to exhibit TreMs,
fungi can be considered in certain cases as TreMs, so it will be is also internationally recognized (Blicharska and Mikusiński,
important to distinguish between studies where these taxa are 2014; Watson et al., 2018). This result hence underscores the still
considered as TreMs per se or as TreM users. underdeveloped potential of TreMs for social sciences, e.g., in
There was no theme directly related to the factors explaining terms of importance to Indigenous communities or influence on
TreM presence, abundance and diversity at the tree scale, the feeling of naturalness.
although it is an important part of TreM research. When reading The low frequency of the “Old-growth” and “Natural” themes
the manuscripts of the corpus, we notice however that this topic can result to a certain extent from the scarcity of natural forests
is particularly recurrent (32.7% of the corpus; Table 3). The in Western Europe (Sabatini et al., 2021). This also explains
absence of a specific theme is probably because this subject is why forests taken as “natural references” were often forests
often mixed with those of TreMs as an indicator of biodiversity unmanaged for a given period of time (e.g., Vuidot et al.,
or of the impact of forest management on TreMs (48.4% of the 2011; Packalen et al., 2013; Lelli et al., 2019; Marziliano et al.,
articles identified as addressing the question of TreM presence; 2021; Schall et al., 2021). Even if forests, independently of
Table 3). Overall, larger and senescent or dead tree are more their management status, remain the main study area for TreM
likely to bear many TreMs (e.g., Michel et al., 2011; Paillet et al., research, we identified a few number of studies focusing of TreMs
2019; Asbeck et al., 2021b; Kõrkjas et al., 2021b; Martin et al., in urban areas (Großmann et al., 2020), in orchards (Parisi et al.,
2021b;). For a same diameter at breast height, hardwoods tend 2020b), or in agricultural landscapes (Parmain and Bouget, 2018).
to present a higher number and diversity of TreMs (Larrieu and This highlights how TreMs can be used in many research projects
Cabanettes, 2012; Bouget et al., 2014a; Paillet et al., 2019; Jahed related to trees, and not only in forests.
et al., 2020; Asbeck et al., 2021b; Marziliano et al., 2021). At the Finally, the concentration of TreM research in Europe, and
stand scale, we generally observe the higher TreMs richness and specifically Western Europe, implies that knowledge on TreMs in
diversity in old and “natural” (i.e., either old-growth, primary or open biomes with dispersed trees (e.g., savannas) absent or rare
intact) forests (9.9% of the corpus; Table 3) or formerly managed in Europe is inexistent. We observed that three forest biomes (i.e.,
forests untouched over several decades (16.8% of the corpus; temperate broadleaf or mixed forest, temperate coniferous forest
Table 3) compared to younger and managed forests. TreMs in and Mediterranean forest) are overrepresented in the corpus,
general or some specific TreM types could thus be used as while for boreal forests a small sample of European and North
naturalness indicators (Winter, 2012), although the difference American research are available (Lilja and Kuuluvainen, 2005;
between natural or abandoned forest and managed forests can Kõrkjas et al., 2021b; Martin et al., 2021a), and Russia is absent.
be sometimes more contrasted (Larrieu et al., 2014b; Sever and
Nagel, 2019; Martin et al., 2021a,b). For example, the TreM form
“Tree injuries and exposed wood” can be abundant in managed Benefits in Expanding the TreM Concept:
forests due to injuries caused by logging activities. Other factors An Example in North America
influencing TreMs have been tested, such as local climatic and As illustrated by our results, few TreM studies have been
topographic conditions (Paillet et al., 2019; Asbeck et al., 2021b), conducted in North America (Franklin et al., 2000; Zielinski
spatial patterns (Kozák et al., 2018; Asbeck et al., 2019, 2020b; et al., 2004; Vonhof and Gwilliam, 2007; Michel and Winter,
Martin et al., 2021b) or the influence of tree age (Kõrkjas et al., 2009; Michel et al., 2011; Martin and Raymond, 2019; Asbeck
2021b), but with less marked results. et al., 2020a; Großmann et al., 2020; Martin et al., 2021a,b). Since
Many of the less frequent themes represented rather generic most of the authors of this article are more familiar with this
ideas [e.g., “Ecology,” “Habitat,” “Plant (General)”]. Some of these area, we will use North America as an example to discuss the
themes, however, indicated specific fields of research that are still value of extending the TreM concept beyond Western Europe.
little considered from the perspective of TreMs, notably “Remote This, however, also applies for all territories with forested biomes
sensing” (Bagaram et al., 2018; Ozdemir et al., 2018; Rehush et al., similar to those of Western Europe, for example the temperate
2018; Asbeck et al., 2019; Frey et al., 2020; Santopuoli et al., 2020), forests of South America, Asia or Oceania. The numerous
“Restoration” (Bouget et al., 2014b; Burgar et al., 2015; Larrieu research projects conducted in temperate forests in Europe, but
