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Towards evidence-based conservation
of subterranean ecosystems
Stefano Mammola
1,2†
*,Melissa B. Meierhofer
3†
,Paulo A.V. Borges
4
,
Raquel Colado
5
,David C. Culver
6
,Louis Deharveng
7
,Teo Delic
8
,Tiziana Di Lorenzo
9
,
Tvrtko Dražina
10,11
,Rodrigo L. Ferreira
12
,Barbara Fiasca
13
,Cene Fišer
8
,
Diana M. P. Galassi
13
,Laura Garzoli
2
,Vasilis Gerovasileiou
14,15
,Christian Griebler
16
,
Stuart Halse
17
,Francis G. Howarth
18
,Marco Isaia
19
,Joseph S. Johnson
20
,
Ana Komericˇki
11
,Alejandro Martínez
2
,Filippo Milano
19
,Oana T. Moldovan
21,22
,
Veronica Nanni
19
,Giuseppe Nicolosi
19
,Matthew L. Niemiller
23
,Susana Pallarés
24
,
Martina Pavlek
11,25
,Elena Piano
19
,Tanja Pipan
26,27
,David Sanchez-Fernandez
5
,
Andrea Santangeli
28
,Susanne I. Schmidt
29,30
,J. Judson Wynne
31
,Maja Zagmajster
8
,
Valerija Zakšek
8
and Pedro Cardoso
1,4
1
Laboratory for Integrative Biodiversity Research (LIBRe), Finnish Museum of Natural History (LUOMUS), University of Helsinki, Pohjoinen
Rautatiekatu 13, Helsinki, 00100, Finland
2
Molecular Ecology Group (dark-MEG), Water Research Institute (IRSA), National Research Council (CNR), Largo Tonolli, 50, Verbania-
Pallanza, 28922, Italy
3
BatLab Finland, Finnish Museum of Natural History Luomus (LUOMUS), University of Helsinki, Pohjoinen Rautatiekatu 13, Helsinki, 00100,
Finland
4
cE3c—Centre for Ecology, Evolution and Environmental Changes / Azorean Biodiversity Group / CHANGE –Global Change and Sustainability
Institute, University of Azores, Faculty of Agrarian Sciences and Environment (FCAA), Rua Capit~ao Jo~ao d’Àvila, Pico da Urze, 9700-042 Angra
do Heroísmo, Azores, Portugal
5
Departament of Ecology and Hidrology, University of Murcia, Murcia, 30100, Spain
6
Department of Environmental Science, American University, 4400 Massachusetts Avenue, N.W, Washington, DC, 20016, U.S.A.
7
Institut de Systématique, Evolution, Biodiversité (ISYEB), CNRS UMR 7205, MNHN, UPMC, EPHE, Museum National d’Histoire
Naturelle, Sorbonne Université, Paris, France
8
SubBio Lab, Department of Biology, Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, Ljubljana, 1000, Slovenia
9
Research Institute on Terrestrial Ecosystems (IRET-CNR), National Research Council, Via Madonna del Piano 10, 50019 Sesto Fiorentino,
Florence, Italy
10
Division of Zoology, Department of Biology, Faculty of Science, University of Zagreb, Rooseveltov Trg 6, Zagreb, 10000, Croatia
11
Croatian Biospeleological Society, Rooseveltov Trg 6, Zagreb, 10000, Croatia
12
Center of Studies in Subterranean Biology, Biology Department, Federal University of Lavras, Campus universitario s/n, Aquenta Sol, Lavras, MG,
37200-900, Brazil
13
Department of Life, Health and Environmental Sciences, University of L’Aquila, Via Vetoio 1, Coppito, L’Aquila, 67100, Italy
14
Department of Environment, Faculty of Environment, Ionian University, M. Minotou-Giannopoulou str, Panagoula, Zakynthos, 29100, Greece
15
Hellenic Centre for Marine Research (HCMR), Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC), Thalassocosmos, Gournes,
Crete, 71500, Greece
16
Department of Functional and Evolutionary Ecology, Division of Limnology, University of Vienna, Djerassiplatz 1, Vienna, 1030, Austria
17
Bennelongia Environmental Consultants, 5 Bishop Street, Jolimont, WA, 6014, Australia
18
Hawaii Biological Survey, Bishop Museum, Honolulu, Hawaii, U.S.A.
