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Spillover but no spillback of two invasive parasitic copepods from invasive Pacific oysters (Crassostrea gigas) to native bivalve hosts

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Abstract

Invasive species can cause indirect effects on native biota by modifying parasite-host interactions and disease occurrence in native species. This study investigated the role of the invasive Pacific oyster (Crassostrea gigas) in potential spillover (co-introduced parasites infect native hosts) and spillback (native or established parasites infect invasive hosts and re-infect native hosts) scenarios of recently introduced (Mytilicola orientalis) and previously established (Mytilicola intestinalis) marine parasitic copepods in two regions in northern Europe, the Dutch Delta and the Wadden Sea. By examining 3416 individuals of 11 potential host species from sympatric host populations, we found that the recently introduced parasite M. orientalis does not only infect its principal host, the invasive Pacific oyster (prevalence at infected sites 2–43 %, mean intensity 4.1 ± 0.6 SE), but also native blue mussels (Mytilus edulis; 3–63 %, 2.1 ± 0.2), common cockles (Cerastoderma edule; 2–13 %, 1.2 ± 0.3) and Baltic tellins (Macoma balthica; 6–7 %, 1.0 ± 0), confirming a spillover effect. Spillback effects were not observed as the previously established M. intestinalis was exclusively found in blue mussels (prevalence at infected locations 3–72 %, mean intensity 2.4 ± 0.3 SE). The high frequency of M. orientalis spillover, in particular to native mussels, suggests that Pacific oysters may cause strong parasite-mediated indirect impacts on native bivalve populations.

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References

  • Aguirre-Macedo ML, Kennedy CR (1999) Diversity of metazoan parasites of the introduced oyster species Crassostrea gigas in the Exe Estuary. J Mar Biol Assoc UK 79:57–63

    Article  Google Scholar 

  • Arakawa KY (1990) Commercially important species of oysters in the world. Mar Freshw Behav Phy 17:1–13

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Bauer ON, Pugachev ON, Voronin VN (2002) Study of parasites and diseases of sturgeons in Russia: a review. J Appl Ichthyol 18:420–429

    Article  Google Scholar 

  • Bouchet P, Rocroi J-P, Bieler R, Carter JG, Coan EV (2010) Nomenclator of bivalve families with a classification of bivalve families. Part 1. Nomenclator of bivalve names of the family-group and above. Part 2. Classification of bivalve families. Malacologia 52:1–184

    Article  Google Scholar 

  • Camacho AP, Villalba A, Labarta U, Beiras R (1997) Absorption efficiency and condition of cultured mussels (Mytilus edulis galloprovincialis Linnaeus) of Galicia (NW Spain) infected by parasites Marteilia refringens Grizel et al. and Mytilicola intestinalis Steuer. J Shellf Res 16:77–82

    Google Scholar 

  • Cole HA (1951) Le Mytilicola en Angleterre. Rev des Trav (de l’Office Sci et Tech Des Peches Marit) 17:9–13

    Google Scholar 

  • Dabouineau L, Ponsero A (2009) Synthesis on biology of common European cockle Cerastoderma edule, 2nd edn. Université Catholique de l’Ouest - Réserve Naturelle Nationale Baie de St-Brieuc, p 17

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Davis MA (2009) Invasion biology. Oxford University Press, Oxford

  • Dekker R, Beukema JJ (2007) Long-term and large-scale variability in productivity of the tellinid bivalve Macoma balthica on Wadden Sea tidal flats. Mar Ecol Prog Ser 337:117–134

    Article  Google Scholar 

  • Dethlefsen V (1972) Zur Parasitologie der Miesmuschel (Mytilus edulis L., 1758). Ber der Dtsch Wiss Komm Meeresforsch 22:344–371

    Google Scholar 

  • Dethlefsen V (1985) Mytilicola intestinalis parasitism. In: Sindermann CJ (ed) Fiches d’identification des maladies et parasites des poissons, crustacés et mollusques, vol 24. ICES, Copenhagen, pp 1–4

  • Drinkwaard AC (1999) Introductions and developments of oysters in the North Sea area: a review. Helgol Meeresunters 52:301–308

