Morphology of First Zoeal Stage of Four Genera of Alvinocaridid Shrimps from Hydrothermal Vents and Cold Seeps: Implications for Ecology, Larval Biology and Phylogeny.

Iván Hernández-Ávila,Florence Pradillon,Marie-Anne Cambon-Bonavita

doi:10.1371/journal.pone.0144657

Abstract

Alvinocaridid shrimps are endemic species inhabiting hydrothermal vents and/or cold seeps. Although indirect evidences (genetic and lipid markers) suggest that their larval stages disperse widely and support large scale connectivity, larval life and mechanisms underlying dispersal are unknown in alvinocaridids. Here we provide for the first time detailed descriptions of the first larval stage (zoea I) of four alvinocaridid species: Rimicaris exoculata and Mirocaris fortunata from the Mid-Atlantic Ridge, Alvinocaris muricola from the Congo Basin and Nautilocaris saintlaurentae from the Western Pacific. The larvae were obtained from onboard hatching of brooding females (either at atmospheric pressure or at habitat pressure in hyperbaric chambers) and from the water column near adult habitats, sampled with plankton pumps or sediment traps. Major characteristics of the alvinocaridid larvae include undeveloped mandible and almost complete absence of setation in the inner margin of the mouth parts and maxillipeds. Although the larvae are very similar between the four species studied, some morphological features could be used for species identification. In addition, undeveloped mouthparts and the large amount of lipid reserves strongly support the occurrence of primary lecithotrophy in the early stage of alvinocaridids. Although lecithotrophy in decapod crustaceans is usually associated with abbreviated larval development, as a mechanism of larval retention, morphological and physiological evidences suggest the occurrence of an extended and lecithotrophic larval stage in the Alvinocarididae. These traits permit the colonization of widely dispersed and fragmented environments of hydrothermal vents and cold seeps. Distribution of larval traits along the phylogenetic reconstruction of the Alvinocarididae and related families suggest that lecithotrophy/planktotrophy and extended/abbreviated development have evolved independently along related families in all potential combinations. However, the Alvinocarididae is the only taxa with a combination of lecithotrophy and extended larval development.

Highlights

Shrimps of the family Alvinocarididae inhabit deep-waters in the Atlantic, Pacific and Indian Oceans, usually at depths greater than 1000 m [1]
Brooding females of Rimicaris exoculata, Mirocaris fortunata, Nautilocaris saintlaurentae and Alvinocaris muricola were collected from hydrothermal vents on the Mid-Atlantic Ridge (R. exoculata and M. fortunata), in the Western Pacific (N. saintlaurentae), and at cold seeps of the Congo Basin (A. muricola) (Table 1)
The similarity between the larvae of R. exoculata obtained on board from hatching at atmospheric pressure or in pressurized chambers and in the plankton pump demonstrates that the low degree of development of mouth parts is neither the product of an ontogenetic anomaly caused by the pre-hatching decompression nor abnormal early hatching of undeveloped larvae

Summary

Introduction

Shrimps of the family Alvinocarididae inhabit deep-waters in the Atlantic, Pacific and Indian Oceans, usually at depths greater than 1000 m [1]. Some species such as Rimicaris exoculata harbour symbiotic bacteria in their gill chambers and within their guts, which supply nutrients to the shrimp in a complex mutualistic association [4], whereas other species depend on grazing on chemoautotrophic bacteria and detritus in their adult stage [2] Populations of these shrimps exhibit high genetic connectivity along the MidAtlantic Ridge [5], between different vent and cold seeps systems in the Atlantic [6] and in vents systems of the Western Pacific and Indian Oceans [7,8]. Published data on larval forms of alvinocaridid shrimps include only brief descriptions or some illustrations, but without clues about important larval traits, differences between species or comparison with other caridean shrimps

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Discussion

Conclusion