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Dynamics of the Upogebia pusilla–Gyge branchialis marine host–parasite system

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Abstract

The influence of burrowing invertebrates on the functioning of soft-bottom ecosystems is tightly dependent on their physiological state, which may itself be strongly affected by parasite infestation. However, the dynamics, prevalence and physiological consequences of parasitism remain poorly known in many species, such as sediment-dwelling crustaceans. During the present study, we investigated the effects of the ectoparasite (bopyrid) isopod Gyge branchialis on the fitness of the gebiidean mud shrimp Upogebia pusilla. A spatial survey conducted in June 2013 at 10 stations scattered across intertidal seagrass meadows of Arcachon Bay (44°40′N, 1°10′W) showed that on average 16 % of mud shrimp were infested by G. branchialis. Moreover, a temporal survey carried out at one of these stations over the year 2014 revealed that prevalence remained relatively high throughout the year, ranging from 10 to 33 %. This interaction has various physiological consequences for U. pusilla. In particular, infested mud shrimp consistently exhibited a significant deficit in total length and individual dry weight as compared with non-infested specimens. Moreover, 89 % of infested males were feminized (i.e., developed female secondary sexual characters), whereas infested females were never ovigerous. Our results demonstrate that G. branchialis strongly impair U. pusilla fitness including its ability to reproduce. Accordingly, through their (1) potential impact on mud shrimp abundances and (2) alteration of their physiological state, high bopyrid infestation could profoundly alter the bioturbation activity of mud shrimp populations and overall their influence on the functioning of soft-bottom ecosystems in Arcachon Bay.

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References

  • Astall CM, Taylor AC, Atkinson RJA (1996) Notes on some branchial isopods parasitic on Upogebiid mud-shrimps (Decapoda: Thalassinidea). J Mar Biol Assoc UK 76:821–824. doi:10.1017/S0025315400031489

    Article  Google Scholar 

  • Astall CM, Taylor AC, Atkinson RJA (1997) Behavioural and physiological implications of a burrow-dwelling lifestyle for two species of Upogebiid mud-shrimp (Crustacea: Thalassinidea). Estuar Coast Shelf Sci. doi:10.1006/ecss.1996.0207

    Google Scholar 

  • Auby I, Labourg P-J (1996) Seasonal dynamics of Zostera noltii hornem. In the bay of Arcachon (France). J Sea Res 35:269–277. doi:10.1016/S1385-1101(96)90754-6

    Article  Google Scholar 

  • Auby I, Bost CA, Budzinski H et al (2011) Régression des herbiers de zostères dans le Bassin d’Arcachon: état des lieux et recherche des causes Régression des herbiers de zostères dans le Bassin d’Arcachon: état des lieux et recherche des causes. IFREMER. http://archimer.ifremer.fr/doc/00054/16507/

  • Bhattacharya CG (1967) A simple method of resolution of a distribution into gaussian components. Biometrics 23:115–135. doi:10.2307/2528285

    Article  CAS  Google Scholar 

  • Bonnier J (1900) Contribution a l’étude des Épicarides, les Bopyridae. Detached from Travaux de la station zoologique de Wimereux, T.VIII. s.n., Paris

  • Bourdon R (1968) Les Bopyridae de mers europeenees. Muséum national d’histoire naturelle, Paris

    Google Scholar 

  • Campos E, de Campos AR, Manriquez I (2009) Intertidal thalassinidean shrimps (Thalassinidea, Callianassidae and Upogebiidae) of the west coast of Baja California, Mexico: annotated checklist, key for identification, and symbionts. Crustaceana 82:1249–1263. doi:10.1163/001121609X12481627024454

    Article  Google Scholar 

  • D’Andrea AF, DeWitt TH (2009) Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: Density-dependent effects. Limnol Oceanogr 54:1911–1932. doi:10.4319/lo.2009.54.6.1911

    Article  Google Scholar 

  • De Montaudouin X, Wegeberg AM, Jensen KT, Sauriau PG (1998) Infection characteristics of Himasthla elongata cercariae in cockles as a function of water current. Dis Aquat Organ 34:63–70. doi:10.3354/dao034063

    Article  Google Scholar 

  • Dumbauld BR, Holden DL, Langness OP (2008) Do sturgeon limit burrowing shrimp populations in Pacific Northwest Estuaries? Environ Biol Fishes 83:283–296. doi:10.1007/s10641-008-9333-y

