Trophic interactions among the macrofauna of the deep-sea hydrothermal vents of Alarcón Rise, Southern Gulf of California

https://doi.org/10.1016/j.dsr.2021.103609Get rights and content

Highlights

  • The trophic structure of the vent fauna of Alarcón Rise included five trophic guilds.

  • Among the primary consumers, the symbiont-bearing species were dominant in biomass.

  • The scavengers/detritivores were the most diverse guild, while predators were scarce.

  • The dominating carbon fixation pathway was the reverse tricarboxylic acid cycle.

  • The high δ34S value of 15.6 ‰ indicated photosynthetic inputs to the non-vent fauna.

Abstract

The Alarcón Rise (AR) hydrothermal system recently discovered in the Southern Gulf of California is characterized by the presence of black smokers, fluids with temperatures up to 360 °C, high concentrations of metal-sulfides and H2S. The trophic structure and the energy flow in the vent community were determined through the carbon (δ13C), nitrogen (δ15N), and sulfur (δ34S) isotopic signatures of 19 macrofaunal species. The δ13C values had an ample range from −36 and −8‰, reflecting a wide variety of carbon sources and the predominance of organic carbon fixed through the reductive tricarboxylic acid cycle (rTCA). The δ15N values varied from −7.9 and 18‰, corresponding to primary and secondary consumers, and the most enriched value (18‰) to a non-vent organism. Dominant organisms included primary consumers such as symbiont-bearing, and bacterivores, which revealed the importance of the bacterial consortium in the energy transfer. Secondary consumers comprised scavengers/detritivores, the most diverse guild, and predators, rather scarce. The δ34S values were between −14.5 and 15.6‰, indicating the assimilation of magmatic sulfur in the vent-fauna, and the complementary assimilation of photosynthetically derived organic matter in the non-vent organisms, hinted by their highest value (15.6‰). Interestingly, an unidentified Actiniaria anemone displayed anomalously depleted δ13C values (−30.4‰), reflecting a potential symbiotic relationship with sulfur-oxidizing endobacteria.

Introduction

Deep-sea hydrothermal vents are ecosystems associated with volcanic and tectonic activity and with extreme physical, chemical, geological, and biological conditions unlike any other environment found on Earth. Their discovery is relatively recent, in 1977 in the Galápagos Rift, so our understanding of these fascinating ecosystems is still developing. Up to 2018, about 721 vent fields had been discovered, 666 confirmed or inferred active and 55 inactive (Beaulieu et al., 2020), and with the increasing in oceanographic exploration and the development of state of the art technology, new vent systems are still being discovered.

Chemosynthetic processes sustain the biological diversity of hydrothermal vents, and the organic carbon flow and energy transfer through the different trophic levels are of crucial importance in maintaining the stability of these ecosystems. Microorganisms are the primary producers and obtain their energy through the oxidation of reduced compounds, mainly sulfides. However, the metabolism of vent autotrophs can also be supported by other organic carbon sources such as the flux of particulate organic matter (POC) from surface waters, and methane emissions from the seabed. Under this ecological scenario, trophic interactions and energy transfer among autotrophic and heterotrophic vent organisms are challenging to elucidate. Several authors (Van Dover, 2007; Soto, 2009; Van Audenhaege et al., 2019) have argued in favor of the employment of stable isotopes of carbon, nitrogen, and, more recently, sulfur, in order to discern potential carbon sources fueling hydrothermal systems and their trophic structure. The dual (δ13C and δ15N) or the threefold isotopic approaches (when sulfur is added to the analysis) provide valuable information on carbon fixation pathways, local nitrogen sources for primary producers or symbionts, trophic levels in heterotrophs (Thurber et al., 2010), and the detection of magmatic or biogenic sulfur sources.

The study of the AR vent communities is still in a descriptive stage. Initially, its benthic biological diversity and abundance were analyzed by Goffredi et al. (2017), who identified an assemblage of 43 species dominated by the siboglinid tubeworm Riftia pachyptila. The prokaryotic diversity of a surficial sediment core from AR was assessed by Espinosa-Asuar et al. (2020), who identified a sulfur-related bacterial community including abundant Thioalkalivibrio and Desulfobulbus, and taxa involved in iron reduction, such as Deferrisoma and Mariprofundus. The geological and geochemical features were further described by Paduan et al. (2018) and Clague et al. (2018).

The functional role and ecological interactions of the biotic communities of the Alarcón Rise vents are poorly understood. Hence, the objective of this research is to analyze the trophic structure of the macrofaunal assemblage of the vent fields of this area using stable isotopes of carbon (δ13C), nitrogen (δ15N) and sulfur (δ34S). Given the environmental conditions prevailing in the study area, we assume the existence of contrasting carbon fixation pathways and perhaps different trophic structures in comparison with neighboring hydrothermal systems in the Gulf of California.

Section snippets

Study area

The Alarcón Rise (AR), located at the mouth of the Gulf of California at 2300 m depth, is the northernmost bare rock spreading segment of the East Pacific Rise (EPR) (Fig. 1) (Clague et al., 2018; Paduan et al., 2018). The AR is a basalt-hosted system characterized by the presence of black smokers and chimneys up to 33 m tall, composed of iron, copper, and zinc sulfides. Their fluids contain high concentrations of H2S and metal-sulfides and reach a maximum temperature of 360 °C (Paduan et al.,

Stable isotope values

A total of 545 specimens encompassing 19 species were analyzed (Fig. 2). Their distribution in the vent system of Alarcón Rise is depicted in Fig. 2, while their δ13C, δ15N, and δ34S ratios are summarized in Table 1.

