| More

Parasites affect hemocyte functionality in the hemolymph of the invasive Atlantic blue crab Callinectes sapidus from a coastal habitat of the Salento Peninsula (SE Italy)

Views: 606 Downloads: 444
PATRIZIA PAGLIARA (http://orcid.org/0000-0001-8936-7367), GIORGIO MANCINELLI
PATRIZIA PAGLIARA, GIORGIO MANCINELLI

Abstract


The blue crab Callinectes sapidus is an invasive alien species in the Mediterranean Sea. In native habitats, it is subjected to mortalities determined by different pathogens, including the dinoflagellate Hematodinium perezi, a parasite also affecting other brachyuran species. Specifically, Hematodinium-associated disease is acknowledged worldwide as an emerging infection for commercially important crustacean species, but the general diffusion in wild species is unknown. Here, a preliminary screening in C. sapidus hemolymph as well as in three indigenous crabs captured in SE Italy, evidenced the presence of unidentified protozoans in more than 70% of specimen, but the number of suspected Hematodinium cells was very low. The parasites occurrence affected C. sapidus hemocytes functionality, interfering with their role in innate immunity (i.e. phagocytosis or DOPA production). More studies are necessary in order to verify the impact of this alien brachyuran on invaded ecosystems as mediated by the spread of parasites and other pathogens.


Keywords


Callinectes sapidus; Hematodinium; alien species; crab hemocytes; phagocytosis; invertebrate immunity

Full Text:

PDF

References


Adlard, R.D., Miller, T.L, Smit, N.J., 2014. The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitology, 31,160-166.

Bachère, E., Mialhe, E., Rodriguez, J., 1995. Identification of defence effectors in the hemolymph of Crustaceans with particular reference to the shrimp Penaeus japonicus (Bate): prospects and applications. Fish and Shellfish Immunology, 5 (8), 597-612.

Beevers, N.D., Kilbride, E., Atkinson, R.J.A., Neil, D.M., 2012. Hematodinium infection seasonality in the Firth of Clyde (Scotland) Nephrops norvegicus population: a re-evaluation. Disease of Aquatic Organisms, 100, 95-104.

Carreras-Aubets, M., Montero, F.E., Padrós, F., Crespo, S., Carrassón, M., 2011. Parasites and hystopathology of Mullus barbatus and Citharus linguatula (Pisces) from two sites in the NW Mediterranean with different degrees of pollution. Scientia Marina, 75, 369-378.

Carrozzo, L., Potenza, L., Carlino, P., Costantini, M.L., Rossi, L. et al., 2014. Seasonal abundance and trophic position of the Atlantic blue crab Callinectes sapidus Rathbun 1896 in a Mediterranean coastal habitat. Rendiconti Lincei Scienze Fisiche e Naturali, 25 (2), 201-208.

Chung, J.S., Pitula, J.S., Schott, E.J., Alvarez, V., Maurer, L. et al., 2015. Elevated water temperature increases the levels of reo-like virus and selected innate immunity genes in hemocytes and hepatopancreas of adult female blue crab, Callinectes sapidus. Fish & Shellfish Immunology, 47, 511-520.

Cilenti, L., Pazienza, G., Scirocco, T., Fabbrocini, A., D’Adamo, R., 2015. First record of ovigerous Callinectes sapidus (Rathbun, 1896) in the Gargano Lagoons (south-west Adriatic Sea). BioInvasions Records, 4 (4), 281-287.

Colla, S.R., Otterstatter, M.C., Gegear, R.J., Thomson, J.D., 2006. Plight of the bumble bee: Pathogen spillover from commercial to wild populations. Biological Conservation 129, 461-467.

Daszak, P., Cunningham, A.A., Hyatt, A.D., 2000. Emerging Infectious Diseases of Wildlife - Threats to Biodiversity and Human Health. Science, 287 (5452), 443-449.

Dulčić, J., Tutman, P., Matić-Skoko, S., Glamuzina, B., 2011. Six years from first record to population establishment: The case of the blue crab, Callinectes sapidus Rathbun, 1896 (Brachyura, Portunidae) in the Neretva river delta (South-Eastern Adriatic Sea, Croatia). Crustaceana, 84, 1211-1220.

Fan, T.J., Wang, X.F., 2002. Purification and partial bio-chemical charactization of phenoloxidase from Penaeus chinensis. Acta Biochimica et Biophysica Sinica, 34 (5), 589-594.

Flowers, E.M., Simmonds, K., Messick, G.A., Sullivan, L., Schott, E.J., 2016. PCR-based prevalence of a fatal reovirus of the blue crab, Callinectes sapidus (Rathbun) along the northern Atlantic coast of the USA. Journal of Fish Diseases, 39, 705-714.

Goedknegt, M.A., Feis, M.E., Wegner, K.M., Luttikhuizen, P.C., Buschbaum, C. et al., 2016. Parasites and marine invasions: Ecological and evolutionary perspectives. Journal of Sea Research, 113, 11-27.

