Abstract
Alvinocaridid shrimps are endemic and globally widespread in chemosynthetic ecosystems such as hydrothermal vents and hydrocarbon seeps. Though the biology of Atlantic alvinocaridid species have received considerable attention, little is known about their Pacific relatives. Here we described population structures and reproductive biology of three Pacific alvinocaridid species—Shinkaicaris leurokolos, Opaepele loihi, Alvinocaris longirostris—with notes on a fourth species—A. dissimilis—from several chemosynthetic ecosystems around Japan and compared their size frequency distributions and reproductive outputs. We showed that population demographics differ among these species, including a significantly larger proportion of juveniles in O. loihi and spatial variation of sex ratio in S. leurokolos, but all shared sex ratios biased toward females. The three shrimp species were characterized by relatively small sizes at onset of maturity, although this varied among sites for A. longirostris. Overall, size-specific fecundities and egg volumes of A. longirostris, O. loihi and S. leurokolos were in a similar range to Atlantic alvinocaridids. In addition, we performed egg incubation experiments of O. loihi under different temperature conditions to characterize thermal physiology during its brooding period. This confirmed a strong influence of temperature on both brooding duration and hatching rate, with a thermal preference that differs from previously published data for A. longirostris and S. leurokolos. Finally, our results indicated that these alvinocaridid species from the northwestern Pacific likely differ in reproductive timing, either through distinct brooding durations and/or distinct brooding periodicity, although further investigations are required to confirm these patterns.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All genetic sequences have been deposited in GenBank under accession numbers OP482454 to OP482487. Dataset on population and reproductive traits are available on the figshare repository: https://doi.org/10.6084/m9.figshare.21345183.
References
Anger K, Moreria GS (1998) Morphometric and reproductive traits of tropical caridean shrimps. J Crustac Biol 18:823–838. https://doi.org/10.2307/1549156
Beedessee G, Watanabe H, Ogura T, Nemoto S, Yahagi T, Nakagawa S, Nakamura K, Takai K, Koonjul M, Marie DEP (2013) High connectivity of animal populations in deep-sea hydrothermal vent fields in the central indian ridge relevant to its geological setting. PLoS ONE 8:e81570. https://doi.org/10.1371/journal.pone.0081570
Brillon S, Lambert Y, Dodson J (2005) Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions. Mar Biol 147:895–911. https://doi.org/10.1007/s00227-005-1633-6
Brunner O, Chen C, Giguère T, Kawagucci S, Tunnicliffe V, Kayama H, Satoshi W (2022) Species assemblage networks identify regional connectivity pathways among hydrothermal vents in the Northwest Pacific. Ecol Evol. https://doi.org/10.1002/ece3.9612
Copley JTP, Young CM (2006) Seasonality and zonation in the reproductive biology and population structure of the shrimp Alvinocaris stactophila (Caridea: Alvinocarididae) at a Louisiana Slope cold seep. Mar Ecol Prog Ser 315:199–209. https://doi.org/10.3354/meps315199
Copley JTP, Jorgensen PBK, Sohn RA (2007) Assessment of decadal-scale ecological change at a deep Mid-Atlantic hydrothermal vent and reproductive time-series in the shrimp Rimicaris exoculata. J Mar Biol Assoc 87:859–867. https://doi.org/10.1017/S0025315407056512
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466. https://doi.org/10.1146/annurev.marine.010908.163757
