hydrothermal vents; stable isotopes; taxonomy; crustaceans; life history; trophic shift
Abstract :
[en] Among hydrothermal vent species, Rimicaris exoculata is one of the most emblematic, hosting abundant and diverse ectosymbioses that provide most of its nutrition. Rimicaris exoculata co-occurs in dense aggregates with the much less abundant Rimicaris chacei in many Mid-Atlantic Ridge vent fields. This second shrimp also houses ectosymbiotic microorganisms but has a mixotrophic diet. Recent observations have suggested potential misidentifications between these species at their juvenile stages, which could have led to misinterpretations of their early-life ecology. Here, we confirm erroneous identification of the earliest stages and propose a new set of morphological characters unambiguously identifying juveniles of each species. On the basis of this reassessment, combined use of C, N and S stable isotope ratios reveals distinct ontogenic trophic niche shifts in both species, from photosynthesis-based nutrition before settlement, towards a chemosynthetic diet afterwards. Furthermore, isotopic compositions in the earliest juvenile stages suggest differences in larval histories. Each species thus exhibits specific early-life strategies that would, without our re-examination, have been interpreted as ontogenetic variations. Overall, our results provide a good illustration of the identification issues persisting in deep-sea ecosystems and the importance of integrative taxonomy in providing an accurate view of fundamental aspects of the biology and ecology of species inhabiting these environments.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Ramirez-Llodra E, et al., 2010 Deep, diverse and definitely different: unique attributes of the world's largest ecosystem. Biogeosciences 7, 2851-2899. (doi:10.5194/bg-7-2851-2010)
Sievert S, Vetriani C,. 2012 Chemoautotrophy at deep-sea vents: past, present, and future. Oceanography 25, 218-233. (doi:10.5670/oceanog.2012.21)
Vrijenhoek RC,. 2009 Cryptic species, phenotypic plasticity, and complex life histories: assessing deep-sea faunal diversity with molecular markers. Deep. Res. Part II Top. Stud. Oceanogr. 56, 1713-1723. (doi:10.1016/j.dsr2.2009.05.016)
Williams AB, Rona PA,. 1986 Two new caridean shrimps (Bresiliidae) from a hydrothermal field on the Mid-Atlantic Ridge. J. Crustac. Biol. 6, 446-462. (doi:10.1163/193724086X00299)
Martin JW, Signorovitch J, Patel H,. 1997 A new species of Rimicaris (Crustacea: Decapoda: Bresiliidae) from the Snake Pit hydrothermal vent field on the Mid-Atlantic Ridge. Proc. Biol. Soc. Washingt. 110, 399-411.
Vereshchaka AL,. 1996 A new genus and family of caridean shrimp (Crustacea: decapoda: Alvinocaridae) from North Atlantic hydrothermal vents. J. Mar. Biol. Assoc. UK 76, 951-961. (doi:10.1017/S002531540004090X)
Shank TM, Lutz RA, Vrijenhoek RC,. 1998 Molecular systematics of shrimp (Decapoda: Bresiliidae) from deep-sea hydrothermal vents. I: Enigmatic 'small orange' shrimp from the Mid-Atlantic Ridge are juvenile Rimicaris exoculata. Mol. Mar. Biol. Biotechnol. 7, 88-96.
Komai T, Segonzac M,. 2008 Taxonomic review of the hydrothermal vent shrimp genera Rimicaris Williams & Rona and Chorocaris Martin & Hessler (Crustacea: Decapoda: Caridea: Alvinocarididae). J. Shellfish Res. 27, 21-41. (doi:10.2983/0730-8000(2008)27[21:TROTHV]2.0.CO;2)
Fry B, Gest H, Hayes JM,. 1983 Sulphur isotopic compositions of deep-sea hydrothermal vent animals. Nature 306, 51-52. (doi:10.1038/306051a0)
Reid WDK, Sweeting CJ, Wigham BD, Zwirglmaier K, Hawkes JA, McGill RAR, Linse K, Polunin NVC, Thrush S,. 2013 Spatial differences in East Scotia Ridge hydrothermal vent food webs: influences of chemistry, microbiology and predation on trophodynamics. PLoS ONE 8, 1-11. (doi:10.1371/journal.pone.0065553)
Hügler M, Sievert SM,. 2011 Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Ann. Rev. Mar. Sci. 3, 261-289. (doi:10.1146/annurev-marine-120709-142712)