et al., 2017), “Climate change” (Augustynczik et al., 2019, 2020), also in Iran and North America, point toward emphasizing the
and “Economy” (Rosenvald et al., 2019). relevance of the TreM concept in temperate forests in general.
We can observe that there are no themes related to social For tropical forests and savannas, specific questions arise with
and cultural perspectives of TreM. To a certain extent, it is regards to the applicability of the TreM concepts in these
possible to consider the study related to choice of retention ecosystems. For reasons of clarity, this subject is discussed in a
trees, partly based on TreMs, between different professional dedicated section.
groups in “marteloscopes” (i.e., tree marking training sites) as Many North American studies have already identified the
social research (Cosyns et al., 2019, 2020; Santopuoli et al., microhabitats of specific taxa, for example lichens and fungi
2019; Joa et al., 2020). TreMs and tree defects are indeed (e.g., Goward and Arsenault, 2018), arthropods (e.g., Schowalter,
two close concepts (Martin and Raymond, 2019), that can 2017), or birds and mammals (e.g., Drapeau et al., 2009).
result in conflicts between forest users as they are seen from Similarly, tree defect surveys are regularly used in certain
different perspectives (e.g., production, conservation, aesthetic). regions of North America to describe forest stand quality and
FIGURE 5 | Biplot of the results of the NMDS on the first and second ordination axes (NMDS1 and NDMS2, respectively). Black dots represent themes (n = 26), and
the number in brackets indicates the number of articles for which the theme was identified.
partially capture the TreM concept (Martin and Raymond, 2019). are common to both continents (e.g., Picea, Abies, Acer, or
Although TreMs are still little studied as a set of key resources Quercus). This could help to assess the differences, similarities
at the stand scale, there is nevertheless a solid scientific basis for and predispositions for TreM development at the tree genus
the concept, and routine forestry practices already in use could level. Similarly, the rainforests of northwestern America have few
result in the rapid uptake of TreMs in both research and forest equivalents in Europe in terms of structure and composition, but
management in North America. some tree species have been introduced in Europe for production
Most of Europe’s forests either have a long history purposes. Michel et al. (2011) observed very specific bark TreMs
of management or are recent forests resulting from the (corresponding to the epiphytic, epixylic, and parasitic form) on
abandonment of former agricultural land. Forest management Douglas fir trees (Pseudotsuga menziesii var. menziesii) in these
and natural disturbance control also truncate significant parts of forests, due to the large dimensions and characteristics of the bark
natural forests dynamics in European forested landscapes of this species. These results underline the possibility of further
(Kuuluvainen, 2009; Sabatini et al., 2020). In contrast, extending our knowledge of TreMs by studying North American
natural forests and those that have been little influenced by forests as new TreMs may be defined and a better understanding
industrialization are much more abundant in North America of TreMs that are rare in Europe can be gained.
compared to Europe, particularly in Canada and in the western From a social sciences’ perspective, there is in North America
United States (Ellis, 2011; Venter et al., 2016; Potapov et al., an increased public awareness to subjects related to trees and
2017), providing interesting references for TreM research. As forests. Forests must now provide services other than timber
a counterpoint to the natural or near-natural forest of North production, such as aesthetical, recreational or spiritual services
America, the forests of Europe provide varied examples of (Sutherland et al., 2016; Siry et al., 2018). Traditional indigenous
long-term anthropogenic impacts on TreMs, ranging from knowledge is also increasingly considered in forest management
close-to-nature silviculture to the alternance between a forest planning (McGregor, 2002; Bélisle and Asselin, 2020; Bélisle
and an agricultural state (Forest Europe, 2015; Jaroszewicz et al., et al., 2021), with the rationale of moving away from a purely
2019). These studies could therefore help to better estimate how western forest management paradigm. The value of some habitat
past and current forest management strategies may influence trees (i.e., cavity trees) is widely recognized in North America
TreMs in North America. (DeGraaf and Shigo, 1985; Tubbs et al., 1987; Ontario Ministry
Some forests in North America are defined by specific of Natural Resources, 2004) but many TreMs are still seen as
characteristics that are not found in Europe, but many genera defects (Martin and Raymond, 2019). The broader use of the
TABLE 3 | List of the articles from the corpus and of the topics addressed.
Topic addressed
Article Relevance as Impact of Factors Managed vs. Managed vs. Other topics
biodiversity management explaining Natural Unmanaged
indicator TreM
occurrence
Asbeck et al. (2019) X X X

