Lifecycle Ecology of Deep-Sea Chemosymbiotic Mussels: A Review

Sven R Laming,Sylvie M Gaudron,Sébastien Duperron

doi:10.3389/fmars.2018.00282

Abstract

Mussels within the subfamily Bathymodiolinae, in particular the larger Bathymodiolus species (sensu lato) thriving at cold seeps and hydrothermal vents, are among the most iconic fauna to colonise deep-sea reducing habitats globally. Fuelled by energy derived from chemosynthetic symbioses, their contribution to ecosystem productivity is conspicuous, with many bathymodioline species forming dense, extensive aggregates. Chemosymbiotic mussels play crucial roles as ecosystem engineers, both through the formation of spatially heterogeneous biogenic reefs and in redistributing reduced-fluid emissions. The notable absence of Bathymodiolinae outside of reducing ecosystems affirms their dependency on these ephemeral habitats, placing spatiotemporal constraints on dispersal to, and colonisation of nascent, chemosynthetically active substrata. Thus, although symbioses may explain why these mussels are so productive in deep-sea reducing habitats, species’ survival over successive generations depends largely upon the adaptive characteristics of their lifecycle as a whole. Despite accumulating data on the biology and ecology of adults however, details remain fragmented regarding earlier developmental junctures during their complex lifecycles. This paper therefore brings together results from research undertaken over recent years on this topic, providing a synthesis of various lifecycle aspects of bathymodiolins from the earliest stages of development, gametogenesis, through to sexual maturity, including the intrinsic, emerging role of symbionts. The review provides a comprehensive overview of our current understanding and identifies areas where further study into these keystone organisms is warranted. The benefits of applying a lifecycle-integrated approach when evaluating the potential impacts of global change and the various activities that ultimately threaten habitats on deep-sea fauna are then discussed.

Highlights

Deep-sea habitats subject to reducing environmental conditions are colonized by a diverse array of specialist and generalist metazoan fauna, supported by chemosynthetic microbial primary production
Some of the most productive metazoan taxa are those that engage in chemosynthetic bacterial symbioses, where metabolic capabilities of the symbionts deliver energy resources that would otherwise be inaccessible directly to the host
This paper summarizes and integrates results from research undertaken over recent years, examining aspects of bathymodioline lifecycles along a developmental trajectory from gametogenesis to sexual maturity (Figure 1)

Summary

Introduction

Deep-sea habitats subject to reducing environmental conditions are colonized by a diverse array of specialist and generalist metazoan fauna, supported by chemosynthetic microbial primary production. Many larger bathymodiolins appear to be gonochoric, including two sets of phylogenetically distant sister species: B. azoricus and B. puteoserpentis from hydrothermal vent sites along the Mid-Atlantic Ridge (MAR) and “Bathymodiolus” mauritanicus and “B.” childressi from cold seeps in the West Nigerian margin and Gulf of Mexico respectively (Eckelbarger and Young, 1999; Tyler et al, 2007; Arellano and Young, 2009; Duperron et al, 2013), Le Pennec and Beninger (1997) identified immature oocytes in the periphery of male acini in B. elongatus suggesting protandric hermaphrodism, and Comtet et al (1999) suggested that B. azoricus might exhibit hermaphroditism.

Results

Conclusion