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Groundwater Biodiversity in a Chemoautotrophic Cave Ecosystem: How Geochemistry Regulates Microcrustacean Community Structure

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Groundwater Biodiversity in a Chemoautotrophic Cave Ecosystem: How Geochemistry Regulates Microcrustacean Community Structure Aquat Ecol DOI 10.1007/s10452-016-9599-7 Groundwater biodiversity in a chemoautotrophic cave ecosystem: how geochemistry regulates microcrustacean community structure Diana M. P. Galassi . Barbara Fiasca . Tiziana Di Lorenzo . Alessandro Montanari . Silvano Porfirio . Simone Fattorini Received: 24 May 2016 / Accepted: 8 September 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract The Frasassi cave system in central Italy analysis separated the copepod assemblages inhabit- hosts one of the few known examples of a ground- ing dripping pools from those of sulfidic lakes. H2S water metazoan community that is supported by concentration, pH and O2 concentration were iden- sulfur-based lithoautotrophic microbes. Despite the tified as the main factors regulating community challenging conditions represented by high concen- structure. These results indicate that the distribution trations of H2S and low concentrations of O2, this of groundwater copepods within the cave system is cave system is home to many invertebrate species. ecologically and spatially structured. Sulfidic lakes Here, we analyzed the copepods inhabiting sulfidic showed lower Simpson dominance, higher Shannon lakes and non-sulfidic dripping pools in order to diversity and higher Pielou equitability at higher H2S investigate how environmental conditions in sulfidic concentrations. The complex community structure of waters regulate the spatial distribution of the cave the copepods of the Frasassi cave system suggests microcrustacean community over time. We also that a chemosynthetically produced food source sampled copepod assemblages of sulfidic lakes under facilitated the colonization of stygobionts in sulfidic conditions of both high and low H2S concentration. groundwater due to their tolerance to the environ- Cluster analysis and canonical correspondence mental conditions. Keywords Frasassi cave system Á Italy Á Groundwater Á Biodiversity Á Chemoautotrophy Handling Editor: Michael T. Monaghan. Electronic supplementary material The online version of this article (doi:10.1007/s10452-016-9599-7) contains supple- mentary material, which is available to authorized users. D. M. P. Galassi (&) Á B. Fiasca Á S. Porfirio Á A. Montanari S. Fattorini Geological Observatory of Coldigioco, Cda. Coldigioco 4, Department of Life, Health and Environmental Sciences, 62021 Apiro, Italy University of L’Aquila, via Vetoio, Coppito, 67100 L’Aquila, Italy S. Fattorini e-mail: [email protected] Departamento de Cieˆncias e Engenharia do Ambiente, CE3C – Centre for Ecology, Evolution and Environmental T. Di Lorenzo Changes/Azorean Biodiversity Group and Universidade Institute of Ecosystem Study, ISE-CNR, via Madonna del dos Ac¸ores, Angra do Heroı´smo, Ac¸ores, Portugal Piano 10, Sesto Fiorentino, 50019 Florence, Italy 123 Aquat Ecol Introduction ectosymbiosis with sulfur-oxidizing bacteria was also postulated (Dattagupta et al. 2009), and some obser- Sulfidic caves represent rare and still very poorly vations on the ecology of ostracods (Peterson et al. known groundwater ecosystems (Engel 2007). The 2013). Although copepods are by far the most presence of toxic gases and reduced oxygen levels abundant and species-rich animal group in groundwa- makes it difficult to sample sulfidic caves, which is a ter (Galassi et al. 2014), there is no available reason of this lack of knowledge. In the case of information on the species inhabiting the Frasassi groundwater species, sampling procedures are further cave system. complicated by the temporal and spatial variability of In this paper, we analyzed the Frasassi copepod the hydrogeological and hydrochemical conditions of assemblages sampled at various sites characterized by these environments (Galdenzi et al. 2008; Flot et al. different geochemical conditions to understand the 2010), and faunal lists are available for only a very influence of environmental variables on community small number of sulfidic cave systems (Engel 2007). structure. For this purpose, we analyzed the compo- Although lithoautotrophic microbes of sulfidic caves sition of copepod assemblages across different habitat can be able to maintain relatively rich and diversified types in the cave system, including both sulfidic lakes invertebrate communities, sulfur-oxidizing chemoau- (at different H2S concentrations) and non-sulfidic totrophy also generates environmental conditions that dripping pools. allow only highly specialized species to survive. Thus, In particular: sulfidic invertebrate communities are recognized as an example of ‘‘life at extremes’’ (Lee et al. 2012), where 1. We tested whether the species composition