Integrative taxonomy revisits the ontogeny and trophic niches ofRimicarisvent shrimps

Abstract

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: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria

“…Among the 519 juveniles examined from the July 1997 expedition, Shank et al (1998) found no males and suggested that: (1) male sexual characteristics were not displayed by juveniles, or (2) R. exoculata could be a protogynous hermaphrodite. Komai & Segonzac (2008) reported that the smallest male they determined by the pleopod morphology was 10.1 mm in carapace length, corresponding to their stage D, or subadults (stage C-subadults for Methou et al 2020), corroborating the first hypothesis of Shank et al (1998).…”

“…Vereshchaka (1997) indicated a settling stage between 3 and 5 mm in carapace length. The smallest stage A juvenile collected, close to adults, by Methou et al (2020) was 5.7 mm in carapace length.…”

“…Upon examination of the abundant specimens of postlarval stages, covering a wide range of sizes (rostral carapace length between 4.8 and 17.4 mm), Komai & Segonzac (2008) described 4 ontogenetic stages (A, B, C and D-subadult), with a dramatic morphological change at size of 7−9 mm in carapace length. In a recent study, Methou et al (2020) revised the ontogenetic description of R. exoculata larvae combining morphological observations and DNA identification. These authors proposed 3 ontogenetic stages, A, B and C-subadult.…”

“…During these stages, no significant increase in size was noticed, with the shrimp probably spending most of its energy for great morphological changes rather than increases in body size (Komai & Segonzac 2008). The most notable changes are the progressive reduction of the rostrum, the fusion of the eye-stalk, the inflation of the branchiostegite, the appearance of numerous plumose setae on the swelling scaphognathites and exo podites (Komai & Segonzac 2008, Methou et al 2020) and a gradual increase in bacterial abundance between 8 and 10 mm in carapace length (Veresh chaka 1996, Gebruk et al 2000. Among the 519 juveniles examined from the July 1997 expedition, Shank et al (1998) found no males and suggested that: (1) male sexual characteristics were not displayed by juveniles, or (2) R. exoculata could be a protogynous hermaphrodite.…”

“…When arriving at vents, juveniles carry abundant stores of lipids of photosynthetic origin. The carbon stable isotope ratio (δ 13 C) showed a graded increase from juveniles, through smaller adults to the older specimens (Gebruk et al 1997b, Polz et al 1998, Methou et al 2020, corresponding to the gradual introduction in the diet of carbon of bacterial chemosynthetic origin. There is also an increase in the proportion of the heavy isotope of nitrogen between the juvenile and the adult stages, which is probably due to epibiont metabolism processes using nitrate (Methou et al 2020).…”