Asbeck et al. (2020b) X X
Asbeck et al. (2020a) X
Asbeck et al. (2021b) X X X X
Asbeck et al. (2021c) X
Augustynczik et al. (2019) X X
Augustynczik et al. (2020) X X
Bagaram et al. (2018) X
Basile et al. (2020) X
Bouget et al. (2013) X
Bouget et al. (2014b) X X X X
Bouget et al. (2014a) X X
Burgar et al. (2015) X X
Buse et al. (2007) X
Cosyns et al. (2019) X
Cosyns et al. (2020) X
Courbaud et al. (2017) X
Cours et al. (2021) X
Demant et al. (2020) X
Frey et al. (2020) X
Fritz and Heilmann-Clausen X
(2010)
Gosselin and Larrieu (2020) X
Großmann et al. (2018) X X
Großmann et al. (2020) X X X
Herrault et al. (2016) X
Jahed et al. (2020) X
Janssen et al. (2016) X
Joa et al. (2020) X
Johann and Schaich (2016) X X
Kameniar et al. (2021) X
Khanalizadeh et al. (2020) X X X
Knuff et al. (2020) X
Kozák et al. (2021) X
Kozák et al. (2018) X X
Kõrkjas et al. (2021b) X X X X
Langridge et al. (2019) X
Larrieu et al. (2009) X
Larrieu and Cabanettes (2012) X
Larrieu et al. (2012) X X
Larrieu et al. (2014a) X
Larrieu et al. (2014b) X X
(Continued)
TABLE 3 | Continued
Topic addressed
indicator TreM
occurrence
Lassauce et al. (2013) X X

