Among hydrothermal vent species, Rimicaris exoculata is one of the most emblematic, hosting abundant and diverse ectosymbioses that provide most of its nutrition. Rimicaris exoculata co-occurs in dense aggregates with the much less abundant Rimicaris chacei in many Mid-Atlantic Ridge vent fields. This second shrimp also houses ectosymbiotic microorganisms but has a mixotrophic diet. Recent observations have suggested potential misidentifications between these species at their juvenile stages, which could have led to misinterpretations of their early-life ecology. Here, we confirm erroneous identification of the earliest stages and propose a new set of morphological characters unambiguously identifying juveniles of each species. On the basis of this reassessment, combined use of C, N and S stable isotope ratios reveals distinct ontogenic trophic niche shifts in both species, from photosynthesis-based nutrition before settlement, towards a chemosynthetic diet afterwards. Furthermore, isotopic compositions in the earliest juvenile stages suggest differences in larval histories. Each species thus exhibits specific early-life strategies that would, without our re-examination, have been interpreted as ontogenetic variations. Overall, our results provide a good illustration of the identification issues persisting in deep-sea ecosystems and the importance of integrative taxonomy in providing an accurate view of fundamental aspects of the biology and ecology of species inhabiting these environments.

Rimicaris exoculata is one of the most well-known and emblematic species of endemic vent fauna. Like many other species from these ecosystems, Rimicaris shrimps host important communities of chemosynthetic bacteria living in symbiosis with their host inside the cephalothorax and gut. For many of these symbiotic partners, the mode of transmission remains to be elucidated and the starting point of the symbiotic relationship is not yet defined, but could begin with the egg. In this study, we explored the proliferation of microbial communities on R. exoculata broods through embryonic development using a combination of NGS sequencing and microscopy approaches. Variations in abundance and diversity of egg microbial communities were analyzed in broods at different developmental stages and collected from mothers at two distinct vent fields on the Mid-Atlantic Ridge (TAG and Snake Pit). We also assessed the specificity of the egg microbiome by comparing communities developing on egg surfaces with those developing on the cuticle of pleopods, which are thought to be exposed to similar environmental conditions because the brood is held under the female’s abdomen. In terms of abundance, bacterial colonization clearly increases with both egg developmental stage and the position of the egg within the brood: those closest to the exterior having a higher bacterial coverage. Bacterial biomass increase also accompanies an increase of mineral precipitations and thus clearly relates to the degree of exposure to vent fluids. In terms of diversity, most bacterial lineages were found in all samples and were also those found in the cephalothorax of adults. However, significant variation occurs in the relative abundance of these lineages, most of this variation being explained by body surface (egg vs. pleopod), vent field, and developmental stage. The occurrence of symbiont-related lineages of Epsilonbacteraeota, Gammaproteobacteria, Zetaproteobacteria , and Mollicutes provide a basis for discussion on both the acquisition of symbionts and the potential roles of these bacterial communities during egg development.

Among the endemic and specialized fauna from hydrothermal vents, Rimicaris shrimps constitute one of the most important and emblematic components of these ecosystems. On the Mid-Atlantic Ridge, 2 species belonging to this genus co-occur: R. exoculata and R. chacei that differ in their morphology, trophic regime and abundance. R. exoculata forms large and dense aggregations on active vent chimney walls in close proximity to vent fluid emissions, whereas R. chacei is much less conspicuous, living mostly in scattered groups or solitary further away from the fluids. However, the recent revision of Rimicaris juvenile stages from the Mid-Atlantic Ridge shows that R. chacei abundance would be higher than expected at these early life stages. Here, we describe and compare the population structure of R. exoculata and R. chacei at the Snake Pit and Trans-Atlantic Geotraverse (TAG) vent fields. We show distinct population demographics between the 2 co-occurring shrimp species with a large post-settlement collapse in R. chacei populations suggesting high juvenile mortality for this species. We describe important spatial segregation patterns between the 2 species and their different life stages. Additionally, our results highlight distinct niches for the earliest juvenile stages of both R. exoculata and R. chacei, compared with all other life stages. Finally, we discuss the potential factors, including predation and competitive interactions, that could explain the differences we observed in the population structure of these 2 species.