19
Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina, 13, Torino, I-10123, Italy
20
Department of Biological Sciences, Ohio University, 57 Oxbow Trail, Athens, OH, 45701, U.S.A.
*Address for correspondence (Tel: +39 0323 518363; E-mail: stefano.mammola@helsinki.fi;stefano.mammola@cnr.it)
†
Equal first authors.
Biological Reviews 97 (2022) 1476–1510 © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical
Society.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited and is not used for commercial purposes.
Biol. Rev. (2022), 97, pp. 1476–1510. 1476
doi: 10.1111/brv.12851
21
Emil Racovita Institute of Speleology, Clinicilor 5, Cluj-Napoca, 400006, Romania
22
Romanian Institute of Science and Technology, Saturn 24-26, Cluj-Napoca, 400504, Romania
23
Department of Biological Sciences, The University of Alabama in Huntsville, 301 Sparkman Drive NW, Huntsville, AL, 35899, U.S.A.
24
Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales, CSIC, Calle de José Gutiérrez Abascal 2, Madrid,
28006, Spain
25
Ruđer Boškovic Institute, Bijenicˇka cesta 54, Zagreb, 10000, Croatia
26
ZRC SAZU, Karst Research Institute, Novi trg 2, Ljubljana, 1000, Slovenia
27
UNESCO Chair on Karst Education, University of Nova Gorica, Glavni trg 8, Vipava, 5271, Slovenia
28
Research Centre for Ecological Change, Organismal and Evolutionary Biology Research Programme, University of Helsinki, Viikinkaari 1,
Helsinki, 00014, Finland
29
Institute of Hydrobiology, Biology Centre CAS, Na Sadkach 702/7, České Budeˇjovice, 370 05, Czech Republic
30
Department of Lake Research, Helmholtz Centre for Environmental Research, Brückstraße 3a, Magdeburg, 39114, Germany
31
Department of Biological Sciences, Center for Adaptable Western Landscapes, Box 5640, Northern Arizona University, Flagstaff, AZ, 86011, U.
S.A.
ABSTRACT
Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of
their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique
conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems
have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assess-
ment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment
allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and
management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosys-
tems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness
of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended,
or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number
of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interven-
tions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has
been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic
biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indi-
rect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more
accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biol-
ogy does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions.
This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and
long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better
towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-
analytical exercises. We also provide a database summarising the available literature, which will help to build quantita-
tive knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and hab-
itats of interest. We view this as a starting point to shift away from the widespread tendency of recommending
conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without
quantitatively testing their effectiveness.
Key words: biospeleology, cave, climate change, conservation biology, ecosystem management, extinction risk, ground-
water, legislation, pollution, subterranean biology
CONTENTS
I. Introduction ......................................................................1478
(1) General overview ...............................................................1478
(2) Definition of subterranean habitats used in this review ..................................1479
II. Materials and methods ..............................................................1479
(1) Systematic literature search .......................................................1479
(2) Additional literature, cross-validation, and caveats .....................................1481
Biological Reviews 97 (2022) 1476–1510 © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical
Society.