Leidinger et al. (2020) X
Lelli et al. (2019) X X X
Lilja and Kuuluvainen (2005) X X
Lindenmayer et al. (2000) X
Lombardi et al. (2018) X
Martin and Raymond (2019) X X
Martin et al. (2021a) X
Martin et al. (2021b) X X X X
Marziliano et al. (2021) X X X
Menkis et al. (2020) X
Michel and Winter (2009) X X X
Michel et al. (2011) X
Müller et al. (2014) X
Ouin et al. (2015) X X
Ozdemir et al. (2018) X
Paillet et al. (2015) X
Paillet et al. (2017) X X X
Paillet et al. (2018) X X X
Paillet et al. (2019) X X
Parisi et al. (2016) X
Parisi et al. (2020a) X
Parisi et al. (2020b) X X
Parmain and Bouget (2018) X X
Percel et al. (2018) X
Percel et al. (2019) X
Plowman et al. (2020) X
Prinzing (2005) X
Przepióra and Ciach (2022) X
Puverel et al. (2019) X
Regnery et al. (2013a) X
Regnery et al. (2013b) X X X
Rehush et al. (2018) X
Reise et al. (2019) X
Rosenvald et al. (2019) X X X
Rotheray et al. (2001) X
Rouvinen et al. (2002) X X
Russo et al. (2004) X
Šálek et al. (2017) X
Santopuoli et al. (2019) X
Santopuoli et al. (2020) X
Schall et al. (2021) X X
Sefidi and Copenheaver X X
(2020)
Sever and Nagel (2019) X X
(Continued)
TABLE 3 | Continued
Topic addressed
indicator TreM
occurrence
Standovár et al. (2016) X

