# A conservation roadmap for the subterranean biome

J. Judson Wynne, Francis Howarth, Stefano Mammola, Rodrigo Lopes

Ferreira, Pedro Cardoso, Tiziana Di Lorenzo, Diana Galassi, Rodrigo

Medellin, Bruce Miller, David Sánchez-fernández, et al.

<figure><img src="image_1.png" /></figure>

## To cite this version:

J. Judson Wynne, Francis Howarth, Stefano Mammola, Rodrigo Lopes Ferreira, Pedro Cardoso, et al.. A conservation roadmap for the subterranean biome. Conservation Letters, 2021, 14 (5), 10.1111/conl.12834. hal-03616068

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# A conservation roadmap for the subterranean biome

J. Judson Wynne<fnref n="1" /> ID | Francis G. Howarth<fnref n="2" /> | Stefano Mammola<fnref n="3" />,<fnref n="4" /> ID |

Rodrigo Lopes Ferreira<fnref n="5" /> | Pedro Cardoso<fnref n="3" /> | Tiziana Di Lorenzo<fnref n="6" /> |

Diana M. P. Galassi<fnref n="7" /> ID | Rodrigo A. Medellin<fnref n="8" /> | Bruce W. Miller<fnref n="9" /> |

David Sánchez-Fernández<fnref n="10" /> ID | Maria Elina Bichuette<fnref n="11" /> ID | Jayant Biswas<fnref n="12" /> ID |

Cory W. BlackEagle<fnref n="13" /> ID | Chaichat Boonyanusith¹⁴ ID | Isabel R. Amorim¹⁵ ID |

Paulo Alexandre Vieira Borges¹⁵ | Penelope J. Boston¹⁶ | Reynold N. Cal¹⁷ |

Naowarat Cheeptham¹⁸ | Louis Deharveng¹⁹ | David Eme²⁰ ID | Arnaud Faille²¹ |

Danté Fenolio²² | Cene Fišer²³ | Žiga Fišer²³ | Samuel M. ‘Ohukani‘öhi‘a

Gon III²⁴ ID | Forough Goudarzi²⁵ | Christian Griebler²⁶ | Stuart Halse²⁷ |

Hannelore Hoch²⁸ | Enock Kale²⁹ | Aron D. Katz³⁰ | Ľubomír Kováč³¹ ID |

Thomas M. Lilley<fnref n="3" /> | Shirish Manchi³² | Raoul Manenti³³ | Alejandro Martínez<fnref n="4" /> |

Melissa B. Meierhofer<fnref n="3" /> | Ana Z. Miller³⁴ | Oana Teodora Moldovan³⁵ |

Matthew L. Niemiller³⁶ | Stewart B. Peck³⁷ | Thais Giovannini Pellegrini<fnref n="5" /> ID |

Tanja Pipan³⁸ | Charity M. Phillips-Lander³⁹ | Celso Poot⁴⁰ | Paul A. Racey⁴¹ |

Alberto Sendra⁴²,⁴³ | William A. Shear⁴⁴ | Marconi Souza Silva<fnref n="5" /> | Stefano Taiti⁴⁵ ID |

Mingyi Tian⁴⁶ | Michael P. Venarsky⁴⁷ | Sebastián Yancovic Pakarati⁴⁸,⁴⁹,⁵⁰ |

Maja Zagmajster²³ | Yahui Zhao⁵¹

<footnote n="1">¹ Department of Biological Sciences, Center for Adaptable Western Landscapes, Northern Arizona University, Flagstaff, Arizona</footnote>

<footnote n="2">² Hawaii Biological Survey, Bishop Museum, Honolulu, Hawaii</footnote>

<footnote n="3">³ Finnish Museum of Natural History Luomus, University of Helsinki, Helsinki, Finland</footnote>

<footnote n="4">⁴ DarkMEG—Molecular Ecology Group, Water Research Institute, National Research Council of Italy, Verbania Pallanza, Italy</footnote>