Minagawa M, Wada E,. 1984 Stepwise enrichment of 15 N along food chains: further evidence and the relation between δ 15 N and animal age. Geochim. Cosmochim. Acta 48, 1135-1140. (doi:10.1016/0016-7037(84)90204-7)
Jan C, et al., 2014 The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environ. Microbiol. 16, 2723-2738. (doi:10.1111/1462-2920.12406)
Petersen JM, Ramette A, Lott C, Cambon-Bonavita MA, Zbinden M, Dubilier N,. 2010 Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma-and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environ. Microbiol. 12, 2204-2218. (doi:10.1111/j.1462-2920.2009.02129.x)
Segonzac M, de Saint Laurent M, Casanova B,. 1993 L'enigme du comportement trophique des crevettes Alvinocarididae des sites hydrothermaux de la dorsale medio-atlantique. Cah. Biol. Mar. 34, 535-571. (doi:10.21411/CBM.A.B3683E29)
Van Dover CL, Fry B, Grassle JF, Humphris S, Rona PA,. 1988 Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar. Biol. 98, 209-216. (doi:10.1007/BF00391196)
Gebruk AV, Southward EC, Kennedy H, Southward AJ,. 2000 Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J. Mar. Biol. Assoc. UK 80, 485-499. (doi:10.1017/S0025315400002186)
Ponsard J, et al., 2013 Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. ISME J. 7, 96-109. (doi: 10.1038/ismej.2012.87)
Pond DW, Gebruk A, Southward EC, Southward AJ, Fallick AE, Bell MV, Sargent JR,. 2000 Unusual fatty acid composition of storage lipids in the bresilioid shrimp Rimicaris exoculata couples the photic zone with MAR hydrothermal vent sites. Mar. Ecol. Prog. Ser. 198, 171-179. (doi: 10.3354/meps198171)
Dixon DR, Dixon LRJ, Pond DW,. 1998 Recent advances in our understanding of the life history of bresilid vent shrimps on the MAR. Cah. Biol. Mar. 39, 383-386. (doi:10.21411/CBM.A.7A5BA34)
Hernández-Ávila I,. 2016 Larval dispersal and life cycle in deep-water hydrothermal vents: the case of Rimicaris exoculata and related species.. PhD thesis, Université de Bretagne occidentale, Brest, France. See https://tel.archives-ouvertes.fr/tel-01612011.
Apremont V, Cambon-Bonavita M-A, Cueff-Gauchard V, François D, Pradillon F, Corbari L, Zbinden M, Kuo C-H,. 2018 Gill chamber and gut microbial communities of the hydrothermal shrimp Rimicaris chacei Williams and Rona 1986: a possible symbiosis. PLoS ONE 13, e0206084. (doi:10.1371/journal.pone.0206084)
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R,. 1994 DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299. (doi:10.1371/journal.pone.0013102)
Coplen TB,. 2011 Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25, 2538-2560. (doi:10.1002/rcm.5129)
Jackson AL, Inger R, Parnell AC, Bearhop S,. 2011 Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol. 80, 595-602. (doi:10.1111/j.1365-2656.2011.01806.x)
Methou, et al.,. In preparation.
Waite DW, et al., 2017 Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Front. Microbiol. 8, 682. (doi:10.3389/fmicb.2017.00682)
Desbruyères D, Almeida A, Biscoito M, Comtet T, Khripounoff A, Le Bris N, Sarradin PM, Segonzac M,. 2000 A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: dispersal vs. environmental controls. Hydrobiologia 440, 201-216. (doi:10.1023/A:1004175211848)
Rybakova E, Galkin S,. 2015 Hydrothermal assemblages associated with different foundation species on the East Pacific Rise and Mid-Atlantic Ridge, with a special focus on mytilids. Mar. Ecol. 36 (S1), 45-61. (doi:10.1111/maec.12262)
Crépeau V, Cambon Bonavita M-A, Lesongeur F, Randrianalivelo H, Sarradin P-M, Sarrazin J, Godfroy A,. 2011 Diversity and function in microbial mats from the Lucky Strike hydrothermal vent field. FEMS Microbiol. Ecol. 76, 524-540. (doi:10.1111/j.1574-6941.2011.01070.x)
Fouquet Y, et al., 2010 Geodiversity of hydrothermal processes along the Mid-Atlantic Ridge and ultramafic-hosted mineralization: a new type of oceanic Cu-Zn-Co-Au volcanogenic massive sulfide deposit. In Diversity of hydrothermal systems on slow spreading ocean ridges, vol. 188 (eds PA Rona, CW Devey, J Dyment, BJ Murton,), pp. 321-367. Washington, DC: American Geophysical Union.
