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A conservation roadmap for the subterranean biome
J. Judson Wynne1Francis G. Howarth2Stefano Mammola3,4
Rodrigo Lopes Ferreira5Pedro Cardoso3Tiziana Di Lorenzo6
Diana M. P. Galassi7Rodrigo A. Medellin8Bruce W. Miller9
David Sánchez-Fernández10 Maria Elina Bichuette11 Jayant Biswas12
Cory W. BlackEagle13 Chaichat Boonyanusith14 Isabel R. Amorim15
Paulo Alexandre Vieira Borges15 Penelope J. Boston16 Reynold N. Cal17
Naowarat Cheeptham18 Louis Deharveng19 David Eme20 Arnaud Faille21
Danté Fenolio22 Cene Fišer23 Žiga Fišer23 Samuel M. ʻOhukaniʻ¯
ohiʻa
Gon III24 Forough Goudarzi25 Christian Griebler26 Stuart Halse27
Hannelore Hoch28 Enock Kale29 Aron D. Katz30 Ľubomír Kováč31
Thomas M. Lilley3Shirish Manchi32 Raoul Manenti33 Alejandro Martínez4
Melissa B. Meierhofer3Ana Z. Miller34 Oana Teodora Moldovan35
Matthew L. Niemiller36 Stewart B. Peck37 Thais Giovannini Pellegrini5
Tanja Pipan38 Charity M. Phillips-Lander39 Celso Poot40 Paul A. Racey41
Alberto Sendra42,43 William A. Shear44 Marconi Souza Silva5Stefano Taiti45
Mingyi Tian46 Michael P. Venarsky47 Sebastián Yancovic Pakarati48,49,50
Maja Zagmajster23 Yahui Zhao51
Department of Biological Sciences, Center for Adaptable Western Landscapes, Northern Arizona University, Flagstaff, Arizona
Hawaii Biological Survey, Bishop Museum, Honolulu, Hawaii
Finnish Museum of Natural History Luomus, University of Helsinki, Helsinki, Finland
DarkMEG—Molecular Ecology Group, Water Research Institute, National Research Council of Italy, Verbania Pallanza, Italy
Centro de Estudos em Biologia Subterrânea, Setor de Biodiversidade Subterrânea, Departamento de Ecologia e Conservação, Universidade Federal de
Lavras, Minas Gerais, Brazil
Research Institute on Terrestrial Ecosystem of the Italian National Research Council, Florence, Italy
Department of Life, Health & Environmental Sciences, University of L’Aquila, L’Aquila, Italy
Instituto de Ecologia, Universidad Nacional Autónoma de México, México
Wildlife Conservation Society, Bronx Zoo, Bronx, NY (Ret.) and Bat Sound Services, Canadian Lakes, Michigan
Departamento de Ecología e Hidrología, Universidad de Murcia, Murcia, Spain
Laboratório de Estudos Subterrâneos, Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, São Carlos, São Paulo,
Brazil
National Cave Research and Protection Organization, Raipur, Chhattisgarh, India
Department of Geosciences, Eastern Kentucky University, Richmond, Kentucky
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the
original work is properly cited.
© The Authors. Conservation Letters published by Wiley Periodicals LLC
Conservation Letters. ;:e. wileyonlinelibrary.com/journal/conl 1of6
https://doi.org/./conl.
2of6 WYNNE .