<footnote n="5">⁵ Centro de Estudos em Biologia Subterrânea, Setor de Biodiversidade Subterrânea, Departamento de Ecologia e Conservação, Universidade Federal de Lavras, Minas Gerais, Brazil</footnote>

<footnote n="6">⁶ Research Institute on Terrestrial Ecosystem of the Italian National Research Council, Florence, Italy</footnote>

<footnote n="7">⁷ Department of Life, Health & Environmental Sciences, University of L'Aquila, L'Aquila, Italy</footnote>

<footnote n="8">⁸ Instituto de Ecologia, Universidad Nacional Autónoma de México, México</footnote>

<footnote n="9">⁹ Wildlife Conservation Society, Bronx Zoo, Bronx, NY (Ret.) and Bat Sound Services, Canadian Lakes, Michigan</footnote>

<footnote n="10">¹⁰ Departamento de Ecología e Hidrología, Universidad de Murcia, Murcia, Spain</footnote>

<footnote n="11">¹¹ Laboratório de Estudos Subterrâneos, Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, São Carlos, São Paulo, Brazil</footnote>

<footnote n="12">¹² National Cave Research and Protection Organization, Raipur, Chhattisgarh, India</footnote>

<footnote n="13">¹³ Department of Geosciences, Eastern Kentucky University, Richmond, Kentucky</footnote>
¹⁴ School of Biology, Nakhon Ratchasima Rajabhat University, Nakhon Ratchasima, Thailand

¹⁵ Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group and Universidade dos Açores, Faculty of Agrarian and Environmental Sciences, Azores, Portugal

¹⁶ NASA Ames Research Center, Moffett Field, California

¹⁷ Runaway Creek Nature Reserve, Belmopan, Belize

¹⁸ Department of Biological Sciences, Faculty of Science, Thompson Rivers University, Kamloops, British Columbia, Canada

¹⁹ Museum National d'Histoire Naturelle, Paris, France

²⁰ IFREMER Centre Atlantique, Unité Ecologie et Modèles pour l'Halieutique, Nantes, France

²¹ Stuttgart State Museum of Natural History, Stuttgart, Germany

²² Center for Conservation and Research, San Antonio Zoo, San Antonio, Texas

²³ SubBio Lab, Department of Biology, Biotechnical Faculty, University of Ljubljana, Slovenia

²⁴ The Nature Conservancy, Honolulu, Hawaii

²⁵ Department of Environment, Isfahan University of Technology, Isfahan, Iran

²⁶ Department of Functional and Evolutionary Ecology, Division of Limnology, University of Vienna, Vienna, Austria

²⁷ Bennelongia Environmental Consultants, Perth, Australia

²⁸ Department Center for Integrative Biodiversity Discovery, Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity, Berlin, Germany

²⁹ Ecomate Management Ltd., Boroko, NCD, Papua New Guinea

³⁰ Engineer Research and Development Center, U.S. Army Corps of Engineers, Champaign, Illinois

³¹ Department of Zoology, Institute of Biology and Ecology, P.J. Šafárik University, Košice, Slovakia

³² Conservation Ecology Division, Salim Ali Centre for Ornithology and Natural History, Coimbatore, India

³³ Department of Environmental Science and Policy, Università degli Studi di Milano, Milan, Italy

³⁴ Laboratório HERCULES, University of Évora, Évora, Portugal and Instituto de Recursos Naturales y Agrobiología de Sevilla, Consejo Superior de Investigaciones Científicas, Seville, Spain

³⁵ Emil Racovita Institute of Speleology, Cluj-Napoca Department, Cluj-Napoca, Romania

³⁶ Department of Biological Sciences, The University of Alabama in Huntsville, Huntsville, Alabama

³⁷ Canadian Museum of Nature, Ottawa, Ontario, Canada

³⁸ ZRC SAZU Karst Research Institute, Ljubljana, Slovenia and UNESCO Chair on Karst Education, University of Nova Gorica, Vipava, Slovenia

³⁹ Space Science and Engineering Division, Southwest Research Institute, San Antonio, Texas