    Article  Google Scholar 

  • Elsner NO, Jacobsen S, Thieltges DW, Reise K (2011) Alien parasitic copepods in mussels and oysters of the Wadden Sea. Helgol Mar Res 65:299–307

    Article  Google Scholar 

  • Feis ME, Goedknegt MA, Thieltges DW, Buschbaum C, Wegner KM (2016) Biological invasions and host–parasite coevolution: different coevolutionary trajectories along separate parasite invasion fronts. Zoology 119:366–374

    Article  PubMed  Google Scholar 

  • Folmer EO, Drent J, Troost K, Büttger H, Dankers N, Jansen J, van Stralen M, Millat G, Herlyn M, Philippart CJM (2014) Large-scale spatial dynamics of intertidal mussel (Mytilus edulis L.) bed coverage in the German and Dutch Wadden Sea. Ecosystems 3:550–566

    Article  Google Scholar 

  • Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

    Article  Google Scholar 

  • Gee JM, Davey JT (1986) Stages in the life history of Mytilicola intestinalis STEUER, a copepod parasite of Mytilus edulis (L.), and the effect of temperature on their rates of development. ICES J Mar Sci 42:254–264

    Article  Google Scholar 

  • Georgiev BB, Anglov A, Vasileva GP, Sánchez MI, Hortas F, Mutafchiev Y, Pankov P, Green AJ (2014) Larval helminths in the invasive American brine shrimp Artemia franciscana throughout its annual cycle. Acta Parasitol 59:380–389

    Article  PubMed  Google Scholar 

  • Goedknegt MA, Feis ME, Wegner KM, Luttikhuizen PC, Buschbaum C, Camphuysen KC, van der Meer J, Thieltges DW (2016) Parasites and marine invasions: ecological and evolutionary perspectives. J Sea Res 113:11–27

    Article  Google Scholar 

  • Gotto V (2004) Commensal and parasitic copepods associated with marine invertebrates. In: Synopses of the British Fauna (new series) no. 46, 2nd edn, Linnean Society of London and the Estuarine and Coastal Sciences Association by Field Studies Council, Shrewsbury

  • Grizel H (1985) Parasitose a Mytilicola orientalis Mori. In: Sindermann DJ (ed) Fiches d’identification des maladies et parasites des poissons, crustacés et mollusques, vol 24. ICES, Copenhagen, pp 1–4

  • Hatcher MJ, Dick JTA, Dunn AM, Perkins S (2012) Disease emergence and invasions. Funct Ecol 26:1275–1287

    Article  Google Scholar 

  • Hepper BT (1953) Artificial infection of various molluscs with Mytilicola intestinalis, Steuer. Nature 172:250

    Article  CAS  PubMed  Google Scholar 

  • Hershberger PK, van der Leeuw BK, Gregg JL, Grady CA, Lujan KM, Gutenberger SK, Purcell MK, Woodson JC, Winton JR, Parsley MJ (2010) Amplification and transport of an endemic fish disease by an introduced species. Biol Invasions 12:3665–3675

    Article  Google Scholar 

  • His E (1977) Observations préliminaires sur la présence de Mytilicola orientalis Mori (1935) chez Crassostrea gigas Thunberg dans le basin d’Arcachon. Bull Soc Géol amis Mus Havre 64:7–8

    Google Scholar 

  • His E (1979) Mytilicolides et myicolides parasites des lamellibranches d’interet commercial du bassin d’Arcachon. Haliotis 8:99–102

    Google Scholar 

  • Holdich DM, Reeve ID (1991) Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introductions and water quality. Aquat Conserv Mar Freshw Ecosyst 1:139–158

    Article  Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    Article  CAS  PubMed  Google Scholar 

  • Kijewski T, Śmietanka B, Zbawicka M, Gosling E, Hummel H, Wenne R (2011) Distribution of Mytilus taxa in European coastal areas as inferred from molecular markers. J Sea Res 65:224–234

    Article  Google Scholar 

  • Korringa P (1968) On the ecology and distribution of the parasitic copepod Mytilicola intestinalis Steuer. Bijdr Dierkd 38:47–57

