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Richness and distribution of tropical oyster parasites in two oceans

  • KATRINA M. PAGENKOPP LOHAN (a1) (a2), KRISTINA M. HILL-SPANIK (a1) (a2), MARK E. TORCHIN (a3), LEOPOLDINA AGUIRRE-MACEDO (a4), ROBERT C. FLEISCHER (a2) and GREGORY M. RUIZ (a1)...
Summary
SUMMARY

Parasites can exert strong effects on population to ecosystem level processes, but data on parasites are limited for many global regions, especially tropical marine systems. Characterizing parasite diversity and distributions are the first steps towards understanding the potential impacts of parasites. The Panama Canal serves as an interesting location to examine tropical parasite diversity and distribution, as it is a conduit between two oceans and a hub for international trade. We examined metazoan and protistan parasites associated with ten oyster species collected from both Panamanian coasts, including the Panama Canal and Bocas del Toro. We found multiple metazoan taxa (pea crabs, Stylochus spp., Urastoma cyrinae). Our molecular screening for protistan parasites detected four species of Perkinsus (Perkinsus marinus, Perkinsus chesapeaki, Perkinsus olseni, Perkinsus beihaiensis) and several haplosporidians, including two genera (Minchinia, Haplosporidium). Species richness was higher for the protistan parasites than for the metazoans, with haplosporidian richness being higher than Perkinsus richness. Perkinsus species were the most frequently detected and most geographically widespread among parasite groups. Parasite richness and overlap differed between regions, locations and oyster hosts. These results have important implications for tropical parasite richness and the dispersal of parasites due to shipping associated with the Panama Canal.

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Corresponding author
*Corresponding author: Marine Invasions Laboratory, Smithsonian Environmental Research Center, Edgewater, Maryland 21037, USA. E-mail: lohank@si.edu
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Current address: Grice Marine Lab, College of Charleston, Charleston, South Carolina 29412, USA.

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References
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Aguirre-Macedo M. L., Simá-Álvarez R. A., Román-Magan M. K. and Güemez-Ricalde J. I. (2007). Parasite survey of the eastern oyster Crassostrea virginica in coastal lagoons of the southern Gulf of Mexico. Journal of Aquatic Animal Health 19, 270279.
Arzul I. and Carnegie R. B. (2015). New perspective on the haplosporidian parasites of molluscs. Journal of Invertebrate Pathology 131, 3242. doi:10.1016/j.jip.2015.07.014
Burreson E. M. (2008). Misuse of PCR assay for diagnosis of mollusc protistan infections. Diseases of Aquatic Organisms 80, 8183.
Burreson E. M. and Ford S. E. (2004). A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17, 499517.
Cáceres-Martínez J., Vásquez-Yeomans R. and Sluys R. (1998). The turbellarian Urastoma cyprinae from edible mussels Mytilus galloprovincialis and Mytilus californianus in Baja California, NW México. Journal of Invertebrate Pathology 72, 214219.
Cáceres-Martínez J., Ortega M. G., Vásquez-Yeomans R., García T. J. P., Stokes N. and Carnegie R. B. (2012). Natural and cultured populations of the mangrove oyster Saccostrea palmula from Sinaloa, Mexico, infected by Perkinsus marinus . Journal of Invertebrate Pathology 110, 321325.
Campos E. (2002). Two new genera of pinnotherid crabs from the tropical eastern Pacific (Decapoda: Brachyura: Pinnotheridae). Journal of Crustacean Biology 22, 328336.
Canestri Trotti G., Baccarani E. M., Gianetto S., Giuffrida A. and Paesanti F. (1998). Prevalence of Mytilicola intestinalis (Copepoda:Mytilicolidae) and Urastoma cyrinae (Turbellaria: Hypotrichinidae) in marketable mussels Mytilus galloprovincialis in Italy. Diseases of Aquatic Organisms 32, 145149.
Casas S. M., Villalba A. and Reece K. S. (2002). Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). I. Identification of the aetiological agent and in vitro modulation of zoosporulation by temperature and salinity. Diseases of Aquatic Organisms 50, 5165.