    Article  Google Scholar 

  • Dumbauld BR, Chapman JW, Torchin ME, Kuris AM (2011) Is the collapse of Mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)? Estuaries Coasts 34:336–350. doi:10.1007/s12237-010-9316-z

    Article  Google Scholar 

  • Dworschak PC (1987) The biology of Upogebia pusilla (Petagna) (Decapoda, Thalassinidea) II. Environments and zonation. Mar Ecol 8:337–358. doi:10.1111/j.1439-0485.1987.tb00193.x

    Article  Google Scholar 

  • Dworschak PC (1988) The biology of Upogebia pusilla (PETAGNA) (Decapoda, Thalassinidea) III. Growth and production. Mar Ecol 9:51–77. doi:10.1111/j.1439-0485.1988.tb00198.x

    Article  Google Scholar 

  • Ford AT (2008) Can you feminise a crustacean? Aquat Toxicol 88:316–321. doi:10.1016/j.aquatox.2008.04.013

    Article  CAS  Google Scholar 

  • Gayanilo FCJ, Sparre P, Pauly D (2005) FAO-ICLARM stock assessment tools II (FiSAT II). Revised version. FAO, Rome

    Google Scholar 

  • Griffen B (2009) Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer. Mar Ecol Prog Ser 391:73–83. doi:10.3354/meps08228

    Article  Google Scholar 

  • Hanekom N, Erasmus T (1988) Variations in size compositions of populations of Upogebia africana (Ortmann) (Decapoda, Crustacea) within the Swartkops estuary and possible influencing factors. South Afr J Zool 23:259–265. doi:10.1080/02541858.1988.11448111

    Article  Google Scholar 

  • Hong J-S, Lee C-L (2014) First record of the Thalassinid Upogebia issaeffi (Balss, 1913) (Crustacea: Decapoda: Upogebiidae) in Korean waters. Ocean Sci J 49:73–82. doi:10.1007/s12601-014-0008-7

    Article  Google Scholar 

  • Hughes TE (1940) The effects on the fat and starch metabolism of Gebia by the parasite Gyge Branchialis. J Exp Biol 17:331–336

    Google Scholar 

  • Kevrekidis T, Gouvis N, Koukouras A (1997) Population dynamics, reproduction and growth of Upogebia pusilla (decapoda, thalassinidea) in the evros delta (North Aegean Sea). Crustacceana 70:799–812. doi:10.1163/156854097X00249

    Article  Google Scholar 

  • Kinoshita K, Itani G, Uchino T (2010) Burrow morphology and associated animals of the mud shrimp Upogebia yokoyai (Crustacea: Thalassinidea: Upogebiidae). J Mar Biol Assoc UK 90:947–952. doi:10.1017/S0025315410000214

    Article  Google Scholar 

  • Mikheev VN, Pasternak AF, Valtonen ET, Taskinen J (2014) Increased ventilation by fish leads to a higher risk of parasitism. Parasit Vectors 7:281. doi:10.1186/1756-3305-7-281

    Article  Google Scholar 

  • Mouritsen KN, McKechnie S, Meenken E et al (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. J Mar Biol Assoc UK 83:307–310. doi:10.1017/S0025315403007124h

    Article  Google Scholar 

  • Nanri T, Fukushige M, Ubaldo JP et al (2010) Occurrence of abnormal sexual dimorphic structures in the gonochoristic crustacean, Upogebia major (Thalassinidea: Decapoda), inhabiting mud tidal flats in Japan. J Mar Biol Assoc UK 91:1049–1057. doi:10.1017/S0025315410001712

    Article  Google Scholar 

  • Nel P, Branch G (2013) Assessment of the abundance and distribution of burrowing sandprawns and mudprawns (Callichirus and Upogebia species) in Langebaan Lagoon, South Africa. Afr J Mar Sci 35:195–208. doi:10.2989/1814232X.2013.795914

    Article  Google Scholar 

  • Papaspyrou S, Thessalou-Legaki M, Kristensen E (2004) Impact of Pestarella tyrrhena on benthic metabolism in sediment microcosms enriched with seagrass and macroalgal detritus. Mar Ecol Prog Ser 281:165–179. doi:10.3354/meps281165

    Article  Google Scholar 

  • Pascal L, Maire O, Volkenborn N et al (2016) Influence of the mud shrimp Upogebia pusilla (Decapoda: Gebiidea) on solute and porewater exchanges in an intertidal seagrass (Zostera noltei) meadow of Arcachon Bay: an experimental assessment. J Exp Mar Biol Ecol 477:69–79. doi:10.1016/j.jembe.2016.01.008

