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

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.

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

“…To date, no bacteria have been observed inside eggs of R. exoculata, but Gammaproteobacteria and Campylobacteria have been reported on their surface (Guri et al 2012, Cowart et al 2017, Methou et al 2019). In the same way, bacterial symbionts appear to be absent in the branchial chamber of post-hatching larvae of R. exoculata (Guri et al 2012, Hernandez-Avila et al 2015 or in their first juvenile stages after recruitment (Komai & Segonzac 2008). Some Campylobacteria and Gammaproteobacteria sequences retrieved from Rainbow seawater samples were closely related (99% similarity) to epibiont sequences from the branchial chamber of shrimp from the same site (Guri et al 2012).…”

“…For example, Vereshchaka et al (1998) noted that R. exoculata is represented in Russian collections by thousands of individuals, among which brooding females are absent. This absence was linked to seasonal breeding and sampling efforts almost entirely restricted to the summer months (Gebruk et al 1997a, Herring 1998, Vereshchaka et al 1998, Ramirez-Llodra et al 2000, Guri et al 2012, Hernandez-Avila et al 2015, Hernandez-Avila 2016. It was also suggested that ovigerous R. exoculata leave the aggregations around high temperature vents, where samples are generally collected, to protect the embryos from hydrothermal fluids and from the risk of mechanical damage caused by the highly active shrimp aggregations (Ramirez-Llodra et al 2000).…”

“…It was also suggested that ovigerous R. exoculata leave the aggregations around high temperature vents, where samples are generally collected, to protect the embryos from hydrothermal fluids and from the risk of mechanical damage caused by the highly active shrimp aggregations (Ramirez-Llodra et al 2000). Brooding females were finally collected among the shrimp aggregations, first in March 2007 at the Logatchev site (Guri et al 2012) and more recently from January to March 2014 and 2018, at the TAG and Snake Pit sites (Hernandez-Avila et al 2015, Methou et al 2019. This supports the first hypothesis of seasonal reproduction.…”

“…The first larvae of R. exoculata were sampled in March 2007 at the Logatchev site (Guri et al 2012) and were described from a January 2014 collection at the TAG site (Hernandez-Avila 2016). They were obtained either from onboard hatching of brooding females or, using a larval pump, from the water column near adults (Hernandez-Avila et al 2015). The detailed description of the first larval stage (zoea I) of R. exoculata brought important cues about the early life history of the species.…”

“…The detailed description of the first larval stage (zoea I) of R. exoculata brought important cues about the early life history of the species. The notable absence of both masticatory processes in the mandible and setation in mouthparts (which usually participate in the process of capture and manipulation of food) suggests that the R. exoculata first larval stage is a non-feeding larva (Hernandez-Avila et al 2015). Both the lack of developed feeding structures and the accumulation of triacylgycerols, wax esters and monounsaturated fatty acids in eggs of alvinocaridid species (Pond et al 1997c) support the occurrence of primary lecithotrophy in the early stage of alvino caridids (Hernandez-Avila et al 2015).…”