⁴⁰ The Belize Zoo and Tropical Education Center, Belmopan, Belize and School of Natural Resources and Environment, University of Florida, Gainesville, Florida

⁴¹ Centre for Ecology and Conservation, University of Exeter, UK

⁴² Colecciones Entomológicas Torres-Sala, Servei de Patrimoni Històric, Ajuntament de València, València, Spain

⁴³ Departament de Didàctica de les Ciències Experimentals i Socials, Facultat de Magisteri, Universitat de València, València, Spain

⁴⁴ Department of Biology, Hampden-Sydney College, Hampden Sydney, Virginia

⁴⁵ Istituto di Ricerca sugli Ecosistemi Terrestri CNR-IRET, Museo di Storia Naturale, Sezione di Zoologia, Firenze, Italy

⁴⁶ Department of Entomology, College of Plant Protection, South China Agricultural University, Guangzhou, China

⁴⁷ Department of Biodiversity Conservation and Attractions, Government of Western Australia, Washington, Kensington, Australia

⁴⁸ Laboratorio de Socioecosistemas, Departamento de Ecología, Universidad Autónoma de Madrid, Madrid, Spain

⁴⁹ Consejo Asesor de Monumentos Nacionales de Chile - Rapa Nui, Chile

⁵⁰ Manu Project, Rapa Nui, Chile

⁵¹ 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 86011.

Email: jut.wynne@nau.edu

**Abstract**

The 15th UN Convention on Biological Diversity (CBD) (COP15) will be held in Kunming, China in October 2021. Historically, CBDs and other multilateral treaties have either alluded to or entirely overlooked the subterranean biome. A multilateral effort to robustly examine, monitor, and incorporate the
subterranean biome into future conservation targets will enable the CBD to further improve the ecological effectiveness of protected areas by including groundwater resources, subterranean ecosystem services, and the profoundly endemic subsurface biodiversity. To this end, we proffer a conservation roadmap that embodies five conceptual areas: (1) science gaps and data management needs; (2) anthropogenic stressors; (3) socioeconomic analysis and conflict resolution; (4) environmental education; and (5) national policies and multilateral agreements.

### KEYWORDS

biodiversity, caves, convention on biological diversity, hypogean, indicator species

The 15th UN Convention on Biological Diversity (CBD) (COP15) (UNEP, 2021) will be held in Kunming, China in October 2021. Historically, CBDs and other multilateral treaties have either alluded to or entirely overlooked the subterranean biome (Sánchez-Fernández et al., 2021). Importantly, while the post-2020 global biodiversity framework (IUCN, 2020) briefly mentioned subterranean ecosystems, the need for an effective protected area network to safeguard biodiversity, freshwater, and ecosystem services had been strenuously and broadly emphasized. Globally, only ~7% of the modeled extent of the subterranean biome overlaps with protected areas (Sánchez-Fernández et al., 2021).

As the upcoming CBD meeting will be held in the South China Karst, a region supporting the highest diversity of subterranean-adapted fishes, beetles, and millipedes globally (and likely to emerge as a subterranean biodiversity 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, subterranean ecosystem services, and the profoundly endemic subsurface biodiversity (Elshall et al., 2020; Mammola et al., 2019, 2020). To this end, this roadmap embodies five conceptual areas: (1) science gaps and data management needs; (2) anthropogenic stressors; (3) socioeconomic analysis and conflict resolution; (4) environmental education; and (5) national policies and multilateral agreements.

Perhaps even more than surface ecosystems, the terrestrial subterranean biome is riddled by extensive knowledge gaps (Box 1, Figure 1). For example, for most known subterranean-obligate species, we have little more than observational data from a few human-accessible localities (Mammola et al., 2019, 2020); this makes assessing species for protective management extremely challenging. While the importance of ecosystem services associated

with groundwater quality and cave-roosting bats is relatively well-documented (Elshall et al., 2020; Griebler et al., 2014; Mammola et al., 2019), a substantial effort will be required to quantify the scope, importance, and habitat requirements of subterranean bioindicator and ecosystem service species (Elshall et al., 2020).