    Article  Google Scholar 

  • Pillay D, Branch GM (2011) Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanogr Mar Biol 49:137–192

    Google Scholar 

  • Pinn EH, Atkinson RJA, Rogerson A (2001) Sexual dimorphism and intersexuality in Upogebia stellata (Crustacea: Decapoda: Thalassinidea). J Mar Biol Assoc UK 81:1061–1062. doi:10.1017/S0025315401005070

    Google Scholar 

  • Plus M, Dalloyau S, Trut G et al (2010) Long-term evolution (1988–2008) of Zostera spp. meadows in Arcachon Bay (Bay of Biscay). Estuar Coast Shelf Sci 87:357–366. doi:10.1016/j.ecss.2010.01.016

    Article  Google Scholar 

  • Repetto M, Griffen BD (2011) Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer. Mar Freshw Res 63:60–67. doi:10.1071/MF11158

    Article  Google Scholar 

  • Sasaki A, Nakao H, Yoshitake S, Nakatsubo T (2014) Effects of the burrowing mud shrimp, Upogebia yokoyai, on carbon flow and microbial activity on a tidal flat. Ecol Res 29:493–499. doi:10.1007/s11284-014-1149-y

    Article  Google Scholar 

  • Smith AE, Chapman JW, Dumbauld BR (2008) Population Structure and Energetics of the Bopyrid Isopod Parasite Orthione griffenis in Mud Shrimp Upogebia pugettensis. J Crustac Biol 28:228–233. doi:10.1163/20021975-99990368

    Article  Google Scholar 

  • Tucker BW (1930) Memoirs: on the effects of an Epicaridan Parasite, Gyge branchialis, on Upogebia littoralis. Q J Microsc Sci s2-74:1–118

    Google Scholar 

  • Tunberg B (1986) Studies on the population ecology of Upogebia deltaura (Leach) (Crustacea, Thalassinidea). Estuar Coast Shelf Sci 22:753–765. doi:10.1016/0272-7714(86)90097-1

    Article  Google Scholar 

  • Ubaldo JP, Nanri T, Takada Y, Saigusa M (2014) Prevalence and patterns of infection by the epicaridean parasite, Gyge ovalis and the emergence of intersex in the estuarine mud shrimp, Upogebia major. J Mar Biol Assoc UK 94:557–566. doi:10.1017/S0025315413001392

    Article  Google Scholar 

  • Williams JD, An J (2009) The cryptogenic parasitic isopod Orthione griffenis Markham, 2004 from the eastern and western Pacific. Integr Comp Biol 49:114–126. doi:10.1093/icb/icp021

    Article  Google Scholar 

  • Williams JD, Boyko CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS One 7:e35350. doi:10.1371/journal.pone.0035350

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to P. Ramond, E. Teisseire, A. Dairain, J. Vongue and I. Pérez for their significant help. We thank the captain and the crewmembers of the R/V Planula IV (CNRS-INSU-FOF) for assistance in the field. We also thank the three reviewers whose thorough and constructive comments greatly helped to improve the manuscript. This work is part of Ludovic Pascal’s doctoral thesis (Université de Bordeaux).

Funding

Ludovic Pascal was supported by a doctoral grant of the French “Ministère de l’Enseignement Supérieur et de la Recherche” (Université de Bordeaux – 2013/AF/25). This work is a contribution to the UPOBA project funded by the CNRS-INSU program (EC2CO-DRIL). It has been partially conducted with financial support from the French National Research Agency (ANR) in the framework of the Investments for the Future Programme, within the COTE Cluster of Excellence (ANR-10-LABX-45). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. EPOC, UMR 5805, Univ. Bordeaux, 33400, Talence, France

    Ludovic Pascal, Xavier de Montaudouin, Antoine Grémare & Olivier Maire

  2. EPOC, UMR 5805, CNRS, 33400, Talence, France

    Ludovic Pascal, Xavier de Montaudouin, Antoine Grémare & Olivier Maire

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  1. Ludovic Pascal
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  2. Xavier de Montaudouin
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Correspondence to Ludovic Pascal.

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Pascal, L., de Montaudouin, X., Grémare, A. et al. Dynamics of the Upogebia pusilla–Gyge branchialis marine host–parasite system. Mar Biol 163, 195 (2016). https://doi.org/10.1007/s00227-016-2969-9

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