Methou P, Hernández-Ávila I, Aube J, Cueff-Gauchard V, Gayet N, Amand L, Shillito B, Pradillon F, Cambon-Bonavita M-A,. 2019 Is it first the egg or the shrimp?-Diversity and variation in microbial communities colonizing broods of the vent shrimp Rimicaris exoculata during embryonic development. Front. Microbiol. 10, 1-19. (doi:10.3389/fmicb.2019.00808)
Riekenberg PM, Carney RS, Fry B,. 2016 Trophic plasticity of the methanotrophic mussel Bathymodiolus childressi in the Gulf of Mexico. Mar. Ecol. Prog. Ser. 547, 91-106. (doi:10.3354/meps11645)
Lee RW, Childress JJ,. 1994 Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl. Environ. Microbiol. 60, 1852-1858. (doi:10.1128/AEM.60.6.1852-1858.1994)
Nakagawa S, Takaki Y, Shimamura S, Reysenbach A, Takai K,. 2007 Deep-sea vent epsilonproteobacterial genomes provide insight into emergence of pathogens. Proc. Natl Acad. Sci. USA 104, 12 146-12 150. (doi:10.1073/pnas.0700687104)
Sievert SM, et al., 2008 Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol. 74, 1145-1156. (doi:10.1128/aem.01844-07)
Stokke R, Dahle H, Roalkvam I, Wissuwa J, Daae FL, Tooming-Klunderud A, Thorseth IH, Pedersen RB, Steen IH,. 2015 Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm. Environ. Microbiol. 17, 4063-4077. (doi:10.1111/1462-2920.12970)
Szafranski KM, Deschamps P, Cunha MR, Gaudron SM, Duperron S,. 2015 Colonization of plant substrates at hydrothermal vents and cold seeps in the northeast Atlantic and Mediterranean and occurrence of symbiont-related bacteria. Front. Microbiol. 6, 1-14. (doi:10.3389/fmicb.2015.00162)
Flaherty EA, Ben-David M,. 2010 Overlap and partitioning of the ecological and isotopic niches. Oikos 119, 1409-1416. (doi:10.1111/j.1600-0706.2010.18259.x)
Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL,. 2007 A niche for isotope ecology. Front. Ecol. Environ. 5, 429-436. (doi:10.1890/060150.01)
Pizzochero AC, Michel LN, Chenery SR, McCarthy ID, Vianna M, Malm O, Lepoint G, Das K, Dorneles PR,. 2017 Use of multielement stable isotope ratios to investigate ontogenetic movements of Micropogonias furnieri in a tropical Brazilian estuary. Can. J. Fish. Aquat. Sci. 373, 1-10. (doi:10.1139/cjfas-2017-0148)
Fang J, Uhle M, Billmark K, Bartlett DH, Kato C,. 2006 Fractionation of carbon isotopes in biosynthesis of fatty acids by a piezophilic bacterium Moritella japonica strain DSK1. Geochim. Cosmochim. Acta 70, 1753-1760. (doi:10.1016/j.gca.2005.12.011)
Nègre-Sadargues G, Castillo R, Segonzac M,. 2000 Carotenoid pigments and trophic behaviour of deep-sea shrimps (Crustacea, Decapoda, Alvinocarididae) from a hydrothermal area of the Mid-Atlantic Ridge. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 127, 293-300. (doi:10.1016/S1095-6433(00)00258-0)
Van Dover CL,. 2002 Trophic relationships among invertebrates at the Kairei hydrothermal vent field (Central Indian Ridge). Mar. Biol. 141, 761-772. (doi:10.1007/s00227-002-0865-y)
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. (doi:10.3354/meps07270)
Trask JL, Van Dover CL,. 1999 Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol. Oceanogr. 44, 334-343. (doi:10.4319/lo.1999.44.2.0334)
Laming SR, Gaudron SM, Duperron S,. 2018 Lifecycle ecology of deep-sea chemosymbiotic mussels: a review. Front. Mar. Sci. 5, 582. (doi: 10.3389/fmars.2018.00282)
Nomaki H, et al., 2019 Nutritional sources of meio-and macrofauna at hydrothermal vents and adjacent areas: natural-abundance radiocarbon and stable isotope analyses. Mar. Ecol. Prog. Ser. 622, 49-65. (doi:10.3354/meps13053)
Herring PJ, Dixon DR,. 1998 Extensive deep-sea dispersal of postlarval shrimp from a hydrothermal vent. Deep. Res. Part I Oceanogr. Res. Pap. 45, 2105-2118. (doi:10.1016/S0967-0637(98)00050-8)
Adams DK, Arellano SM, Govenar B,. 2012 Larval dispersal: vent life in the water column. Oceanography 25, 256-268. (doi:10.5670/oceanog.2012.24)
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. UK 80, 739-740. (doi:10.1017/S0025315400002605)
Glover AG, Wiklund H, Chen C, Thomas G,. 2018 Managing a sustainable deep-sea 'blue economy' requires knowledge of what actually lives there. Elife 7, e41319. (doi:10.7554/eLife.41319)