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The Chemoautotrophically Based Movile Cave Groundwater Ecosystem, a Hotspot of Subterranean Biodiversity

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The Chemoautotrophically Based Movile Cave Groundwater Ecosystem, a Hotspot of Subterranean Biodiversity diversity Article The Chemoautotrophically Based Movile Cave Groundwater Ecosystem, a Hotspot of Subterranean Biodiversity Traian Brad 1,2,† , Sanda Iepure 1,2,† and Serban M. Sarbu 3,4,*,† 1 “Emil Racovit, ă” Institute of Speleology, str. Clinicilor nr. 5-7, 400006 Cluj-Napoca, Romania; [email protected] (T.B.); [email protected] (S.I.) 2 Institutul Român de S, tiint, ă s, i Tehnologie, str. Virgil Fulicea nr. 3, 400022 Cluj-Napoca, Romania 3 “Emil Racovit, ă” Institute of Speleology, str. Frumoasă nr. 31, 010986 Bucure¸sti,Romania 4 Department of Biological Sciences, California State University, Chico, CA 95929, USA * Correspondence: [email protected] † All the three authors have the same contribution. Abstract: Movile Cave hosts one of the world’s most diverse subsurface invertebrate communities. In the absence of matter and energy input from the surface, this ecosystem relies entirely on in situ primary productivity by chemoautotrophic microorganisms. The energy source for these microor- ganisms is the oxidation of hydrogen sulfide provided continuously from the deep thermomineral aquifer, alongside methane, and ammonium. The microbial biofilms that cover the water surface, the cave walls, and the sediments, along with the free-swimming microorganisms, represent the food that protists, rotifers, nematodes, gastropods, and crustacean rely on. Voracious water-scorpions, leeches, and planarians form the peak of the aquatic food web in Movile Cave. The terrestrial com- munity is even more diverse. It is composed of various species of worms, isopods, pseudoscorpions, spiders, centipedes, millipedes, springtails, diplurans, and beetles. An updated list of invertebrate species thriving in Movile Cave is provided herein. With 52 invertebrate species (21 aquatic and 31 Citation: Brad, T.; Iepure, S.; Sarbu, terrestrial), of which 37 are endemic for this unusual, but fascinating environment, Movile Cave is S.M. The Chemoautotrophically the first known chemosynthesis-based groundwater ecosystem. Therefore, Movile Cave deserves Based Movile Cave Groundwater stringent attention and protection. Ecosystem, a Hotspot of Subterranean Biodiversity. Diversity 2021, 13, 128. Keywords: Movile Cave; Romania; subterranean biodiversity; chemoautotrophically based; ground- https://doi.org/10.3390/d13030128 water ecosystem Academic Editor: Michael Wink Received: 24 February 2021 1. Introduction Accepted: 12 March 2021 Movile Cave is an underground void, which has no natural opening to the surface. Published: 17 March 2021 It is located on the outskirts of the town of Mangalia (SE Romania), 2 km from the Black Sea shore [1] and it was intercepted 18 m below the surface by an artificial geological Publisher’s Note: MDPI stays neutral survey shaft dug in June 1986. The cave is developed in Sarmatian limestones (12.5 MY), with regard to jurisdictional claims in which were covered by Quaternary deposits (clays and loess), approximately 2.5 million published maps and institutional affil- iations. years ago [2], and it was formed by classical karst dissolution processes combined with sulfuric acid speleogenesis (SAS), a process mediated by sulfur-oxidizing bacteria [3]. Additional geographical description information and geological data is presented in Sarbu et al. 2019 [1]. The cave appears as a horizontal maze, with a total development of 240 m, and consists of two levels (Figure1). The upper level is dry and it lacks speleothems. The Copyright: © 2021 by the authors. ◦ atmosphere in the upper level is warm (21 C) and it contains 19% dioxygen (O2) and Licensee MDPI, Basel, Switzerland. 1% carbon dioxide (CO ). The lower level is 40 m long and partially flooded, with the This article is an open access article 2 Lake Room and three Air-Bells as the only aerated zones. The O concentration decreases distributed under the terms and 2 conditions of the Creative Commons gradually in the Air-Bells to 7%, while the CO2 concentration increases to 3.5% due to the Attribution (CC BY) license (https:// activity of microorganisms, which form biofilms [4,5]. In the Air-Bells, the O2 dissolved creativecommons.org/licenses/by/ in water originates from the cave atmosphere and it is rapidly used for the oxidation of 4.0/). hydrogen sulfide (H2S) and methane (CH4). Below a depth of 1 mm, the water becomes Diversity 2021, 13, 128. https://doi.org/10.3390/d13030128 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 128 2 of 13 mm, the water becomes completely anoxic [6]. The water is relatively stagnant at the surface in the Lake Room and in the nearby Air-Bells, while some flow (i.e., 5 l s−1) was completelydetected at anoxicdepths [ 6over]. The 1 m water in the is relativelyflooded cave stagnant passages at the [3]. surface in the Lake Room and in the nearby Air-Bells, while some flow (i.e., 5 l s−1) was detected at depths over 1 m in the flooded cave passages [3]. Figure 1. Plan of Movile Cave (a) with depiction of the water surfaces (dotted areas) in Lake Room and the three Air-Bells (AB)Figure (b). 