    Google Scholar 

  • Lauckner G (1983) Diseases of mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals. Biologische Anstalt Helgoland, Hamburg, pp 477–1083

    Google Scholar 

  • Lewicki KE, Huyvaert KP, Piaggio AJ, Diller LW, Franklin AB (2015) Effects of barred owl (Strix varia) range expansion on Haemoproteus parasite assemblage dynamics and transmission in barred and northern spotted owls (Strix occidentalis caurina). Biol Invasions 17:1713–1727

    Article  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Wiley-Blackwell, West Sussex

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group, Auckland

  • McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ, Symes A, Chanson J, Hoffmann M (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108

    Article  Google Scholar 

  • Miller A, Vincent RE (2006) Rapid natural selection for resistance to an introduced parasite of rainbow trout. Evol Appl 1:336–341

    Article  Google Scholar 

  • Moehler J, Wegner KM, Reise K, Jacobsen S (2011) Invasion genetics of Pacific oyster Crassostrea gigas shaped by aquaculture stocking practices. J Sea Res 66:256–262

    Article  Google Scholar 

  • Moore MN, Lowe DM, Gee JM (1978) Histopathological effects induced in Mytilus edulis by Mytilicola intestinalis and the histochemistry of the copepod intestinal cells. J Cons Int Explor Mer 38:6–11

    Article  CAS  Google Scholar 

  • Mori T (1935) Mytilicola orientalis, a new species of parasitic Copepoda. Zool Soc Jpn 47:687–693

    Google Scholar 

  • Parker IM, Simberloff D, Lonsdale D, Goodel K et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19

    Article  Google Scholar 

  • Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alternative acanthocephalan infections in native fish. J Anim Ecol 80:990–998

    Article  PubMed  Google Scholar 

  • Paterson RA, Lal A, Dale M, Townsend CR, Poulin R, Tompkins DM (2013) Relative competence of native and exotic fish hosts for two generalist native trematodes. Int J Parasitol: Parasites Wildl 2:136–143

    Google Scholar 

  • Perdon J, Troost K (2012) Handboek monstertuigen schelpdier inventarisaties. CVO: 12.006, IMARES, Yerseke

  • Pogoda B, Jungblut S, Buck BH, Hagen W (2012) Infestation of oysters and mussels by mytilicolid copepods: differences between natural coastal habitats and two offshore cultivation sites in the German Bight. J Appl Ichtyol 28:756–765

    Article  Google Scholar 

  • Poulin R, Morand S (1997) Parasite body size distributions: interpreting patterns of skewness. Int J Parasitol 27:959–964

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshw Biol 56:676–688

    Article  Google Scholar 

  • Prenter J, MacNeil C, Dick JT, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Reise K (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Senckenberg Marit 28:167–175

    Article  Google Scholar 

  • Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643–689

    Article  Google Scholar 

  • Sheath DJ, Williams CF, Reading AJ, Britton JR (2015) Parasites of non-native freshwater fishes introduced to England and Wales suggest enemy release and parasite acquisition. Biol Invasions 17:2235–2246

    Article  Google Scholar 

  • Simberloff D, Martin J, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 25:58–66

    Article  Google Scholar 

  • Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2014) Generalized linear mixed models using AD Model Builder. R package version 0.8.0

  • Sparks AK (1962) Metaplasia of the gut of the oyster Crassostrea gigas (Thunberg) caused by infection with the copepod Mytilicola orientalis Mori. J Invert Pathol 4:57–62

    Google Scholar 

  • Steuer A (1902) Mytilicola intestinalis n. gen. n. spec. aus dem Darme von Mytilus galloprovincialis Lam. (Vorläufige Mittheilung). Lam Zool Anz 25:635–637

    Google Scholar 

  • Stock JH (1965) On copepoda associated with Dutch molluscs. Basteria 29:65–71

    Google Scholar 

  • Stock JH (1993) Copepoda (Crustacea) associated with commercial and non-commercial Bivalvia in the East Scheldt, The Netherlands. Bijdr Dierk 63:61–64