School of Biology, Nakhon Ratchasima Rajabhat University, Nakhon Ratchasima, Thailand
Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group and Universidade dos Açores, Faculty of Agrarian and
Environmental Sciences, Azores, Portugal
NASA Ames Research Center, Moffett Field, California
Runaway Creek Nature Reserve, Belmopan, Belize
Department of Biological Sciences, Faculty of Science, Thompson Rivers University, Kamloops, British Columbia, Canada
Museum National d’Histoire Naturelle, Paris, France
IFREMER Centre Atlantique, Unité Ecologie et Modèles pour l’Halieutique, Nantes, France
Stuttgart State Museum of Natural History, Stuttgart, Germany
Center for Conservation and Research, San Antonio Zoo, San Antonio, Texas
SubBio Lab, Department of Biology, Biotechnical Faculty, University of Ljubljana, Slovenia
The Nature Conservancy, Honolulu, Hawaii
Department of Environment, Isfahan University of Technology, Isfahan, Iran
Department of Functional and Evolutionary Ecology, Division of Limnology, University of Vienna, Vienna, Austria
Bennelongia Environmental Consultants, Perth, Australia
Department Center for Integrative Biodiversity Discovery, Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity,
Berlin, Germany
Ecomate Management Ltd., Boroko, NCD, Papua New Guinea
Engineer Research and Development Center, U.S. Army Corps of Engineers, Champaign, Illinois
Department of Zoology, Institute of Biology and Ecology, P.J. Šafárik University, Košice, Slovakia
Conservation Ecology Division, Salim Ali Centre for Ornithology and Natural History, Coimbatore, India
Department of Environmental Science and Policy, Università degli Studi di Milano, Milan, Italy
Laboratório HERCULES, University of Évora, Évora, Portugal and Instituto de Recursos Naturales y Agrobiología de Sevilla, Consejo Superior de
Investigaciones Científicas, Seville, Spain
Emil Racovita Institute of Speleology, Cluj-Napoca Department, Cluj-Napoca, Romania
Department of Biological Sciences, The University of Alabama in Huntsville, Huntsville, Alabama
Canadian Museum of Nature, Ottawa, Ontario, Canada
ZRC SAZU Karst Research Institute, Ljubljana, Slovenia and UNESCO Chair on Karst Education, University of Nova Gorica, Vipava, Slovenia
Space Science and Engineering Division, Southwest Research Institute, San Antonio, Texas
The Belize Zoo and Tropical Education Center, Belmopan, Belize and School of Natural Resources and Environment, University of Florida,
Gainesville, Florida
Centre for Ecology and Conservation, University of Exeter, UK
Colecciones Entomológicas Torres-Sala, Servei de Patrimoni Històric, Ajuntament de València, València, Spain
Departament de Didàctica de les Cièncias Experimentals i Socials, Facultat de Magisteri, Universitat de València, València, Spain
Department of Biology, Hampden-Sydney College, Hampden Sydney, Virginia
Istituto di Ricerca sugli Ecosistemi Terrestri CNR-IRET, Museo di Storia Naturale, Sezione di Zoologia, Firenze, Italy
Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China
Department of Biodiversity Conservation and Attractions, Government of Western Australia, Washington, Kensington, Australia
Laboratorio de Socioecosistemas, Departamento de Ecología, Universidad Autónoma de Madrid, Madrid, Spain
Consejo Asesor de Monumentos Nacionales de Chile - Rapa Nui, Chile
Manu Project, Rapa Nui, Chile
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Correspondence
J. Judson Wynne,Department of Biological
Sciences, Center for Adaptable Western
Landscapes, Northern Arizona University,
Flagstaff, AZ .
Email: jut.wynne@nau.edu
Abstract
The th UN Convention on Biological Diversity (CBD) (COP) will be held
in Kunming, China in October . Historically, CBDs and other multilat-
eral treaties have either alluded to or entirely overlooked the subterranean
biome. A multilateral effort to robustly examine, monitor, and incorporate the
WYNNE . 3of6
subterranean biome into future conservation targets will enable the CBD to fur-
ther improve the ecological effectiveness of protected areas by including ground-
water resources, subterranean ecosystem services, and the profoundly endemic
subsurface biodiversity. To this end, we proffer a conservation roadmap that
embodies five conceptual areas: () science gaps and data management needs; ()
anthropogenic stressors; () socioeconomic analysis and conflict resolution; ()
environmental education; and () national policies and multilateral agreements.