Danovaro R, Fanelli E, Aguzzi J, Billett D, Carugati L, Corinaldesi C, Dell’Anno A, Gjerde K, Jamieson AJ, Kark S, McClain C, Levin L, Levin N, Ramirez-Llodra E, Ruhl H, Smith CR, Snelgrove PVR, Thomsen L, Van Dover CL, Yasuhara M (2020) Ecological variables for developing a global deep-ocean monitoring and conservation strategy. Nat Ecol Evol 4:181–192. https://doi.org/10.1038/s41559-019-1091-z
García-Guerrero MU (2010) Effect of temperature on consumption rate of main yolk components during embryo development of the prawn Macrobrachium americanum (Crustacea: Decapoda: Palaemonidae). J World Aquac Soc 41:84–92. https://doi.org/10.1111/j.1749-7345.2009.00336.x
Gaudron SM, Lefebvre S, Marques GM (2021) Inferring functional traits in a deep—sea wood—boring bivalve using dynamic energy budget theory. Sci Rep. https://doi.org/10.1038/s41598-021-02243-w
Gollner S, Colaço A, Gebruk A, Halpin PN, Higgs N, Menini E, Mestre NC, Qian PY, Sarrazin J, Szafranski K, Van Dover CL (2021) Application of scientific criteria for identifying hydrothermal ecosystems in need of protection. Mar Policy 132:104641. https://doi.org/10.1016/j.marpol.2021.104641
Hernández-Ávila I, Cambon-Bonavita MA, Pradillon F (2015) Morphology of first zoeal stage of four genera of alvinocaridid shrimps from hydrothermal vents and cold seeps: Implications for ecology, larval biology and phylogeny. PLoS ONE 10:1–27. https://doi.org/10.1371/journal.pone.0144657
Hernández-Ávila I, Cambon-Bonavita M-A, Sarrazin J, Pradillon F (2022) Population structure and reproduction of the alvinocaridid shrimp Rimicaris exoculata on the Mid-Atlantic Ridge: variations between habitats and vent fields. Deep Sea Res Part I Oceanogr Res Pap 186:3–5. https://doi.org/10.1016/j.dsr.2022.103827
Husson B, Sarradin PM, Zeppilli D, Sarrazin J (2017) Picturing thermal niches and biomass of hydrothermal vent species. Deep Res Part II Top Stud Oceanogr 137:6–25. https://doi.org/10.1016/j.dsr2.2016.05.028
Jollivet D, Empis A, Baker MC, Hourdez S, Comtet T, Desbruyères D, Tyler PA (2000) Reproductive biology, sexual dimorphism, and population structure of the deep sea hydrothermal vent scale-worm, Branchipolynoe seepensis (Polychaeta: Polynoidae ). J Mar Biol Assoc United Kingdom 80:55–68. https://doi.org/10.1017/S0025315499001563
Ke Z, Li R, Chen Y, Chen D, Chen Z, Lian X, Tan Y (2022) A preliminary study of macrofaunal communities and their carbon and nitrogen stable isotopes in the Haima cold seeps, South China Sea. Deep Res Part I Oceanogr Res Pap 184:103774. https://doi.org/10.1016/j.dsr.2022.103774
Kelly NE, Metaxas A (2007) Population structure of two deep-sea hydrothermal vent gastropods from the Juan de Fuca Ridge, NE Pacific. Mar Biol 153:457–471. https://doi.org/10.1007/s00227-007-0828-4
Komai T, Segonzac M (2005) A revision of the genus Alvinocaris Williams and Chace (Crustacea: Decapoda: Caridea: Alvinocarididae), with descriptions of a new genus and a new species of Alvinocaris. J Nat Hist 39:1111–1175. https://doi.org/10.1080/00222930400002499
Komai T, Tsuchida S (2015) New records of Alvinocarididae (Crustacea: Decapoda: Caridea) from the southwestern Pacific hydrothermal vents, with descriptions of one new genus and three new species. J Nat Hist. https://doi.org/10.1080/00222933.2015.1006702
Li X (2015) Report on two deep-water caridean shrimp species (Crustacea: Decapoda: Caridea: Alvinocarididae, Acanthephyridae) from the northeastern South China Sea. Zootaxa 3911:130–138. https://doi.org/10.11646/zootaxa.3911.1.8
Lunina AA, Vereshchaka AL (2014) Distribution of hydrothermal alvinocaridid shrimps: effect of geomorphology and specialization to extreme biotopes. PLoS ONE. https://doi.org/10.1371/journal.pone.0092802
Macdonald P, Du J (2012) Mixdist: finite mixture distribution models.