1. Plan of Movile Cave (a) with depiction of the water surfaces (dotted areas) in Lake Room and the three Air-Bells (AB) (b). Movile Cave is the first subterranean groundwater ecosystem described to be solely basedMovile on chemosynthesis Cave is the first [7]. subterranean Reduced chemical groundwater compounds ecosystem such as desc H2S,ribed CH4 andto be ammo- solely + niumbased (NH on 4chemosynthesis) are supplied continuously [7]. Reduced and chemical in large amountscompounds by thesuch thermomineral as H2S, CH water4 and thatammonium ascends (NH along4+) geological are supplied faults continuously from an artesian and in aquifer large amounts [5] located by at the a depththermomineral of 180 to 200water m inthat Mesozoic ascends limestonesalong geological [2]. Movile faults Cavefrom isan a artesian window aquifer of access [5] tolocated a groundwater at a depth 2 aquiferof 180 thatto 200 occupies m in Mesozoic a surface arealimestones of approximately [2]. Movile 50 Cave to 100 is km a windowand supports of access a partic- to a ulargroundwater hypogean aquifer ecosystem. that Otheroccupies windows a surface of accessarea of to approximately the aquifer are 50 the to old 100 hand-dug km2 and wellssupports in the a particular town of Mangalia hypogean and ecosystem. in the surrounding Other windows villages, of access as well to as the several aquifer thermal are the sulfidicold hand-dug springs wells located in the along town the of sea-shore, Mangalia at and distances in the surrounding of 1 to 3 km fromvillages, Movile as well Cave. as Severalseveral thermal of the endemic sulfidic speciessprings that located inhabit along Movile the sea-shore, Cave were at distances also encountered of 1 to 3 km in these from springsMovile andCave. wells. Several of the endemic species that inhabit Movile Cave were also encounteredAlong with in these CH4 springsand NH and4,H wells.2S represents the energy source for a wide variety of microorganisms [8] that use O , nitrate, sulfate, and ferric iron (Fe3+) as electron ac- Along with CH4 and NH4, H2 2S represents the energy source for a wide variety of ceptors [9–11]. The carbon fixed in situ by microorganisms, either swimming freely or microorganisms [8] that use O2 , nitrate, sulfate, and ferric iron (Fe3+) as electron acceptors congregated[9–11]. The incarbon thick biofilms,fixed in represents situ by themi foodcroorganisms, base of the either trophic swimming webs in Movile freely Cave. or Aquaticcongregated invertebrates in thick biofilms, that graze represents on microorganisms, the food base roam of the at thetrophic water webs surface in Movile where Cave. O2 is available in small concentrations. Terrestrial invertebrates are rarely found in the upper Aquatic invertebrates that graze on microorganisms, roam at the water surface where O2 dry sections of the cave, but they are unusually abundant in the lower, partially flooded is available in small concentrations. Terrestrial invertebrates are rarely found in the upper cave level (Figure1), in the Lake Room and the Air-Bells, where isopods, pseudoscorpions, dry sections of the cave, but they are unusually abundant in the lower, partially flooded millipedes, and insects feed on nearly any organic debris or graze on soil microorganisms, cave level (Figure 1), in the Lake Room and the Air-Bells, where isopods, while predatory chilopods and spiders chase their prey, consisting of isopods, collembola, pseudoscorpions, millipedes, and insects feed on nearly any organic debris or graze on beetles or other spiders. soil microorganisms, while predatory chilopods and spiders chase their prey, consisting Analogous chemosynthesis-based cave ecosystems, such as those in the Frasassi caves of isopods, collembola, beetles or other spiders. (Italy) [12–14], Melissotrypa Cave (Greece) [15], Ayyalon Cave (Israel) [16,17], and Tashan Analogous chemosynthesis-based cave ecosystems, such as those in the Frasassi Cave (Iran) [18–20], display comparable diversities of cave dwelling invertebrates with caves (Italy) [12–14], Melissotrypa Cave (Greece) [15], Ayyalon Cave (Israel) [16,17], and large numbers of endemisms (Table1). These ecosystems also depend primarily on in Tashan Cave (Iran) [18–20], display comparable diversities of cave dwelling invertebrates Diversity 2021, 13, 128 3 of 13 situ carbon fixation by chemoautotrophic microorganisms using the H2S present in water. The natural resources in these ecosystems sustain, just like in Movile Cave, the growth of diverse and complex microbial communities, that form biofilms. Table 1. The number of invertebrate species encountered in sulfidic cave ecosystems analogous to Movile Cave. All endemic species encountered in these sulfidic ecosystems are restricted to caves. Cave Species Present Endemic Species Movile Cave (Romania) 52 37 Frasassi caves (Italy) 56 16 Melissotrypa Cave (Greece) 30 8 Ayyalon Cave (Israel) 8 7 Tashan Cave (Iran) 3 3 These ecosystems can be appropriate examples for the ecological theory regarding the diversity-driven speciation [21] and convergent or parallel evolution.
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