Coen L. D., Brumbaugh R. D., Bushek D., Grizzle R., Luckenbach M. W., Posey M. H., Powers S. P. and Tolley S. G. (2007). Ecosystem services related to oyster restoration. Marine Ecology Progress Series 341, 303307.
da Silva P. M., Scardua M. P., Vianna R. T., Mendonca R. C., Vieira C. B., Dungan C. F., Scott G. P. and Reece K. S. (2014). Two Perkinsus spp. infect Crassostrea gasar oysters from cultured and wild populations of the Rio São Francisco estuary, Sergipe, northeastern Brazil. Journal of Invertebrate Pathology 119, 6271.
Dang C., Dungan C. F., Scott G. P. and Reece K. S. (2015). Perkinsus sp. infections and in vitro isolates from Anadara trapezia (mud arks) of Queensland, Australia. Diseases of Aquatic Organisms 113, 5158.
Darriba D., Taboada G. L., Doallo R. and Posada D. (2012). jModelTest2: more models, new heuristics and parallel computing. Nature Methods 9, 772. doi: 10.1038/nmeth.2109
Fleming L. C., Michael D. B. B. and Bacon G. B. (1981). On some commensal Turbellaria of the Canadian east coast. In The Biology of the Turbellaria (ed. Schockaert E. R. and Ball I. R.), pp. 131137. Springer, The Hague, The Netherlands.
Geller J., Meyer C., Parker M. and Hawk H. (2013). Redesign of PCR primers for mitochondrial cytochrome oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources 13, 851861.
Glynn P. W. (1972). Observations on the ecology of the Caribbean and Pacific coasts of Panama. In The Panamic Biota: Some observations prior to a sea-level canal (ed. Jones M. L.), pp. 1330. Bulletin of the Biological Society of Washington, Washington, DC.
Goggin C. L. and Cannon L. R. G. (1989). Occurrence of a turbellarian from Australian tridacnid clams. International Journal for Parasitology 19, 345346.
Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W. and Gascuel O. (2010). New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3·0. Systematic Biology 59, 307321.
Hartikainen H., Ashford O. S., Berney C., Okamura B., Feist S. W., Baker-Austin C., Stentiford G. D. and Bass D. (2014). Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians. The ISME Journal 8, 177186.
Holt R. D., Dobson A. P., Begon M., Bowers R. G. and Schauber E. M. (2003). Parasite establishment in host communities. Ecology Letters 6, 837842.
Jones M. L. (1972). The Panamic Biota: Some Observations Prior to a Sea-Level Canal. Bulletin of the Biological Society of Washington, Washington, DC.
Katoh K. and Toh H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286298.
Katoh K., Misawa K., Kuma K. and Miyata T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066.
Kemp W. M., Boynton W. R., Adolf J. E., Boesch D. F., Boicourt W. C., Brush G., Cornwell J. C., Fisher T. R., Glibert P. M., Hagy J. D., Harding L. W., Houde E. D., Kimmel D. G., Miller W. D., Newell R. I. E., Roman M. R., Smith E. M. and Stevenson J. C. (2005). Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Marine Ecology Progress Series 303, 129.
Krasnov B. R., Poulin R., Shenbrot G. I., Mouillot D. and Khokhlova I. S. (2005). Host specificity and geographic range in haematophagous ectoparasites. Oikos 108, 449456.
Krasnov B. R., Shenbrot G. I., Khokhlova I. S., Mouillot D. and Poulin R. (2008). Latitudinal gradients in niche breadth: empirical evidence from haematophagous ectoparasites. Journal of Biogeography 35, 592601.
Lessios H. A. (2008). The great American schism: divergence of marine organisms after the rise of the Central American isthmus. Annual Review of Ecology, Evolution, and Systematics 39, 6391.
Lindenfors P., Nunn C. L., Jones K. E., Cunningham A. A., Sechrest W. and Gittleman J. L. (2007). Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecology and Biogeography 16, 496509.
Manning R. B. (1993). Three genera removed from the synonymy of Pinnotheres Bosc. 1802 (Brachyura: Pinnotheridae). Proceedings of the Biological Society of Washington 106, 523523.
Marko P. B. and Moran A. L. (2009). Out of sight, out of mind: high cryptic diversity obscures the identities and histories of geminate species in the marine bivalve subgenus Acar . Journal of Biogeography 36, 18611880.