    Google Scholar 

  • Theisen BF (1987) Mytilicola intestinalis Steuer and the condition of its host Mytilus edulis L. Ophelia 27:77–86

    Article  Google Scholar 

  • Thieltges DW, Krakau M, Andresen H, Fottner S, Reise K (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgol Mar Res 60:307–316

    Article  Google Scholar 

  • Thieltges DW, Reise K, Prinz K, Jensen KT (2009) Invaders interfere with native parasite-host interactions. Biol Invasions 11:1421–1429

    Article  Google Scholar 

  • Thorstad EB, Finstad AG, Jensen AJ (2007) To what extent does ethanol and freezing preservation cause shrinkage of juvenile Atlantic salmon and European minnow? Fish Manag Ecol 14:295–298

    Article  Google Scholar 

  • Tompkins DM, Sainsbury AW, Nettleton P, Buxton D, Gurnell J (2002) Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proc R Soc B 269:529–533

    Article  PubMed  PubMed Central  Google Scholar 

  • Troost K (2010) Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. J Sea Res 64:145–165

    Article  Google Scholar 

  • Van Zweeden C, Troost K, van Asch M, Kesteloo-Hendrikse JJ (2012) Het kokkelbestand in de Nederlandse kustwateren in 2012. IMARES Wageningen Report, C094/12. IMARES Wageningen UR, Ijmuiden, 45 pp

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Warner RE (1968) Role of introduced diseases in extinction of endemic Hawaiian avifauna. Condor 70:101–120

    Article  Google Scholar 

  • Watermann B, Thomsen A, Kolodzey H, Daehne B, Meemken M, Pijanowska U, Liebezeit G (2008) Histopathological lesions of molluscs in the harbour of Norderney, Lower Saxony, North Sea (Germany). Helgol Mar Res 62:167–175

    Article  Google Scholar 

  • Wells K (2015) The importance of parasite geography and spillover effects for global patterns of host-parasite associations in two invasive species. Divers Distrib 21:477–486

    Article  Google Scholar 

  • Wilson CB (1938) A new copepod from Japanese oysters transplanted to the Pacific Coast of the United States. J Wash Acad Sci 28:284–288

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

We thank the Netherlands Organization for Scientific Research (NWO) and the German Bundesministerium für Bildung und Forschung (BMBF) for funding (bilateral NWO-ZKO project 839.11.002). Anne-Karin Schuster thanks the German Academic Exchange Service (DAAD) for financial support. We are grateful to Anneke Bol for help with the molecular analysis and Rob Dekker, Jarco Havermans, Reinier Nauta, Simone Muck and Jennifer Welsh for their support with field work and Carola van Zweeden and Ad van Gool for the provision of samples. We also thank Karsten Reise for his fruitful comments that improved the manuscript. Finally, we appreciate the feedback of the three anonymous reviewers that helped to improve the manuscript.

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Authors and Affiliations

  1. Department of Coastal Systems and Utrecht University, NIOZ Royal Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB, Den Burg, Texel, The Netherlands

    M. Anouk Goedknegt, Anne-Karin Schuster, A. Sarina Jung, Pieternella C. Luttikhuizen, Jaap van der Meer & David W. Thieltges

  2. Institute of Environmental Sciences, University of Koblenz-Landau, Fortstraße 7, 76829, Landau, Germany

    Anne-Karin Schuster & René Gergs

  3. Helmholtz Centre for Polar and Marine Research, Alfred Wegener Institute, Wadden Sea Station Sylt, Hafenstrasse 43, 25992, List/Sylt, Germany

    Christian Buschbaum & K. Mathias Wegner

  4. IMARES Wageningen UR, P.O. Box 77, 4400 AB, Yerseke, The Netherlands

    Karin Troost

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  1. M. Anouk Goedknegt
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Goedknegt, M.A., Schuster, AK., Buschbaum, C. et al. Spillover but no spillback of two invasive parasitic copepods from invasive Pacific oysters (Crassostrea gigas) to native bivalve hosts. Biol Invasions 19, 365–379 (2017). https://doi.org/10.1007/s10530-016-1285-0

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