Trends in subterranean conservation 1477
(3) Metadata extraction ............................................................1481
(4) Data visualisation and statistical analyses .............................................1482
(5) To meta-analyse or not to meta-analyse? ............................................1482
III. Overview of quantitative results .......................................................1482
(1) General summary of the literature ..................................................1482
(2) Temporal trends ...............................................................1483
IV. Current knowledge and research trajectories for conservation interventions ......................1483
(1) Assessment ....................................................................1484
(2) Education ....................................................................1487
(3) Monitoring ...................................................................1487
(4) Protection ....................................................................1490
(5) Regulation ....................................................................1490
(6) Restoration ...................................................................1490
V. Future directions ...................................................................1491
(a) Do not reinvent the wheel .................................................... 1491
(b) Be meticulous with study design and reporting of statistics ........................... 1491
(c) Embrace ignorance ......................................................... 1492
(d) Look beyond your backyard .................................................. 1492
(e) Focus on the gaps ........................................................... 1492
(f) Be aware of constraints ...................................................... 1492
(g) Dialogue with decision-makers and stakeholders ................................... 1492
VI. Conclusions .......................................................................1492
VII. Acknowledgements .................................................................1493
VIII. Author contributions ................................................................1493
IX. Data accessibility ...................................................................1493
X. References ........................................................................1493
XI. Supporting information ..............................................................1510
I. INTRODUCTION
(1) General overview
Modern conservation science benefits from an increasing use
of data to support evidence-based conservation interventions
(Sutherland et al., 2004,2019,2020; Salafsky et al., 2019;
Downey et al., 2021) and recognition of biases in terms of
where these efforts are placed (Buxton et al., 2021; Fonseca
et al., 2021). First, we are collectively building upon a quanti-
tative understanding of what constitutes effective conserva-
tion interventions to ensure the protection and recovery of
biodiversity and ecosystems (Sutherland et al., 2019). Second,
we now appreciate that, given limited resources available for
conservation, we need to maximise their effective allocation –
for example by redirecting part of the funding devoted to
monitoring and inventories towards direct and cost-effective
conservation interventions (Lindenmayer, Piggott &
Wintle, 2013; Buxton et al., 2020). Third, we have now iden-
tified how cognitive biases have permeated conservation
investments and efforts in the past –for example more atten-
tion given to charismatic organisms (Mammola et al., 2020b;
Adamo et al., 2021; Delso, Fajardo & Muñoz, 2021) and vis-
ibly appealing landscapes (Watson et al., 2014). By openly dis-
cussing these issues, we are setting the stage for a more
effective allocation of conservation efforts and funding in
the years ahead (Buxton et al., 2021).
Following recent trends, it is clear there should be a sub-
stantial shift of focus towards the species and ecosystems
traditionally overlooked in most global conservation
agendas, such as caves and other subterranean ecosystems
(Sanchez-Fernandez et al., 2021; Wynne et al., 2021; see def-
inition in Section I.2). Due to the intrinsic inaccessibility of
subterranean ecosystems (Ficetola, Canedoli &
Stoch, 2019) and many impediments to research
(Mammola et al., 2021a), we currently know too little about
subterranean biota to be able to routinely implement cost-
effective conservation interventions. To date, conservation
of subterranean ecosystems has been dominated by
problem-based studies focused on identifying the main
drivers associated with subterranean biodiversity decline
(Mammola et al., 2019a; Gerovasileiou & Bianchi, 2021).
For example, we have elucidated the ecological impacts of
polluted surface waters percolating underground
(Di Lorenzo et al., 2015,2021; Manenti et al., 2021), the
long-term consequences of climate change on specialised
subterranean organisms adapted to thermally stable condi-
tions (Mammola et al., 2019c; Pallarés et al., 2020a,b; Colado
et al., 2022), and some of the negative impacts that patho-
gens and alien species can cause to subterranean ecosystems
(Howarth et al., 2007; Wynne et al., 2014; Howarth &
Stone, 2020; Hoyt, Kilpatrick & Langwig, 2021).
However, problem diagnosis alone is notoriously insufficient
for implementing conservation (Williams, Balmford &
Wilcove, 2020). It is vital to start exploring solution-based
approaches, namely proposing and implementing conservation
interventions and then monitoring their efficacy. There are
examples of habitat manipulation to increase bat survivability
Biological Reviews 97 (2022) 1476–1510 © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical
Society.
1478 Stefano Mammola et al.
under pathogenic stress (Turner et al., 2021), cave habitat resto-
ration for invertebrate populations (Humphreys, 1991;Man-
enti et al., 2019), and several studies synthesising quantitative
knowledge on conservation interventions for managing bat
populations, including species roosting or hibernating in caves
(e.g. Tobin & Chambers, 2017; Berthinussen, Richardson &
Altringham, 2021;Sutherlandet al., 2021). More often, how-
ever, conservation interventions are indirect and/or not
assessed quantitatively. We are frequently guilty of concluding
our research papers with lofty, often abstract
recommendations such as “We should monitor the popula-
tion…”,“Management of the [habitat/species/population]
is strongly advised…”,and“It would be important to protect
the site.…”Although the intentions are good, this can contrib-
ute to an information overload that may complicate, or even
misguide, conservation and management efforts
(Landhuis, 2016;Jeschkeet al., 2019).