Natural history information on the subterranean biome lags equally behind. Data deficiencies to be addressed should include developing a network of voucher specimen collections available both in brick-and-mortar locations 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., 2020), will provide conservationists and resource managers with the data to identify research needs and foster 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 synergistically contribute to or augment existing archives (Frick et al., 2020) (e.g., GBIF, iDigBio, and BoldSystems).

Although researchers have qualitatively summarized most of the likely anthropogenic stressors threatening subterranean biodiversity and ecosystem function (Box 2) (Elshall et al., 2020; Griebler et al., 2014; Leclère et al., 2020; Mammola et al., 2020), their potential impacts have not been quantified (Mammola et al., 2020). Strategically focused, global studies to examine key impacts (in particular, surface habitat loss) (Hedrick et al., 2020) 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 coordinated effort, researchers and policymakers can amass the information required to develop mitigation strategies to optimize decision-making.

Solutions (Box 3) will require scientists and legislators to work closely with local communities and municipalities to both ameliorate future land-use disputes and to find sustainable and economically viable pathways
<figure><img src="image_3.png" /><figcaption>**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: (1) toward a feedback loop of monitoring, adaptive management, and local resource policy development – with monitoring and management iteratively improved as scientific data dictates; and (2) 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</figcaption></figure>

forward. Importantly, 50% of humans rely on groundwater for consumption, while 43% use it for agricultural purposes (Elshall et al., 2020). As we increasingly convert natural ecosystems to agriculture, pastureland, and human habitation, surface biodiversity, and ecosystem function (Gibson et al., 2011), 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 complete transparency (Gibson et al., 2011).
Successful environmental and conservation education programs (Box 4) should be crafted to: (i) address local problems/topics; (ii) establish partnerships and programs with local researchers and resource managers; (iii) emphasize 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., 2013). Educational efforts must be established in partnership with local schools and universities, scientific organizations, indigenous and community groups, businesses, non-governmental organizations, and government agencies.

Conservation policies (Box 5) to protect significant subterranean habitats are lacking at most regional and national levels (Mammola et al., 2020). However, policies have been implemented to better manage local and regional groundwater resources (Elshall et al., 2020). Barring the European Union's Habitat Directive (which marginally considers subterranean habitats; EU, 2021), no multilateral agreements have been adopted to specifically include the subterranean biome (Sánchez-Fernández et al., 2021). Solidly integrating surface with subsurface conservation targets through equitable stakeholder participation represents a foundational next step toward optimally securing the groundwater supply (Elshall et al., 2020), safeguarding ecosystem services (Frick et al., 2020; Mammola et al., 2020), 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 conservation actions to protect the world's subterranean ecosystems. 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 positions are provided.

## CONFLICT OF INTEREST

We declare no conflict of interest with this work.

## ORCID

J. Judson Wynne https://orcid.org/0000-0003-0408-0629

Stefano Mammola https://orcid.org/0000-0002-4471-9055

Diana M. P. Galassi https://orcid.org/0000-0002-6448-2710

David Sánchez-Fernández https://orcid.org/0000-0003-1766-0761

Maria Elina Bichuette https://orcid.org/0000-0002-9515-4832

Jayant Biswas https://orcid.org/0000-0001-6422-6111

Cory W. BlackEagle https://orcid.org/0000-0002-3968-6850

Chaichat Boonyanusith https://orcid.org/0000-0003-1487-2160

Isabel R. Amorim https://orcid.org/0000-0001-6847-3320

David Eme https://orcid.org/0000-0001-8790-0412

Samuel M. ‘Ohukani’ōhi’a Gon III https://orcid.org/0000-0003-0397-3089

Lubomír Kováč https://orcid.org/0000-0001-8194-2128

Thais Giovannini Pellegrini https://orcid.org/0000-0001-6725-9429

Stefano Taiti https://orcid.org/0000-0002-4909-6037

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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*. 2021;14:e12834. https://doi.org/10.1111/conl.12834