Marsh L, Copley JT, Tyler PA, Thatje S (2015) In hot and cold water: differential life-history traits are key to success in contrasting thermal deep-sea environments. J Anim Ecol 84:898–913. https://doi.org/10.1111/1365-2656.12337
Methou P, Michel LN, Segonzac M, Cambon-Bonavita M-A, Pradillon F (2020) Integrative taxonomy revisits the ontogeny and trophic niches of Rimicaris vent shrimps. R Soc Open Sci 7:200837. https://doi.org/10.1098/rsos.200837
Methou P, Hernández-Ávila I, Cathalot C, Cambon-Bonavita M-A, Pradillon F (2022a) Population structure and environmental niches of Rimicaris shrimps from the Mid-Atlantic Ridge. Mar Ecol Prog Ser 684:1–20. https://doi.org/10.3354/meps13986
Methou P, Chen C, Kayama H, Cambon M-A, Pradillon F (2022b) Reproduction in deep-sea vent shrimps is influenced by diet, with rhythms apparently unlinked to surface production. Ecol Evol. https://doi.org/10.1002/ece3.9076
Methou P (2019) Lifecycles of two hydrothermal vent shrimps from the Mid-Atlantic Ridge: Rimicaris exoculata and Rimicaris chacei
Miller KA, Thompson KF, Johnston P, Santillo D (2018) An overview of seabed mining including the current state of development, environmental impacts, and knowledge gaps. Front Mar Sci. https://doi.org/10.3389/fmars.2017.00418
Mullineaux LS, Metaxas A, Beaulieu SE, Bright M, Gollner S, Grupe BM, Herrera S, Kellner JB, Levin LA, Mitarai S, Neubert MG, Thurnherr AM, Tunnicliffe V, Watanabe HK, Won YJ (2018) Exploring the ecology of deep-sea hydrothermal vents in a metacommunity framework. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00049
Nakajima R, Yamakita T, Watanabe H, Fujikura K, Tanaka K, Yamamoto H, Shirayama Y (2014) Species richness and community structure of benthic macrofauna and megafauna in the deep-sea chemosynthetic ecosystems around the Japanese archipelago: an attempt to identify priority areas for conservation. Divers Distrib 20:1160–1172. https://doi.org/10.1111/ddi.12204
Nye V, Copley JTP, Tyler PA (2013) Spatial variation in the population structure and reproductive biology of Rimicaris hybisae (Caridea: Alvinocarididae) at Hydrothermal Vents on the Mid-Cayman Spreading Centre. PLoS ONE. https://doi.org/10.1371/journal.pone.0060319
Pereira OS, Shimabukuro M, Bernardino AF, Gomes Sumida PY (2020) Molecular affinity of Southwest Atlantic Alvinocaris muricola with Atlantic Equatorial Belt populations. Deep Res Part I Oceanogr Res Pap. https://doi.org/10.1016/j.dsr.2020.103343
Pond DW, Dixon DR, Bell MV, Fallick AE, Sargent JR, David W, Sargentl JR (1997) Occurrence of 16:2(n-4) and 18:2(n-4) fatty acids in the lipids of the hydrothermal vent shrimps Rimicaris exoculata and Alvinocaris markensis: nutritional nutritional and trophic implications. Mar Ecol Prog Ser 156:167–174. https://doi.org/10.3354/meps156167
Pradillon F, Shillito B, Young CM, Gaill F (2001) Developmental arrest in vent worm embryos. Nature 413:698–699. https://doi.org/10.1038/35099674
R Core Team (2020) R: A language and environment for statistical computing. https://www.r-project.org
Ramirez-Llodra E, Segonzac M (2006) Reproductive biology of Alvinocaris muricola (Decapoda: Caridea: Alvinocarididae) from cold seeps in the Congo Basin. J Mar Biol Assoc United Kingdom 86:1347. https://doi.org/10.1017/S0025315406014378
Ramirez-Llodra E, Tyler PA, Copley JTP (2000) Reproductive biology of three caridean shrimp, Rimicaris exoculata, Chorocaris chacei and Mirocaris fortunata. J Mar Biol Assoc United Kingdom 80:473–484. https://doi.org/10.1017/S0025315400002174