The δ13C values of the fauna ranged from −36 to −8‰. The most depleted values corresponded to the vesicomyid clam Calyptogena magnifica, whereas the most enriched values were detected in the polychaete worms Alvinella pompejana and Riftia pachyptila (Table 1). The δ15N values varied

Carbon isotope values (δ13C)

The vesicomyid clam C. magnifica exhibited the most depleted δ13C values (-32.4‰ to −36‰; Table 1), influenced by the symbiotic sulfur-oxidizing bacteria this species harbors, which assimilate the carbon fixed through the CBB cycle, presenting δ13C values lower than −22‰ (Roeske and O’Leary, 1984; Robinson et al., 2003; Reid et al., 2013). Actiniaria sp. 2 had the second most depleted δ13C value (−30.4‰), suggesting that this species potentially harbors thiotrophic bacteria or filter-feeds on

Conclusions

The three-prong isotopic approach, employing δ13C, δ15N, and δ34S as biochemical tracers, was applied to unravel complex trophic interactions among macrofauna at the newly discovered Alarcón Rise hydrothermal vent system, where previously only biological diversity had been described. The δ13C values indicated the predominance of organic carbon fixed through the rTCA, whose enzymatic machinery functions efficiently under temperatures from 20°C to 90°C. The δ15N values revealed the existence of

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

Special thanks to Robert Vrijenhoek, for his invaluable help during the development of this project and for his comments that greatly improved this manuscript. Thanks to K. Walz, L. Lundsten, E. Krylova, G. Rouse, D. Clague, R. Zierenberg, J. Armstrong-Altrin, E. López, and S. Chakraborty for their assistance. Thanks also to the captain and crew of the R/V Western Flyer and the pilots of the ROV Doc Ricketts. Thanks to the two anonymous reviewers for their positive criticism to our scientific

References (48)

  • D.C. Bergquist et al.

    Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web

    Mar. Ecol. Prog. Ser.

    (2007)
  • M. Biscoito et al.

    Fishes from the hydrothermal vents and cold-seeps, an update

    Cah. Biol. Mar.

    (2002)
  • A. Bourbonnais et al.

    Subseafloor nitrogen transformations in diffuse hydrothermal vent fluids of the Juan de Fuca Ridge, evidenced by the isotopic composition of nitrate and ammonium

    Geochem. Geophys.

    (2012)
  • D.A. Butterfield et al.

    Seafloor eruptions and evolution of hydrothermal fluid chemistry

    Phil. Trans. Roy. Soc. Lond.

    (1997)
  • B.J. Campbell et al.

    The versatile epsilon-proteobacteria: key players in sulphidic habitats

    Nat. Microbiol. Rev.

    (2006)
  • S.C. Cary et al.

    Worms bask in extreme temperatures

    Nature

    (1998)
  • P. Chevaldonne et al.

    Some like it hot… and some even hotter

    Nature

    (1992)
  • D.A. Clague et al.

    Geology of the Alarcon Rise, southern Gulf of California

    Geochem. Geophys.

    (2018)
  • M. Daly et al.

    The first sea anemone (Cnidaria: anthozoa: Actiniaria) from a whale fall

    J. Nat. Hist.

    (2007)
  • D. Desbruyéres et al.

    Handbook of Deep-Sea Hydrothermal Vent Fauna

    (1997)
  • D. Desbruyères et al.

    Données écologiques sur unnouveau site d’hydrothermalisme actif de la ride du Paci-fique oriental. CR Acad

    Sci. Paris, Sér III

    (1982)
  • L. Espinosa-Asuar et al.

    Chapter 7, Bacterial communities from deep hydrothermal systems: the Southern Gulf of California as an example or primeval environments

  • C.R. Fisher et al.

    Nutritional interactions in Galapagos Rift hydrothermal vent communities: inferences from stable carbon and nitrogen isotope analyses

    Mr. Ecol. Prog. Ser.

    (1994)
  • S.K. Goffredi et al.

    Hydrothermal vent fields discovered in the southern Gulf of California clarify the role of habitat in augmenting regional diversity

    Proc. R. Soc. Lon. B Biol.

    (2017)

    • Cited by (5)

    • Insights into the functional role of fungi in deep-sea hydrothermal vents through the analysis of stable isotopes of carbon, nitrogen, and sulfur

      2023, Fungal Ecology

    • Metal bioaccumulation and transfer in benthic species based on isotopic signatures of individual amino acids in South China Sea cold seep environments

      2023, Environmental Pollution
      Citation Excerpt :

      These results suggest that water exposure or bacterial assimilation was the major metal source for the higher trophic level species. Predators have different nutrient strategies of symbiont-bearing, filter-feeders, bacterivores from symbiotic bacteria, subsurface bacteria, and attached bacteria individually in chemoautotrophic environments (Salcedo et al., 2021). Certain metals were anomalously enriched in sediments and pore fluids at cold hydrocarbon seeps (Wang et al., 2019b), which were reflected by corresponding enrichments in these cold seep benthic tissues (Fig. 6).

    • Trophic diversity of chemosymbiont hosts in deep-sea hydrothermal vents using amino acid nitrogen isotopes

      2023, Frontiers in Marine Science

    • Niche partitioning of hydrothermal vent fauna in the North Fiji Basin, Southwest Pacific inferred from stable isotopes

      2022, Marine Biology

    • Fungal Diversity in Sediments From Deep-Sea Extreme Ecosystems: Insights Into Low- and High-Temperature Hydrothermal Vents, and an Oxygen Minimum Zone in the Southern Gulf of California, Mexico

      2022, Frontiers in Marine Science
    1

    Present address: Instituto de Biología, Universidad Nacional Autónoma de México, Tercer Circuito s/n, Ciudad Universitaria, 04510, Mexico City, Mexico.

    2

    Retired.

    View full text
    © 2021 Elsevier Ltd. All rights reserved.