Two questions naturally follow concerning conservation
and management of the subterranean biome: (i) how often
have conservation interventions been quantified and statisti-
cally tested in relation to various anthropogenic threats; and
(ii) how has the frequency of the different conservation inter-
ventions, whether proposed or tested, changed over time? To
approach these questions, we undertook a systematic litera-
ture review across a breadth of publications focused on con-
servation interventions for subterranean ecosystems (Fig. 1).
Our efforts were designed to build a quantitative understand-
ing of the number of interventions that have (or have not)
been tested, as well as to target threats, organisms, systems,
and types of conservation interventions lacking research.
Finally, we build upon positive cases of successful conserva-
tion to provide examples of robust study designs that monitor
the effectiveness of conservation interventions.
(2) Definition of subterranean habitats used in this
review
We used the term ‘subterranean habitat/ecosystem’in a
broad sense to encompass all lightless subterranean spaces,
dry or filled with water, generally representing buffered cli-
matic conditions, and where organisms do not encounter sur-
face habitats in all three dimensions. The latter condition
excludes soil habitats. For the purpose of this analysis, we
divide subterranean habitats into six artificial categories: (i)
caves –cavities of different origins [karst, volcanic, tectonic,
glacier caves, and other voids formed by solution or erosion]
that are directly accessible to humans; (ii)showcaves–caves
made accessible to the general public for tourism, managed
by a government or commercial organisation; (iii)artificial –
all subterranean spaces of man-made origin, such as mines,
bunkers, blockhouses, and water conduits; (iv)groundwater–
aquatic subterranean habitats such as aquifers, springs,
cenotes, and subterranean rivers; (v)fissural systems –all fis-
sures and pore spaces whose size prevents human entry, with
similar habitats occurring close to the surface usually listed
under the umbrella term shallow subterranean habitats (Culver &
Pipan, 2014); these habitats are only accessible via indirect
means, for example using subterranean sampling devices
(Mammola et al., 2016); and (vi) marine/anchialine –saline
groundwater habitats represented through the ecotone that
extends from the coast to fresh groundwater. Marine subterra-
nean ecosystems (e.g. submarine caves) are those subject to
direct marine influence, whereas ‘anchialine’is generally used
for subterranean or semi-subterranean water bodies with a
marine origin that has penetrated inland and remains isolated
from the ocean (Sket, 1996).
II. MATERIALS AND METHODS
We conducted a systematic literature review to amass an
extensive list of publications that discussed and/or tested con-
servation interventions for subterranean species or habitats –
including terrestrial, freshwater, and marine/anchialine sub-
terranean systems (see Section I.2 for definitions). The
PRISMA workflow (Moher et al., 2009; Page et al., 2021)
and a summary of this review is provided in Fig. 1A.
Throughout the text, we use the term ‘intervention’in a
broad sense, namely any direct or indirect action associated
with the conservation of the species/system (see Section II.3
for further details).
(1) Systematic literature search
On 03 February 2021, we performed standardised literature
searches in the Web of Science. Different search terms were ini-
tially trialed by S.M. and M.B.M. in a scoping exercise to
refine the procedure, that is running a search and considering
the relevance of the first 200 references. Based upon this
exploratory trial, we refined search terms to minimise the
number of irrelevant references. We found that using overly
broad search terms (e.g. ‘subterranean habitat’,‘groundwa-
ter’) resulted in an overwhelming number of articles. For
example, a search with the term ‘groundwater’yielded
>37,000 papers, most of which were irrelevant because they
referred to (hydro)geological aspects. At the same time, more
specific subterranean biology terms such as ‘caves’captured
several archaeological, palaeontological, and medical papers
–for example the term ‘cave’is used in Osteology. The final
search string that maximised both specificity and sensitivity
was (Search #1):
TS =(“cave”OR “subterranean biology”)AND
TS =(“conserv*”OR “managem*”OR “restorat*”OR
“preserv*”OR “policy”OR “policies”OR “politic*”OR
“protect*”OR “reintroduc*”OR “regulat*”OR “legislat*”
OR “IUCN”OR “CITES”OR “sustainabil*”) NOT
TS =(“surgery”OR “surgical”OR “medicine”OR “Nean-
derthal”OR “osteology”OR “bones”OR “anthropology”
OR “Homo”OR “therapy”OR “art”OR “cranial”OR
“paleontolog*”).