Stevens CJ, Limén H, Pond DW, Gélinas Y, Juniper SK (2008) Ontogenetic shifts in the trophic ecology of two alvinocaridid shrimp species at hydrothermal vents on the Mariana Arc, western Pacific Ocean. Mar Ecol Prog Ser 356:225–237. https://doi.org/10.3354/meps07270
Teixeira S, Serrão EA, Arnaud-Haond S (2012) Panmixia in a fragmented and unstable environment: the hydrothermal shrimp Rimicaris exoculata disperses extensively along the Mid-Atlantic ridge. PLoS ONE 7:1–10. https://doi.org/10.1371/journal.pone.0038521
Teixeira S, Olu K, Decker C, Cunha RL, Fuchs S, Hourdez S, Serrão EA, Arnaud-Haond S (2013) High connectivity across the fragmented chemosynthetic ecosystems of the deep Atlantic Equatorial Belt: efficient dispersal mechanisms or questionable endemism? Mol Ecol 22:4663–4680. https://doi.org/10.1111/mec.12419
Thaler AD, Plouviez S, Saleu W, Alei F, Jacobson A, Boyle EA, Schultz TF, Carlsson J, Van Dover CL (2014) Comparative population structure of two deep-sea hydrothermal-vent- associated decapods (Chorocaris sp. 2 and Munidopsis lauensis) from southwestern Pacific back-arc basins. PLoS ONE 9:1–13. https://doi.org/10.1371/journal.pone.0101345
Tong LJ, Moss GA, Pickering TD, Paewai MP (2000) Temperature effects on embryo and early larval development of the spiny lobster Jasus edwardsii, and description of a method to predict larval hatch times. Mar Freshw Res 51:243–248. https://doi.org/10.1071/MF99049
Tyler PA, Dixon DR (2000) Temperature/pressure tolerance of the first larval stage of Mirocaris fortunata from Lucky Strike hydrothermal vent field. J Mar Biol Assoc United Kingdom 80:739–740. https://doi.org/10.1017/S0025315400002605
Van Dover CL (2019) Inactive sulfide ecosystems in the deep sea: a review. Front Mar Sci 6:1–40. https://doi.org/10.3389/fmars.2019.00461
Van Dover CL, Trask JL (2000) Diversity at deep-sea hydrothermal vent and intertidal mussel beds. Mar Ecol Prog Ser 195:169–178. https://doi.org/10.3354/meps195169
Van Audenhaege L, Fariñas-Bermejo A, Schultz T, Lee Van Dover C (2019) An environmental baseline for food webs at deep-sea hydrothermal vents in Manus Basin (Papua New Guinea). Deep Res Part I Oceanogr Res Pap 148:88–99. https://doi.org/10.1016/j.dsr.2019.04.018
Van Dover CL, Arnaud-Haond S, Gianni M, Helmreich S, Huber JA, Jaeckel AL, Metaxas A, Pendleton LH, Petersen S, Ramirez-Llodra E, Steinberg PE, Tunnicliffe V, Yamamoto H (2018) Scientific rationale and international obligations for protection of active hydrothermal vent ecosystems from deep-sea mining. Mar Policy 90:20–28. https://doi.org/10.1016/j.marpol.2018.01.020
Vrijenhoek RC (2010) Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Mol Ecol 19:4391–4411. https://doi.org/10.1111/j.1365-294X.2010.04789.x
Watanabe H, Yahagi T, Nagai Y, Seo M, Kojima S, Ishibashi J, Yamamoto H, Fujikura K, Mitarai S, Toyofuku T (2016) Different thermal preferences for brooding and larval dispersal of two neighboring shrimps in deep-sea hydrothermal vent fields. Mar Ecol 37:1282–1289. https://doi.org/10.1111/maec.12318
Watanabe HK, Shigeno S, Fujikura K, Matsui T, Kato S, Yamamoto H (2019) Faunal composition of deep-sea hydrothermal vent fields on the Izu–Bonin–Mariana Arc, northwestern Pacific. Deep Res Part I Oceanogr Res Pap 149:103050. https://doi.org/10.1016/j.dsr.2019.05.010
Watanabe HK, Chen C, Kojima S, Kato S, Yamamoto H (2020) Population connectivity of the crab Gandalfus yunohana from deep-sea hydrothermal vents in the northwestern Pacific. J Crustac Biol. https://doi.org/10.1093/jcbiol/ruaa045
Yahagi T, Watanabe H, Ishibashi JI, Kojima S (2015) Genetic population structure of four hydrothermal vent shrimp species (Alvinocarididae) in the Okinawa Trough, Northwest Pacific. Mar Ecol Prog Ser 529:159–169. https://doi.org/10.3354/meps11267
