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Anchialine Cave Environments: a novel chemosynthetic ecosystem and its ecology

Abstract

It was long thought that dark, nutrient depleted environments, such as the deep sea and subterranean caves, were largely devoid of life and supported low-density assemblages of endemic fauna. The discovery of hydrothermal vents in the 1970s and their subsequent study have revolutionized ecological thinking about lightless, low oxygen ecosystems. Symbiosis between chemosynthetic microbes and their eukaryote hosts has since been demonstrated to fuel a variety of marine foodwebs in extreme environments. We also now know these systems to be highly productive, exhibiting greater macrofaunal biomass than areas devoid of chemosynthetic influx. This dissertation research has revealed chemosynthetic bacteria and crustaceans symbionts that drive another extreme ecosystem - underwater anchialine caves - in which a landlocked, discrete marine layer rests beneath one or more isolated layers of brackish or freshwater.

Most anchialine caves contain low invertebrate abundances, yet some have inexplicably large biomasses of shrimp and remipedes, a rare crustacean class endemic to caves. Since only anecdotal evidence of remipede feeding in the field has been published and little ecological information about anchialine organisms is known, in situ studies are crucial to understanding whether there are direct or indirect links between chemosynthetic input into anchialine foodwebs and remipede abundance. This dissertation research integrates studies of geochemistry, microbiology, invertebrate food web dynamics, and behavior in these extreme ecosystems. Findings include the following: 1) highly stratified anchialine caves support communities of freeliving chemosynthetic bacteria, 2) Typhlatya pearsei, an anchialine shrimp, harbors chemosynthetic endosymbiotic bacteria, 3) the remipede, S. tulumensis, may also harbor chemosynthetic symbionts ectobiotically 4) food webs in the cave are complex and vary spatially, driving community structure changes 5) remipedes likely use chemical gradients and specialized chemosensory receptors to navigate in their lightless environment.

This combined body of research provides the first systematic study into anchialine ecology and has found them to be rich in taxa for comparative study with other chemosynthetic systems. For example, the finding of the first chemosynthetic endosymbiosis in a crustacean, T. pearsei, and the first chemosynthetic epibiosis in a remipede, S. tulumensis, allows for a variety of comparative coevolutionary studies. Typhlatya, a genus of troglobytic shrimp, are found in anchialine systems across the Caribbean and Bermuda and likely all contain chemoendosymbiotic bacteria. As such this discovery provides a springboard for comparative research into the transmission and evolution of chemosynthetic symbiotic associations. The most interesting outcomes, however, may result from comparing ecological and ecosystem function patterns described in caves to those known for deepwater as well as molluscan and annelid systems. Furthermore, anchialine systems, a primary source for agricultural, domestic, and industrial water use, are especially susceptible to climate change. Therefore, not only are studies of ecosystem function such as this imperative to conserving endemic cave fauna and their suitable habitat, but they may also help in the preservation of clean water caches for future generations.

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