Morand S. (2015). (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. International Journal for Parasitology: Parasites and Wildlife 4, 8087.
Moss J. A., Xiao J., Dungan C. F. and Reece K. S. (2008). Description of Perkinsus beihaiensis n. sp., a new Perkinsus sp. parasite in oysters of southern China. Journal of Eukaryotic Microbiology 55, 117130.
Murina G. V. and Solonchenko A. I. (1991). Commensals of Mytilus galloprovincialis in the Black Sea: Urastoma cyrinae (Turbellaria) and Polydora ciliata (Polychaeta). In The Biology of the Turbellaria (ed. Schockaert E. R. and Ball I. R.), pp. 385387. Springer, The Hague, The Netherlands.
Nunn C. L., Altizer S. M., Sechrest W. and Cunningham A. A. (2005). Latitudinal gradients of parasite species richness in primates. Diversity and Distributions 11, 249256.
Olsson A. A. (1972). Origin of the existing Panamic molluscan biotas in terms of their geologic history and their separation by the Isthmian land barrier. In The Panamic Biota: Some Observations Prior to a Sea-Level Canal (ed. Jones M. L.), pp. 117124. Bulletin of the Biological Society of Washington, Washington, DC.
Pagenkopp Lohan K. M., Hill-Spanik K. M., Torchin M. E., Strong E. E., Fleischer R. C. and Ruiz G. M. (2015). Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean. Marine Biology 162, 957968.
Poulin R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423434.
Poulin R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763.
Poulin R. (2010). Latitudinal gradients in parasite diversity: bridging the gap between temperate and tropical areas. Neotropical Helminthology 4, 169177.
Poulin R., Krasnov B. R., Mouillot D. and Thieltges D. W. (2011). The comparative ecology and biogeography of parasites. Philosophical Transactions: Biological Sciences 366, 23792390.
Prenter J., MacNeil C., Dick J. T. and Dunn A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution 19, 385390.
Reece K. S., Dungan C. F. and Burreson E. M. (2008). Molecular epizootiology of Perkinsus marinus and P. chesapeaki infections among wild oysters and clams in Chesapeake Bay, USA. Diseases of Aquatic Organisms 82, 237248.
Renault T., Stokes N. A., Chollet B., Cochennec N., Berthe F. C. J., Gerard A. and Burreson E. M. (2000). Haplosporidiosis in the Pacific oyster Crassostrea gigas from the French Atlantic coast. Diseases of Aquatic Organisms 42, 207.
Ronquist F. and Huelsenbeck J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Ruiz G. M., Torchin M. E. and Grant K. (2009). Using the Panama Canal to Test Predictions about Tropical Marine Invasions. Smithsonian Institution, Washington, DC.
Schemske D. W., Mittelbach G. G., Cornell H. V., Sobel J. M. and Roy K. (2009). Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics 40, 245269.
Smith J. T., Jackson J. B. and Fortunato H. (2006). Diversity and abundance of tropical American scallops (Bivalvia: Pectinidae) from opposite sides of the central American Isthmus. Veliger 48, 2645.
Taraschewski H. (2006). Hosts and parasites as aliens. Journal of Helminthology 80, 99128.
Torchin M. E., Muira O. and Hechinger R. F. (2015). Parasite species richness and intensity of interspecific interactions increase with latitude in two wide-ranging hosts. Ecology http://dx.doi.org/10.1890/15-0518.1
Torres J., Miquel J., Casanova J. C., Ribas A., Feliu C. and Morand S. (2006). Endoparasite species richness of Iberian carnivores: influences of host density and range distribution. Biodiversity and Conservation 15, 46194632.
Villalba A., Reece K. S., Camino Ordás M., Casas S. M. and Figueras A. (2004). Perkinsosis in molluscs: a review. Aquatic Living Resources 17, 411432.
Wang Z., Lu X., Liang Y. and Wang C. (2010). Haplosporidium nelsoni and H. costale in the Pacific oyster Crassostrea gigas from China's coasts. Diseases of Aquatic Organisms 89, 223228.
Wood J. L. and Andrews J. D. (1962). Haplosporidium costale (Sporozoa) associated with a disease of Virginia oyster. Science 136, 710711.
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