Zbinden M, Cambon-Bonavita M (2020) Biology and ecology of Rimicaris exoculata, a symbiotic shrimp from deep-sea hydrothermal vents. Mar Ecol Prog Ser 652:187–222. https://doi.org/10.3354/meps13467
Zhou Y, Chen C, Zhang D, Wang Y, Kayama H, Jin W, Dass S, Ruiyan B, Han Y, Sun D, Xu P, Lu B, Zhai H, Han X, Tao C, Qiu Z, Sun Y, Liu Z, Qiu W, Wang C (2022) Delineating biogeographic regions in Indian Ocean deep-sea vents and implications for conservation. Divers Distrib. https://doi.org/10.1111/ddi.13535
Acknowledgements
We thank the captains and crews of numerous research cruises conducted on-board R/V Kairei (KR15-16, KR15-17, KR16-16), R/V Natsushima (NT05-05, NT10-17, NT13-22, NT15-13), R/V Kaiyo (KY14-01), R/V Yokosuka (YK17-17, YK19-10, YK22-05), and R/V Shinsei-Maru (KS-21-20, KS-22-2). We also thank the pilots and the operation team of the HOV Shinkai 6500 and of the ROVs Kaiko, Hyper-Dolphin, and KM-ROV during these research cruises. We gratefully acknowledge the chief scientists of the relevant expeditions: Shinsuke Kawagucci (JAMSTEC; NT10-17, KR15-16), Hironori Komatsu (National Museum of Nature and Science, Tsukuba; KS-22-2), Hiroko Makita (JAMSTEC and Tokyo University of Marine Science and Technology; YK17-17), Junichi Miyazaki (JAMSTEC; KR16-16), Tatsuo Nozaki (JAMSTEC; KS-21-20), Ken Takai (JAMSTEC; NT15-13, KY14-01, YK19-10, YK22-05), Hiroyuki Yamamoto (JAMSTEC; NT13-22, KR15-17).
Funding
PM was supported by a JAMSTEC Young Research Fellow fellowship. CC and HKW were supported by a Grant-in-Aid for Scientific Research (KAKENHI) from the Japan Society for the Promotion of Science (JSPS), grant code 18K06401.
Author information
Authors and Affiliations
Contributions
PM collected specimens from the KS-21-20 expedition, carried out the identification of shrimps, including molecular barcoding, and measurement of specimens from all sampling cruises except NT13-22 and KY14-01, lead the data analysis, participated in the conception and design of the study and drafted the original manuscript; VN conducted identification, measurements and data analysis of specimens collected during NT13-22 and KY14-01 cruises, participated in the design of the study and critically revised the manuscript; JC participated in the design of the study and critically revised the manuscript. HKW carried out the collection of specimens from YK19-10, designed and conducted in vitro egg incubation experiment and its analysis, and critically revised the manuscript. YN conducted the in vitro egg incubation experiment, and critically revised the manuscript. CC collected and sorted materials from most of the relevant expeditions, assisted in drafting the original manuscript, and coordinated the study. All authors gave final approval for submission and publication of the manuscript in its current form.
Corresponding author
Ethics declarations
Conflict of interest
We have no conflict of interest.
Ethics approval
Faunal collections were conducted in Japanese exclusive economic zone by Japanese government research vessels. Research animals were invertebrate caridean shrimps and no live experiments with animals were conducted in this study.
Additional information
Responsible Editor: H.-J. Hoving.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Methou, P., Nye, V., Copley, J.T. et al. Life-history traits of alvinocaridid shrimps inhabiting chemosynthetic ecosystems around Japan. Mar Biol 170, 75 (2023). https://doi.org/10.1007/s00227-023-04221-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-023-04221-4