KEYWORDS
biodiversity, caves, convention on biological diversity, hypogean, indicator species
The th UN Convention on Biological Diversity (CBD)
(COP) (UNEP, )willbeheldinKunming,China
in October . Historically, CBDs and other multi-
lateral treaties have either alluded to or entirely over-
looked the subterranean biome (Sánchez-Fernández et al.,
). Importantly, while the post- global biodiver-
sity framework (IUCN, ) briefly mentioned subter-
ranean ecosystems, the need for an effective protected area
network to safeguard biodiversity, freshwater, and ecosys-
tem services had been strenuously and broadly empha-
sized. Globally, only ∼% of the modeled extent of the sub-
terranean biome overlaps with protected areas (Sánchez-
Fernández et al., ).
As the upcoming CBD meeting will be held in the
South China Karst, a region supporting the highest diver-
sity of subterranean-adapted fishes, beetles, and millipedes
globally (and likely to emerge as a subterranean biodi-
versity hotspot), we provide this roadmap for conserving
the world’s subterranean resources. Through a multilateral
effort to robustly examine, monitor, and incorporate the
subterranean biome into future conservation targets, the
CBD will further improve the ecological effectiveness of
protected areas by including groundwater resources, sub-
terranean ecosystem services, and the profoundly endemic
subsurface biodiversity (Elshall et al., ; Mammola
et al., ,). To this end, this roadmap embodies
five conceptual areas: () science gaps and data man-
agement needs; () anthropogenic stressors; () socioeco-
nomic analysis and conflict resolution; () environmen-
tal education; and () national policies and multilateral
agreements.
Perhaps even more than surface ecosystems, the terres-
trial subterranean biome is riddled by extensive knowl-
edgegaps(Box,Figure). For example, for most known
subterranean-obligate species, we have little more than
observational data from a few human-accessible locali-
ties (Mammola et al., ,); this makes assessing
species for protective management extremely challenging.
While the importance of ecosystem services associated
with groundwater quality and cave-roosting bats is rela-
tively well-documented (Elshall et al., ; Griebler et al.,
; Mammola et al., ), a substantial effort will be
required to quantify the scope, importance, and habitat
requirements of subterranean bioindicator and ecosystem
service species (Elshall et al., ).
Natural history information on the subterranean biome
lags equally behind. Data deficiencies to be addressed
should include developing a network of voucher speci-
men collections available both in brick-and-mortar loca-
tions and as digital archives. Additionally, the creation or
adoption of an array of digital archives, tantamount to
the World Karst Spring hydrograph database (Olarinoye
et al., ), will provide conservationists and resource
managers with the data to identify research needs and fos-
ter international and interdisciplinary collaborations. Such
archives must house information on the geospatial extent
of subterranean habitats, reference barcode/genetic and
functional trait data on subterranean species, and syner-
gistically contribute to or augment existing archives (Frick
et al., ) (e.g., GBIF, iDigBio, and BoldSystems).
Although researchers have qualitatively summarized
most of the likely anthropogenic stressors threatening sub-
terranean biodiversity and ecosystem function (Box )
(Elshall et al., ; Griebler et al., ; Leclère et al.,
; Mammola et al., ), their potential impacts have
not been quantified (Mammola et al., ). Strategically
focused, global studies to examine key impacts (in par-
ticular, surface habitat loss) (Hedrick et al., ) should
be conducted across a range of subterranean habitats, a
panoply of associated indicators, and ecosystem service
and short-range endemic species. Through such a coordi-
nated effort, researchers and policymakers can amass the
information required to develop mitigation strategies to
optimize decision-making.
Solutions (Box ) will require scientists and legisla-
tors to work closely with local communities and munic-
ipalities to both ameliorate future land-use disputes and
to find sustainable and economically viable pathways
4of6 WYNNE .