of the the only successful species are those able to cope with groundwater assemblages is ecologically and low O2 and high H2S concentrations (Galdenzi et al. spatially structured according to the geochemical 2008; Macalady et al. 2008). conditions of different water bodies within the Large cave systems may include both sulfidic and cave system. Our hypothesis is that, if sulfide non-sulfidic groundwater bodies, thus offering the concentration is a key factor in determining opportunity of investigating how communities species composition, assemblages in the sulfidic respond to the exceptionally high selective pressures lakes should be profoundly different from those of represented by sulfidic conditions in comparison with dripping pools. Also, we hypothesized that communities of non-sulfidic environments within the species composition of the investigated lakes is same cave system. However, probably because of influenced by temporal variations in the sulfide difficulties in conducting standardized sampling in concentration (i.e., high- vs. low-sulfide concen- sulfidic caves and the rarity of these ecosystems, no tration, thereafter H and L, respectively). study attempted to determine the effects of geochem- 2. We tested whether different environmental ical parameters on their animal community structure parameters have different roles in determining (Engel 2012). species composition and abundance. Namely, we The large Frasassi cave system (central Italy) hypothesized that high-sulfide concentration represents an exceptionally well-suited model for should be an important driver of species compo- such a study. The Frasassi cave system is among the sition of lake assemblages, whereas dripping pool most studied sulfidic cave ecosystems in the world assemblages should be composed of species (Galdenzi 1990; Sarbu et al. 2000; Macalady et al. associated with higher oxygen concentration and 2006, 2008; Galdenzi et al. 2008; Jones et al. higher pH values. 2010, 2015). Its invertebrate fauna is represented by 3. We tested whether different sulfide concentrations gastropods (Bodon and Cianfanelli 2012) and pre- determine differences in species dominance, dominantly by crustaceans, especially amphipods diversity and equitability in the copepod commu- (Flot et al. 2010; Bauermeister et al. 2012, 2013; Fisˇer nity inhabiting the sulfidic lakes. We hypothe- et al. 2015) and ostracods (Peterson et al. 2013). sized that if H2S concentration is the major driver Previous research on the crustaceans of the Frasassi of species community structure, temporal varia- cave system involved evolutionary studies on amphi- tions in H2S concentration should be reflected in pods (Flot et al. 2010; Fisˇer et al. 2015), for which changes in the community structure. 123 Aquat Ecol Fig. 1 Map of the Frasassi cave system (central Italy) showing the location of the sampling sites (modified after Flot et al. 2010) Copepod species were classified according to their Materials and methods degree of dependence on groundwater into two main ecological categories: stygobites and non-stygobites. Geological setting Stygobites are species that complete their entire life cycle in groundwater, being unable to survive and The Frasassi cave system (coordinates WGS84-G: reproduce in surface-water habitats. Non-stygobites 43.402°N, 12.962°E, Fig. 1) consists of several inter- are species living in surface freshwater; they may enter connected levels, as a result of alternating erosion and groundwater both actively and passively (Galassi deposition driven by Quaternary glacial–interglacial 2001). cycles during a steady, generalized tectonic uplift of 123 Aquat Ecol the region around the Frasassi Gorge, a long and steep Different lakes within the cave system have widely canyon eroded by the Sentino River. The cave system different H2S and O2 concentrations (Macalady et al. develops in the Calcare Massiccio, a limestone 2008; Flot et al. 2010). Some small lakes, as Lago platform interspersed with a network of fractures. Verde (Grotta del Fiume, Fig. 2a, b) and Lago Claudia The plateau overlies the uppermost Triassic Burano (Grotta Grande del Vento), are fed more directly by Formation, which consists of a 2000-m-thick succes- the deep sulfidic zone of the aquifer, with a lower sion of evaporitic anhydrites, black shales and bitu- contribution of bicarbonate water formed above the minous limestones. The presence of marls and chert sulfidic stratum due to the very slow groundwater overlying the Calcare Massiccio limits rock perme- flow. Conversely, Lago della Bottiglia (Pozzo dei ability and the seepage network feeding the aquifer Cristalli; Fig. 2c) tends to be less sulfidic than Lago (Sarbu et al. 2000; Galdenzi et al. 2008; Galdenzi Verde and Lago Claudia, both in dry and wet periods 2012). (Peterson et al. 2013). Freshwater seepage and occa- The groundwater is of two types: bicarbonate and sional runoff feed not only the sulfidic
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