Forum Scientists’ Warning on the Conservation of Subterranean Ecosystems Downloaded from https://academic.oup.com/bioscience/article-abstract/69/8/641/5519083 by Texas A+M at Galveston user on 15 August 2019 STEFANO MAMMOLA , PEDRO CARDOSO , DAVID C. CULVER, LOUIS DEHARVENG, RODRIGO L. FERREIRA, CENE FIŠER, DIANA M. P. GALASSI, CHRISTIAN GRIEBLER, STUART HALSE , WILLIAM F. HUMPHREYS, MARCO ISAIA, FLORIAN MALARD, ALEJANDRO MARTINEZ , OANA T. MOLDOVAN, MATTHEW L. NIEMILLER, MARTINA PAVLEK , ANA SOFIA P. S. REBOLEIRA , MARCONI SOUZA-SILVA, EMMA C. TEELING, J. JUDSON WYNNE, AND MAJA ZAGMAJSTER In light of recent alarming trends in human population growth, climate change, and other environmental modifications, a “Warning to humanity” manifesto was published in BioScience in 2017. This call reiterated most of the ideas originally expressed by the Union of Concerned Scientists in 1992, including the fear that we are “pushing Earth’s ecosystems beyond their capacities to support the web of life.” As subterranean biologists, we take this opportunity to emphasize the global importance and the conservation challenges associated with subterranean ecosystems. They likely represent the most widespread nonmarine environments on Earth, but specialized subterranean organisms remain among the least documented and studied. Largely overlooked in conservation policies, subterranean habitats play a critical role in the function of the web of life and provide important ecosystem services. We highlight the main threats to subterranean ecosystems and propose a set of effective actions to protect this globally important natural heritage. Keywords: biodiversity crisis, caves, extinction risk, groundwater, nature conservation “Human beings and the natural world are on a collision articles focused on particular biological or social systems course.” (William J. Ripple, Oregon State University, Corvallis, —Union of Concerned Scientists’ Manifesto, 1992 Oregon, personal communication, 7 September 2018). As a group of subterranean biologists with different areas of uilding on the manifesto World Scientists’ Warning expertise and a strong commitment to biodiversity conser- B to Humanity, issued in 1992 by the Union of Concerned vation, we take this opportunity to examine some alarming Scientists, Ripple and colleagues (2017) recently published a trends underscored by the Alliance of World Scientists from passionately debated article titled “World scientists’ warning a subterranean perspective. We discuss the implications that to humanity: A second notice.” This novel proclamation, this Ripple and colleagues (2017) manifesto has for the con- which was endorsed by more than 15,000 cosignatory sci- servation of the subterranean realm, which includes some entists (the Alliance of World Scientists), reiterated most of of the most unique, secluded, understudied, and difficult to the ideas and concerns presented in the first manifesto and, study environments on our planet. in particular, the fear that humans are “pushing Earth’s eco- Although subterranean habitats are not at the forefront of systems beyond their capacities to support the web of life.” one’s mind when thinking about global conservation issues, The second notice highlighted alarming trends in several they support exceptional forms of life and represent critical environmental issues over the last 25 years (1992–2016), habitats to be preserved and prioritized in conservation poli- including global climate change, deforestation, biodiversity cies. Although some conservation efforts have been devoted loss, human population increase, and a decline in freshwater to protect subterranean ecosystems at a local level, no global resources. assessment has been conducted that explicitly takes these Since its publication, this second notice has been exten- resources into account (e.g., Brooks et al. 2006, Sutherland sively discussed in the scientific literature and social media, et al. 2018). Even though there are common conservation stimulating an upsurge of discipline-specific follow-up concerns that affect all biological systems, many of them are BioScience 69: 641–650. © The Author(s) 2019. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights reserved. For Permissions, please e-mail: [email protected]. doi:10.1093/biosci/biz064 Advance Access publication 19 June 2019 https://academic.oup.com/bioscience August 2019 / Vol. 69 No. 8 • BioScience 641 Forum more acute and visible in the subterranean realm and are biota we observe in a cave are just the tip of the subterranean emphasized in this contribution. biodiversity iceberg, what can we do practically to protect the full extent of subterranean habitats and their inhabitants? The challenges of protecting the unknown To make sound decisions for the conservation of the sub- In the era of drones, satellites, and remote-sensing technol- terranean world, there is first an urgent need to accelerate ogy, most of the accessible places on Earth have been directly scientific research, aimed at exploring subterranean biodi- or indirectly mapped and explored. A remarkable exception versity together with the abiotic and biotic factors that drive to the geographic knowledge of our planet comes from the its distribution patterns across space and time. Available Downloaded from https://academic.oup.com/bioscience/article-abstract/69/8/641/5519083 by Texas A+M at Galveston user on 15 August 2019 subterranean world, which is therefore recognized as one estimates (Zagmajster et al. 2018) suggest that most obligate of the most important frontiers of modern exploration subterranean species worldwide have not yet been described (Ficetola et al. 2019). Subterranean ecosystems are likely the (i.e., a Linnean shortfall). In the epoch of the sixth mass most widespread nonmarine environments on Earth. For extinction crisis, many of these species may face extinction example, more than 50,000 caves have been documented in before they are discovered and formally described—a phe- the United States, with nearly 10,000 known from the state nomenon described by Wilson (1992) as “centinelan extinc- of Tennessee alone (Niemiller and Zigler 2013), and some tions.” Moreover, several other knowledge gaps impede our 25,000 caves are estimated solely for the Dinarides, a 60,000 ability to protect and conserve subterranean biodiversity square kilometers European karst region that is considered (table 1). The distribution (i.e., the Wallacean shortfall) and to be the world’s most significant area of subterranean fauna the life history of most described subterranean species are radiation (Zagmajster et al. 2010). However, subterranean virtually unknown. Acquiring basic knowledge about bio- ecosystems are by no means restricted to those subterra- logical and functional diversity of subterranean organisms nean voids that we have mapped and listed in speleological (i.e., the Raunkiæran shortfall), their phylogenetic relation- cadasters (i.e., caves). ships (i.e., the Darwinian shortfall), their interactions within First, most subterranean voids have no entrances that are different subterranean communities (i.e., the Eltonian short- accessible to humans (Curl 1958). The small and inacces- fall), and their sensitivity to environmental perturbations sible network of underground voids and fissures is almost (i.e., the Hutchinsonian shortfall), represent pivotal steps limitless, and this network (rather than caves) represents toward consolidating scientific knowledge to support con- the elective habitat for most subterranean species (Howarth servation planning (Cardoso et al. 2011A, Diniz-Filho et al. 1983). Second, groundwater (i.e., water in the voids in 2013, Hortal et al. 2015) and further understanding the consolidated and unconsolidated rocks) represents 95% of ecosystem services that the subterranean fauna provide. global unfrozen fresh water and hosts organisms special- ized to survive at limits of life (Fišer et al. 2014), as well as The importance of safeguarding subterranean more numerous species that are important to maintaining biodiversity groundwater quality (Griebler et al. 2014). Furthermore, The first argument emphasizing the importance of pro- anchialine ecosystems, represented by coastal, tidally influ- tecting subsurface ecosystems emerges when consider- enced, subterranean estuaries located within crevicular and ing the fascinating evolutionary changes many animals cavernous terrains, are a specialized habitat straddling the have undergone to become adapted to underground life. border between subterranean freshwater and marine envi- Subterranean species are astonishing and bizarre outcomes ronments and host a specialized subterranean fauna (Bishop of evolution (figure 1), and subterranean habitats represent et al. 2015). Also, a variety of superficial underground sources of unexpected—often serendipitous—scientific dis- habitats, collectively termed shallow subterranean habitats, coveries. The study of these remarkable species allows us to supports an extensive array of subterranean biota (Culver travel outside the limits of our own imagination, exploring and Pipan 2014). Finally, if one is keen to account also for unique biological adaptations (Soares and Niemiller 2013, microbial life, a large amount of continental prokaryotic bio- Yoshizawa et al. 2014, 2018a), learning about fundamen- mass and, as yet, an unknown prokaryote diversity is hidden tal ecoevolutionary processes (Juan et al. 2010, Mammola within these systems