FIGURE 1 Conservation roadmap flows from addressing data gaps and data management needs (green ovals with callout box) to policy
development and implementation (blue). Data acquisition and management moves in two directions: () toward a feedback loop of
monitoring, adaptive management, and local resource policy development – with monitoring and management iteratively improved as
scientific data dictates; and () to providing information necessary to create educational outreach programs (yellow), which are further
sculpted by human activities (red). Socio-economic analyses (purple) aim to both characterize and lessen anthropogenic impacts and
stressors. This information then feeds into local resource management formulation; national policy and multilateral agreements are both
shaped and influenced by local decision-making
forward. Importantly, % of humans rely on groundwater
for consumption, while % use it for agricultural purposes
(Elshall et al., ). As we increasingly convert natural
ecosystems to agriculture, pastureland, and human habita-
tion, surface biodiversity, and ecosystem function (Gibson
et al., ), as well as aquifers and other groundwater habi-
tats will become increasingly threatened and degraded. To
maximize effectiveness and reduce conservation conflicts,
improved dialog between social and natural scientists must
occur so that social, political, and scientific contexts are
well articulated, and stakeholders can negotiate with com-
plete transparency (Gibson et al., ).
WYNNE . 5of6
Successful environmental and conservation education
programs (Box ) should be crafted to: (i) address local
problems/topics; (ii) establish partnerships and programs
with local researchers and resource managers; (iii) empha-
size action focused projects (e.g., ecological restoration,
cave cleanups, and monitoring bioindicators and bat/bird
roosts); and (iv) create targeted projects that quantify
and report program outcomes (Redpath et al., ).
Educational efforts must be established in partnership
with local schools and universities, scientific organiza-
tions, indigenous and community groups, businesses, non-
governmental organizations, and government agencies.
Conservation policies (Box ) to protect significant
subterranean habitats are lacking at most regional and
national levels (Mammola et al., ). However, poli-
cies have been implemented to better manage local and
regional groundwater resources (Elshall et al., ).
Barring the European Union’s Habitat Directive (which
marginally considers subterranean habitats; EU, ), no
multilateral agreements have been adopted to specifically
include the subterranean biome (Sánchez-Fernández et al.,
). Solidly integrating surface with subsurface con-
servation targets through equitable stakeholder participa-
tion represents a foundational next step toward optimally
securing the groundwater supply (Elshall et al., ), safe-
guarding ecosystem services (Frick et al., ; Mammola
et al., ), and protecting subterranean diversity.
While numerous lacunae exist concerning subterranean
resources, sound directives can be enacted promptly with
adaptive management. This roadmap represents a viable
framework for near-term and longer duration conserva-
tion actions to protect the world’s subterranean ecosys-
tems. Formulating targets to further reduce threats to the
subterranean biome is essential to this year’s CBD meeting
in Kunming. We must act now.
AUTHOR CONTRIBUTIONS
J. Judson Wynne and Stefano Mammola conceived the
project. Francis Howarth developed the initial roadmap.
All other authors contributed to roadmap development
and finalization.
ETHICS STATEMENT
No data collection or scientific inquiries requiring ethics
considerations were undertaken. Thus, this work complies
with appropriate ethical standards.
DATA ACCESSIBILITY STATEMENT
We did not collect any primary data to develop this
manuscript. All references that aided in refining our posi-
tions are provided.
CONFLICT OF INTEREST
We declare no conflict of interest with this work.
ORCID
J. Judson Wynne https://orcid.org/---
Stefano Mammola https://orcid.org/---
Diana M. P. Galassi https://orcid.org/---
David Sánchez-Fernández https://orcid.org/--
-
Maria Elina Bichuette https://orcid.org/--
-
Jayant Biswas https://orcid.org/---
Cory W. BlackEagle https://orcid.org/---
Chaichat Boonyanusith https://orcid.org/--
-
Isabel R. Amorim https://orcid.org/---
David Eme https://orcid.org/---
Samuel M. ʻOhukaniʻ¯
ohiʻa Gon III https://orcid.org/
---
Ľubomír Kováč https://orcid.org/---
Thais Giovannini Pellegrini https://orcid.org/-
--
Stefano Taiti https://orcid.org/---
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How to cite this article: Wynne JJ, Howarth FG,
Mammola S, et al. A conservation roadmap for the
subterranean biome. Conservation Letters.
;14:e. https://doi.org/./conl.
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