This search yielded 3,269 papers. In parallel, we con-
ducted a second search for groundwater and anchialine sys-
tems (Search #2) using the search string:
Biological Reviews 97 (2022) 1476–1510 © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical
Society.
Trends in subterranean conservation 1479
TS =(“groundwater”OR “anchialine”)ANDTS
=(“fauna”OR “stygob*”OR “organism*”)AND
TS =(“conserv*”OR “managem*”OR “restorat*”OR
“preserv*”OR “policy”OR “policies”OR “politic*”OR
“protect*”OR “reintroduc*”OR “regulat*”OR “legislat*”
OR “IUCN”OR “CITES”OR “sustainabil*”).
(A)
(B)
Fig. 1. Summary of the sampled literature and extracted metadata. (A) PRISMA diagram depicting the flow of information through
the different phases of the systematic literature review. For the list of studies extracted from the Web of Science, including excluded
studies with reasons for exclusion, see Appendix S1. (B) Summary of the metadata collected for the database. For the link to the
data repository see Section VII. Original silhouettes by Irene Frigo.
Biological Reviews 97 (2022) 1476–1510 © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical
Society.
1480 Stefano Mammola et al.
This search yielded an additional 998 papers, with less than
100 papers overlapping with Search #1. All papers originating
from these two searches (N=4,265) were screened for inclu-
sion in the review based on an agreed set of criteria (Appendix
S1). We included studies that: (i) statistically tested the effec-
tiveness of conservation interventions (e.g. gating to prevent
access to caves), based on quantitative variables describing
the status of species or ecosystems (e.g. population or range
trends) (hereafter ‘testing’); (ii) discussed or recommended con-
servation interventions without testing their effectiveness; (iii)
discussed research priorities for conservation of subterranean
biodiversity and/or performed risk assessments; and (iv)
focused on surface management/protection measures that
affect subterranean ecosystems. Studies were excluded that
either: (i) focused on non-subterranean habitats (see Section-
I.2) or (ii) did not focus on the biological component of the tar-
get subterranean ecosystem (e.g. studies examining methods to
restore cave-wall paintings at archaeological sites).
We carried outthe initial screeningby making independent
selections based on titles and abstracts. To test the consistency
of selection criteria, S.M. and M.B.M. independently classified
the first 100 papers and calculated inter-rater agreement using
Cohen’s kappa. The value of kappa was 0.7, well above the
standard threshold of acceptable inter-rater agreement of 0.4
(Cohen, 1960). Given this result, we used these criteria to
screen the remaining papers based on their titles and abstracts.
If it was evident that a given study did not address our key
research questions, we discarded it. Subsequently, we exam-
ined the full text of the references taken forward from this
screening (N=708) to determine if they addressed our
research questions (Appendix S1).
For both Web of Science searches, we set up an alert for rel-
evant references when they entered the Web of Science data-
base from February to October 2021, which generated an
additional 42 references.
(2) Additional literature, cross-validation, and
caveats
To ensure a better coverage of the current conservation liter-
ature (Gusenbauer & Haddaway, 2020; Sutherland
et al., 2020), we cross-checked the final database with the list
of papers focusing on subterranean ecosystems included
within the Conservation Evidence database (N=15, of which
11 were also available in the Web of Science; online database
accessed on 03 February 2021 using the query “Habitat =
Rocky Habitats & Caves”and manually extracting relevant
entries; Sutherland et al., 2019). We further cross-checked
the final database with the lists of papers analysed in three
ongoing systematic literature surveys focusing on the environ-
mental impacts related to the exploitation of caves for tourism
(E. Piano, G. Nicolosi, S. Mammola, B. Baroni, E. Cumino,
N. Muzzulini, V. Balestra, R. Bellopede & M. Isaia, unpub-
lished), on alien species in subterranean ecosystems
(G. Nicolosi, L. Verbrugge, M. Isaia & S. Mammola, unpub-
lished), on conservation of cave-dwelling bats (M.B. Meierho-
fer, J.S. Johnson, J. Perez-Jimenez, F. Ito, P.W. Webela,
S.