Vonhof and Gwilliam (2007) X
Vuidot et al. (2011) X X X
Winter et al. (2005) X X
Winter and Möller (2008) X X X
Winter and Brambach (2011) X
Winter et al. (2015) X X X
Zehetmair et al. (2015b) X
Zehetmair et al. (2015a) X
Zielinski et al. (2004) X
For reasons of concision, we only included the five most common topics (87% of the articles addressed at least one of these topics) and the remaining ones have been grouped in
the “Other topics” column. “Natural forests” refers to forests where there is no evidence of past forest management, while “unmanaged forests” refers to forests that were previously
managed but have been abandoned for at least several decades.
TreM concept in North America could therefore be a step toward biodiversity have been carried out on isolated trees in agricultural
improving the balance between ecological, economic and social landscapes in Europe (Parmain and Bouget, 2018; Froidevaux
forest services. et al., 2022), highlighting that these indicators can also be relevant
outside of closed-canopy forests.
Is the TreM Concept Applicable in Tropical Overall, the concept of TreMs is potentially applicable across
all forest ecosystems, but some challenges related to these
Forests and Savannas? indicators may be exacerbated in certain contexts, in particular
None of the studies included in our literature review focused on
the tropical forests. The previously identified gap between
tropical forests or savannas, which may raise questions about
the financial resources allocated to research in countries of
the applicability of the TreMs concept in these contexts. This
the Global North compared with other can further reinforce
does not mean, however, that TreMs are absent from these
these challenges. Thus, practical constraints seem to be the
areas or have no ecological value. As part of our literature
main limitation to the application or evaluation of the TreM
review, we identified studies of species dependent on individual
concept in tropical forests and in savannas. The relative novelty
TreMs conducted in the tropical forest (Whitfield et al., 2005;
and confidentiality of this indicator may also help explain
Cockle et al., 2012; Carvajal-Ocampo et al., 2019) and in
its use only in a limited number of forest ecosystems. A
the savanna (Pringle et al., 2015; Haddad, 2016). It is also
wider dissemination of the TreM concept may facilitate the
likely that new TreMs absent from the Larrieu et al. (2018a)
development of research projects exploring their ecological
typology can be observed in these areas, such as bromeliads
relevance in more meridional forests.
(Rogy et al., 2019). However, the high biodiversity and turnover
that can characterize some tropical forests can make it more
complex to identify clear links between TreMs and different CONCLUSION AND PERSPECTIVES
taxa. Identifying these relationships in comparatively “simpler”
temperate forests is already challenging, as they demand adapted TreMs is still a recent yet rapidly expanding ecological concept
TreM and species surveys (Asbeck et al., 2021a). The structural that can serve as a useful biodiversity and naturalness indicator.
complexity that can define tropical forests (i.e., very tall trees, However, we identified many gaps in current TreM research,
high number of canopy layers) is also a potential challenge for both in terms of geographical extent (most of the existing
TreM identification, but current research on individual TreMs research comes from Western Europe, representing a limited
in these forests demonstrates that such surveys are possible. set of biomes, tree genera, and disturbance history) or in
The research conducted in the temperate rainforest of North themes addressed (focus on the value of TreMs as biodiversity
America (Michel and Winter, 2009), characterized by very tall indicators, the impact of forest management on TreMs and the
trees, also underlines that tree height poses a challenge for TreM factors explaining TreM occurrence), supporting, respectively,
surveys but is still feasible. The continuous improvement of our two assumptions. Extending the TreM concept to a larger
technologies such as LiDAR can also greatly facilitate the study geographical scale and a greater diversity of themes will therefore
of the characteristics of very tall trees (Disney et al., 2020). certainly be beneficial in strengthening the robustness and
Regarding savannas, several research on TreMs and the related applicability of this indicator.
The homogenized TreM typology proposed by Larrieu et al. provide a significant amount of data on a large spatial scale. They
(2018b) can be seen as a major step toward a greater utilization require, however, sound communication and pedagogical work
of the TreM concept. Previous research often used “ad hoc” from the scientific community to ensure data quality. This citizen
typologies, with specific TreM classes and size thresholds, thus science approach would also raise public awareness about the
limiting comparisons and the possibility of performing syntheses importance of TreMs for forest biodiversity and more generally
and meta-analyses without degrading the information. Larrieu about the importance of natural forests, particularly old seral
et al. (2018b) typology is thus expected to serve as a basis for new stages that harbor TreMs.
TreM studies in Europe and beyond. This typology is however
designed for temperate and Mediterranean forests, underscoring DATA AVAILABILITY STATEMENT
that research in new areas and biomes will be useful to test
its relevance and robustness. The hierarchical structure of this The datasets presented in this study can be found in online
typology is precisely designed to facilitate the inclusion of new repositories. The names of the repository/repositories and
TreMs, while avoiding the creation of new sub-typologies that accession number(s) can be found at: https://figshare.com/
would limit the replicability of studies. Accordingly, it provides articles/dataset/Data_Systematic_Review_Tree-Related_
a further step toward establishing a relevant typology for all Microhabitats/17033435.
forest ecosystems.
The need to evaluate the robustness of current TreM AUTHOR CONTRIBUTIONS
typologies and to extend their scope to new contexts also
highlights the importance of international collaborations. MM, YP, and LL conceived the ideas, designed methodology,
Combining the experience gained from the study of TreMs and collected the data. MM performed the analyses and wrote
with knowledge of the local characteristics of forests in the first draft of the manuscript. MM, YP, LL, CK, PR, PD,
different regions will certainly facilitate new collaborations and NF interpreted the results. YP, LL, CK, PR, PD, and NF
and management strategies. Similarly, interdisciplinary research contributed critically to the drafts and gave final approval for
should be encouraged. Working with forest managers would publication. All authors contributed to the article and approved
also help define strategies to better integrate TreMs in forest the submitted version.
management planning and daily operations in the field. In
this context, a communication and training program for forest ACKNOWLEDGMENTS
managers and practitioners would be essential to reduce the
negative perception of some TreMs as “defects” to be removed. We thank Valentina Buttò for creating the tree illustration in
The efforts initiated by certain research projects to facilitate the Figure 1, as well as Celine Emberger and Rita Bütler for sharing
integration of TreMs in routine forest management (Larrieu the biodiversity illustrations in Figure 1.
et al., 2019, 2021; Martin and Raymond, 2019; Reise et al.,
2019) should be continued. Finally, the recent growing interest SUPPLEMENTARY MATERIAL
in “citizen” surveys, where data are spontaneously sampled by
generally non-professional citizens, offers a good opportunity to The Supplementary Material for this article can be found
complete our knowledge of distribution patterns of TreMs across online at: https://www.frontiersin.org/articles/10.3389/ffgc.2022.
both continents. Such inventories have the potential to quickly 818474/full#supplementary-material
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SYSTEMATIC REVIEW

published: 08 July 2022

Tree-Related Microhabitats Are

INTRODUCTION are highly-dependant on specific TreMs. Some TreMs such as

FIGURE 2 | PRISMA diagram of the systematic review conducted.

To analyze the co-occurrence of the different themes identified

T and Bauhus J (all authors main affiliations located in DISCUSSION

Rank Author # Articles Group Rank Theme # Articles Frequency (%)

1 Larrieu L 20 A 1 Management (forest) 60 59.4

17 Parisi F 5 16 Land use 17 16.8

A same letter indicates a same co-occurrence group.

Asbeck et al. (2019) X X X

Lassauce et al. (2013) X X

Standovár et al. (2016) X

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