Bacterivory of the hydrothermal-vent-specific copepod Stygiopontius senokuchiae (Dirivultidae, Siphonostomatoida) from copepodite through adult stages

Abstract

Stygiopontius senokuchiae is a hydrothermal-vent-specific copepod species (Dirivultidae, Siphonostomatoida) and abundantly distributes near vent orifices. This species is thought to have an early juvenile planktic stage, and previous studies using bulk tissue stable-isotope and radioisotope data suggest that adults ingest chemoautotrophic microbes growing on vent chimneys. However, ontogenetic changes in their diets have not been investigated. We analysed gut contents of copepodite I to adult stages of S. senokuchiae collected from a hydrothermal-vent chimney at the Izu-Ogasawara Arc to check for the presence of bacterial cells in oral tubes and guts. We compared these results with an unidentified co-occurring calanoid and a species of Ectinosoma (Harpacticoida) and to other Siphonostomatoid copepods, namely Hatschekia labracis (Hatschekiidae), which was attached to a scarbreast tuskfin (Choerodon azurio, Labridae), and Asterocheres sp. 1 (Asterocheridae), which was attached to a spirastrellid sponge. Carbon isotope ratios of S. senokuchiae at different stages and Ectinosoma were measured to complement the nutritional insights obtained from gut-content analysis. Our results clearly showed that most S. senokuchiae individuals possessed bacteria in the oral tube or gut regardless of growth stage, whereas the coexisting Ectinosoma and calanoid did not. The carbon isotopic compositions confirmed that S. senokuchiae gains its nutrition from chemoautotrophic bacteria that use the rTCA carbon-fixation pathway. Comparisons with other Siphonostomatoida copepods suggest that Dirivultidae are specifically adapted to feed on bacteria at hydrothermal-vent chimneys, allowing their high dominance and evolutionary success in these habitats.

Highly structured populations of deep-sea copepods associated with hydrothermal vents across the Southwest Pacific, despite contrasting life history traits

“…A growing body of literature is emerging detailing dirivultid copepods as feeding predominantly on chemoautotrophs [ 8 , 34 , 40 – 42 , 96 ]. These studies elucidate two important findings, firstly that the gut contents of dirivultid copepods are mostly composed of chemoautotrophic bacteria based on lipid composition and depleted δ 13 C signatures [ 41 ], and secondly, that there is a gradient of specialisation across species in the family, where some members are found very close to the vent source (e.g., S . quadrispinosus ) and have evolved to contain high levels of hemoglobin to cope with depleted oxygen levels [ 23 , 97 ].…”

“…They have also been found in the gills of Alvinocarid shrimp [18], where they may be feeding on symbiotic bacteria. Studies suggest that this family is bacterivore, feeding on chemoautotrophic bacterial mats and films to differing degrees of discrimination [21,34,[40][41][42]51], further suggestive of the fact that these organisms are chemosynthetic obligates. In contrast, harpacticoid members of the Miraciidae, Ameiridae and Laophontidae families exist at vent environments in much lower abundance, found predominantly in ambient benthic sediments and shallow water environments [18,20,21,43,54,55].…”

Highly structured populations of copepods at risk to deep‐sea mining: Integration of genomic data with demogenetic and biophysical modelling

“…The removal of these abundant copepods from the vent environment through mining may have unprecedented consequences for the ecosystem as a whole. Being the most abundant animal where hard substrate is available, dirivultid copepods represent an unexplored but potentially important functional group in these systems, feeding predominantly on chemoautotrophic bacteria (Nomaki et al, 2023) and forming close associations with a range of megafaunal species including Rimicaris shrimp (Gollner et al, 2016), the squat lobster Shinkai crosnieri (Senokuchi et al, 2018), Bathymodiolin mussels (Gollner et al, 2016), Ifremeria and Alviniconcha snails (Gollner et al, 2016), and the vent polychaete Paralvinella sulfincola, which was hypothesized to utilize the vent copepod Stygiopontius quadrispinosus as a primary food source when densities of the copepod were high (1852 ind. per worm) (Limén et al, 2008).…”

“…The community composition, succession, functional importance, and connectivity of hydrothermal vent mega-and macrofauna have been explored since hydrothermal vents were discovered in 1977. Recently, hydrothermal vent meiofauna has gained interest due to their potentially important role in the food web (Limén et al, 2007(Limén et al, , 2008Nomaki et al, 2023), broad horizontal range of vent-endemic genera (Gollner et al, 2011(Gollner et al, , 2016, and the ability of non-vent-endemic genera to adapt to an unprecedented range of hydrothermal vent conditions (Nakasugi et al, 2021;Nomaki et al, 2019). Understanding the genetic connectivity of smaller size classes in these habitats is crucial due to their ephemeral nature and potential to create isolated populations at risk of local extinctions despite observed gene flow among populations along fast and slow spreading MORs (Beedessee et al, 2013;Breusing et al, 2015Breusing et al, , 2016Craddock et al, 1995;Gollner et al, 2011Gollner et al, , 2016Hurtado et al, 2004;Jollivet et al, 1995;Mullineaux et al, 2010;Perez et al, 2021;Teixeira et al, 2011Teixeira et al, , 2012Won et al, 2003;Yahagi et al, 2019;Yearsley et al, 2020).…”

“…The Dirivultidae (Siphonostomatoida) exist in the tens to hundreds of thousands of individuals per vent wherever basalt rock, hard-shelled megafauna assemblages, or patches of dead organisms creating landscapes of exoskeletons exist (Diaz-Recio Lorenzo et al, 2021;Gollner et al, 2010Gollner et al, , 2016. The Dirivultidae (Siphonostomatoida) contains at least 80 described species that have adapted to vent environments, dominating areas of high temperatures with high concentrations of hydrogen sulphide and low oxygen levels where they feed predominantly on chemoautotrophic bacteria (Diaz-Recio Lorenzo et al, 2021;Gollner et al, 2016;Nakasugi et al, 2021;Nomaki et al, 2019Nomaki et al, , 2023Watanabe et al, 2021). They have a lecithotrophic developmental mode and likely disperse via hydrothermal plumes, settling as vent-obligate adults.…”