Trophic structure and energy flow in a shallow-water hydrothermal vent: Insights from a stable isotope approach.

Ni-Na Chang,Li-Hung Lin,Pei-Ling Wang,Tzu-Hsuan Tu,Ming-Shiou Jeng,Yoshito Chikaraishi,Vanesa Magar

doi:10.1371/journal.pone.0204753

Abstract

Shallow-water hydrothermal vent ecosystems are distinct from the deep-sea counterparts, because they are in receipt of sustenance from both chemosynthetic and photosynthetic production and have a lack of symbiosis. The trophic linkage and energy flow in these ecosystems, however remain elusive, which allows us poor understanding of the whole spectrum of biological components distributed across such environmental gradients. In this study, a thorough isotopic survey was conducted on various biological specimens and suspended particulates collected along four transects across the venting features of a shallow-water hydrothermal field off Kueishan Island, Taiwan. The isotope data combined with a Bayesian-based mixing model indicate that the vent-associated particulate organic matter (vent POM), as primary contribution of chemoautotrophic populations, has a high δ13C value (−18.2 ± 1.1‰) and a low δ15N value (−1.7 ± 0.4‰). Zooplankton and epibenthic crustaceans, as the fundamental consumers, exhibit δ13C and δ15N values ranging from −21.3 to −19.8‰ and +5.1 to +7.5‰, respectively, and can utilize the vent POM for 38–53% of their diets. The vent-obligate crab Xenograpsus testudinatus shows a large variation in δ13C (from −18.8 to −13.9‰) and δ15N values (from 1.1 to 9.8‰), although an omnivorous trophic level (2.5) is identified for it using δ15N values of amino acids, and it can utilize the vent POM for 6–87% of its diet. The consistently low (< 10.0‰) and overlapping δ15N values for most of the analyzed macroinvertebrates suggest extensive ingestion of chemosynthetic production complementing the photosynthetic production, a weak prey–predator relationship and low trophic complexity possibly imposed by the extreme environmental contexts of shallow-water hydrothermal ecosystems.

Highlights

Studies of hydrothermal vent ecosystems distributed along mid-ocean ridges and back-arc spreading centers have greatly expanded our knowledge regarding the energy sources of marine communities
During our visual survey through scuba diving, the vent crab X. testudinatus constituted the majority of the faunal abundance, followed by the sea anemones Anthopleura sp. and sea snails A. misera
The sea snails were generally present with patches of green macroalgae (C. catenata) with A. misera being more abundant than E. contractus

Summary

Introduction

Studies of hydrothermal vent ecosystems distributed along mid-ocean ridges and back-arc spreading centers have greatly expanded our knowledge regarding the energy sources of marine communities. The discharge of hot, reducing fluids into the cold, oxidized deep sea facilitates the generation of strong redox and temperature gradients, both of which favor the colonization of microbial communities possessing various physiological characteristics. These chemoautotrophic microbes efficiently sustain vent communities via bacteria–invertebrate symbioses or heterotrophic consumption, rendering deep-sea vent ecosystems analogous to oases in the desert [3]. Determining the energy flow would, provide an important basis to quantify the potential export of geothermal energy and chemical fluxes from vent ecosystems to the open ocean [4,5] Distinct from their deep-sea counterparts, shallow-water hydrothermal vents occur in coastal euphotic zones. The respective contributions of photosynthetic and chemoautotrophic primary production to benthic and even pelagic communities are poorly understood and a quantitative picture of energy transfer in such ecosystems is required

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