The symbiotic shrimp Rimicaris exoculata dominates the macrofauna inhabiting the active smokers of the deep-sea mid Atlantic ridge vent fields. We investigated the nature of the host mechanisms controlling the vital and highly specialized ectosymbiotic community confined into its cephalothoracic cavity. R. exoculata belongs to the Pleocyemata, crustacean brooding eggs, usually producing Type I crustins. Unexpectedly, a novel anti-Gram-positive type II crustin was molecularly identified in R. exoculata. Re-crustin is mainly produced by the appendages and the inner surfaces of the cephalothoracic cavity, embedding target epibionts. Symbiosis acquisition and regulating mechanisms are still poorly understood. Yet, symbiotic communities were identified at different steps of the life cycle such as brooding stage, juvenile recruitment and molt cycle, all of which may be crucial for symbiotic acquisition and control. Here, we show a spatio-temporal correlation between the production of Re-crustin and the main ectosymbiosis-related life-cycle events. Overall, our results highlight (i) a novel and unusual AMP sequence from an extremophile organism and (ii) the potential role of AMPs in the establishment of vital ectosymbiosis along the life cycle of deep-sea invertebrates.

Variations in offspring production according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure based on non‐photosynthetic primary production, these relationships remain largely under‐studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps as a study case to explore relationships between reproduction, diets, and food supply in these environments. For that, we compared reproductive outputs of three congeneric shrimps differing by their diets. They inhabit vents located under oligotrophic waters of tropical gyres with opposed latitudes, allowing us to also examine the prevalence of phylogenetic vs environmental drivers in their reproductive rhythms. For this, we used both our original data and a compilation of published observations on the presence of ovigerous females covering various seasons over the past 35 years. We report distinct egg production trends between Rimicaris species relying solely on chemosymbiosis— R. exoculata and R. kairei —and one relying on mixotrophy, R. chacei . Besides, our data suggest a reproductive periodicity that does not correspond to seasonal variations in surface production, with substantial proportions of brooding females during the same months of the year, despite those months corresponding to either boreal winter or austral summer depending on the hemisphere. These observations contrast with the long‐standing paradigm in deep‐sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from the surface. Our results suggest the presence of an intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year‐round observations in order to understand the life history of vent animals.

Hydrothermal vent shrimps in the genus Rimicaris are among the most charismatic deep-sea animals of Atlantic and Indian Oceans, often occurring on towering black smokers in dense aggregates of thousands of individuals. Although this dominance is only possible because of symbiosis, no study on the symbiosis of Indian Ocean Rimicaris species has been conducted.

Among the endemic and specialized fauna from hydrothermal vents, Rimicaris shrimp surely constitutes one of the most important and emblematic component of these ecosystems. In the Mid Atlantic Ridge, two species affiliated to this genus co-occur: Rimicaris exoculata and Rimicaris chacei that differ by their morphology, their trophic regime as well as by their abundance. The first forms large and dense aggregations on active vent chimney walls in close proximity to vent fluid emissions, whereas the second is recognized as much less conspicuous, living mostly in scattered groups or solitary further away from the fluids. However, the recent revision of Rimicaris juvenile stages from the Mid Atlantic Ridge show that R. chacei abundance would be higher than expected at these early life stages. Here, we describe and compare the population structures of R. exoculata and R. chacei at the Snake Pit and TAG vent fields. We show widely distinct population demographics between the two co-occurring shrimps with a large post settlement collapse in R. chacei population suggesting a large juvenile mortality for this species. We also observe important spatial segregation patterns between the two species and their different life stages. Additionally, our results highlight distinct niches for the earliest juvenile stages of both R. exoculata and R. chacei, compared to all the other life stages. Finally, we discuss the potential factors - predation and competitive interactions among others - that could explain the differences we observe in the population structure of these two species.

Connectivity among isolated habitat patches via planktonic larval dispersal is crucial for maintaining the regional diversity of hydrothermal vents. Despite, increasing sophistication of techniques for simulating dispersal, limited information on biological and behavioural traits of vent-associated species has unknown affects on the applicability of these methods for conservation. Here we focus on the role of periodic reproduction on dispersal among hydrothermal vents, as periodic spawning has increasingly been observed in a variety of taxa. For generalizeability, we simulate the dispersal of larvae under treatments of periodic and aperiodic release timing at various depths, with a consistant but variable planktonic larval duration. Our results show a highly variable effect of periodicity on the characteristics and distribution of dispersal, which are heavily modified by the dispersal depth and source location. The capacity for reproductive periodicity to impact the among-site dispersal warrents further investigation into its prevelance and timing among vent-associated fauna.