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Contrasting reproductive biology of two hydrothermal gastropods from the Mid-Atlantic Ridge: implications for resilience of vent communities

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Abstract

The recovery of populations and their ability to recolonise a disturbed habitat is mainly dependent on their reproductive biology (e.g., fecundity, frequency of reproduction, and time to maturity) and recruitment success. To assess recolonisation processes and connectivity of vent communities, and infer their resilience to natural and anthropogenic disturbances, we studied the life-history traits of two dominant species of vent gastropods from the northern Mid-Atlantic Ridge: Protolira valvatoides and Pseudorimula midatlantica. Gonad morphology, gametogenesis, and reproductive outputs related to shell length were described using histological analyses, and population structure was assessed from individuals’ size–frequency distributions. Samples were collected at different locations of the Montségur and Eiffel Tower edifices (Lucky Strike vent field) in April 2015, July 2017, and August 2018 to inform on spatial and temporal variations of their reproductive outputs and demography. All stages of oocyte development were found in the gonads of both species, suggesting a continuous gametogenesis and asynchronous reproduction. However, the two species showed contrasting reproductive strategies. Indeed, while P. midatlantica is gonochoric with a fecundity of up to 327 mature oocytes, P. valvatoides is hermaphrodite with an extremely low fecundity including a maximum of eight vitellogenic oocytes. Maximum oocyte size was 176 µm for P. midatlantica and 272 µm for P. valvatoides. We infer from previous knowledge and our results that both species exhibit a lecithotrophic development of larvae. There was no evidence of temporal variability of reproductive traits, but environmental conditions seem to affect gametogenetic maturity and oocyte size of P. midatlantica limpets. Variations in population structure at the edifice scale suggest habitat selection of individuals related to biotic and abiotic factors.

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Availability of data and material

Data are available from the authors on reasonable request. The data used in this study are available online (https://doi.org/10.17882/71838).

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Acknowledgements

We would like to thank the captains and crews of the oceanographic cruises Momarsat 2015, 2017, and 2018 aboard the vessels N/O Pourquoi pas? and L’Atalante, as well as the ROV Victor6000 team. We are particularly grateful to Pierre-Marie Sarradin and Mathilde Cannat, chief scientists of the cruises who greatly supported our sampling program. We are also sincerely thankful to Sandra Fuchs for sample collection and Julie Tourolle for providing the map as well as all the technicians of the deep sea Ifremer lab. Many thanks to all members of the histological lab of the Norwegian Veterinary Institute and especially to Randi Terland who provided valuable help and assistance with histological processes. We are also grateful to Lucile Durand for the help on imagery acquisition and Florence Pradillon for proofreading the last version of this manuscript. This research was supported by the European H2020 MERCES (Project ID 689518) and by the eCOREF project funded by Equinor (Norway). Julien Marticorena PhD project was funded by Ifremer and Equinor. This project is part of the EMSO-Azores (https://www.emso-fr.org) regional node and EMSO ERIC Research Infrastructure (https://emso.eu/). ERLL was supported by the European H2020 MERCES (Project ID 689518).

Funding

This research was supported by the European H2020 MERCES (Project ID 689,518) and by the eCOREF project funded by Equinor (Norway). Julien Marticorena PhD project was funded by Ifremer and Equinor. This project is part of the EMSO-Azores (https://www.emso-fr.org) regional node and EMSO ERIC Research Infrastructure (https://emso.eu/). ERLL was supported by the European H2020 MERCES (Project ID 689,518).

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Contributions

JM, MM, JS, and ERLL conceived the ideas and designed the methodology. JM, MM, and JS collected the data, and JM processed and analysed the data. JM wrote the first draft of the manuscript and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to J. Marticorena.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for sampling were followed in the current study.

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Communicated by M.G. Chapman.

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227_2020_3721_MOESM1_ESM.png

Supplementary file1 Fig.S1 Mean oocyte size-frequency histograms (mean ± SD) of pooled individuals of Protolira valvatoides for each sampling period. Colors: Grey bars represent previtellogenic oocytes and yellow bars represent vitellogenic oocytes. Abbreviations: N, number of individuals; n, number of oocytes measured. (PNG 316 kb)

227_2020_3721_MOESM2_ESM.png

Supplementary file2 Fig.S2 Mean oocyte size-frequency histograms (mean ± SD) of pooled individuals of Pseudorimula midatlantica for each sampling period. Colors: Grey bars represent previtellogenic oocytes and yellow bars represent vitellogenic oocytes. Abbreviations: N, number of individuals; n, number of oocytes measured. (PNG 326 kb)

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Marticorena, J., Matabos, M., Sarrazin, J. et al. Contrasting reproductive biology of two hydrothermal gastropods from the Mid-Atlantic Ridge: implications for resilience of vent communities. Mar Biol 167, 109 (2020). https://doi.org/10.1007/s00227-020-03721-x

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