Goedknegt, M.A., Havermans, J., Waser, A.M., Luttikhuizen, P.C., Velilla, E. et al., 2017. Cross-species comparison of parasite richness, prevalence, and intensity in a native compared to two invasive brachyuran crabs. Aquatic Invasions, 12, 1-12.

Granek, E.F., Brumbaugh, D.R., Heppell, S.A., Heppell, S.S., Secord, D., 2005. A blueprint for the oceans: implications of two national commission reports for conservation practitioners. Conservation Biology, 19, 1008-1018.

Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P. et al., 2002. Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.

Innocenti, G., Galil, B.S., 2007. Modus vivendi: invasive host/parasite relations - Charybdis longicollis Leene, 1938 (Brachyura: Portunidae) and Heterosaccus dollfusi Boschma, 1960 (Rhizocephala: Sacculinidae). Hydrobiologia, 590, 95-101.

Itami, T., Asano, M., Tokushige, K., Kubono, K., Nakagawa, A. et al., 1998. Enhancement of disease resistance of Kuruma shrimp, Penaeus japonicas after oral administration of peptidoglycan derived from Bifidobacterium thermophilum. Aquaculture, 164, 277-288.

Ju, S.J., Secor, D.H., Harvey, H.R., 2001. Growth rate variability and lipofuscin accumulation rates in the blue crab Callinectes sapidus. Marine Ecology Progress Series, 224, 197-205.

Katsanevakis, S., Wallentinus, I., Zenetos, A., Leppäkoski, E., Çinar, M.E. et al., 2014. Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquatic Invasions, 9, 391-423.

Kuris, A.M., Torchin, M.E., Lafferty, K.D., 2004. Parasites in the thoracic ganglion of Pachygrapsus marmoratus (Brachyura: Grapsidae) from the coast of Portugal. Parasite, 11, 425-427.

Lawson Handley, L-J., Estoup, A., Evans, D.M., Thomas, C.E., Lombaert, E. et al., 2011. Ecological genetics of invasive alien species. BioControl, 56, 409-428.

Leignel, V., Stillman, J.H., Baringou, S., Thabet, R., Metais, I., 2014. Overview on the European green crab Carcinus spp. (Portunidae, Decapoda), one of the most famous marine invaders and ecotoxicological models. Environmental Science and Pollution Research, 21, 9129-9144.

Le Moullac, G., Haffner, P., 2000. Environmental factors affecting immune responses in Crustacea. Aquaculture, 191 (1-3), 121-131.

Li, W., Tang, X., Xing, J., Sheng, X., Zhan, W., 2014. Proteomic analysis of differentially expressed proteins in Fenneropenaeus chinensis hemocytes upon white spot syndrome virus infection. PLoS One, e89962. http://dx.doi.org/10.1371/journal.pone.0089962.

Lin, X., Söderhäll, I., 2011. Crustacean hematopoeisis and the astakine cytokines. Blood, 117, 6417-6424.

Lips, K.R., Brem, F., Brenes, R., Reeve, J.D., Alford, R.A. et al., 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA, 103, 3165-3170.

Mancinelli, G., Carrozzo, L., Marini, G., Costantini, M.L., Rossi, L. et al., 2013a. Occurrence of the Atlantic blue crab Callinectes sapidus (Decapoda, Brachyura, Portunidae) in two Mediterranean coastal habitats: Temporary visitor or permanent resident? Estuarine, Coastal and Shelf Science, 135, 46-56.

Mancinelli, G., Carrozzo, L., Marini, G., Pagliara, P., Pinna, M., 2013b. The co-occurrence of Callinectes sapidus Rathbun, 1896 (Brachyura: Portunidae) and the parasitic dinoflagellate Hematodinium sp. (Dinoflagellata: Syndinidae) in two transitional water ecosystems of the Apulia coastline (South-Italy). Transitional Waters Bulletin, 7, 32-42.

Mancinelli, G., Glamuzina, B., Petrić, M., Carrozzo, L., Glamuzina, L. et al., 2016.The trophic position of the Atlantic blue crab Callinectes sapidus Rathbun 1896 in the food web of Parila Lagoon (South Eastern Adriatic, Croatia): a first assessment using stable isotopes. Mediterranean Marine Science, 17, 634-643.

Mancinelli, G., Chainho, P., Cilenti, L., Falco, S., Kapiris, K. et al., 2017a. The Atlantic blue crab Callinectes sapidus in southern European coastal waters: distribution, impact and prospective invasion management strategies. Marine Pollution Bulletin, 119, 5-11.

Mancinelli, G., Guerra, M.T., Alujević, K., Raho, D., Zotti, M. et al., 2017b. Trophic flexibility of the Atlantic blue crab Callinectes sapidus in invaded coastal systems of the Apulia region (SE Italy): A stable isotope analysis. Estuarine, Coastal and Shelf Science, 198, 421-431.

Mancuso, M., Zaccone, R., Carella, F., Maiolino, P., De Vico, G., 2013. First episode of a shell disease syndrome in Carcinus aestuarii (Crustacea: Decapoda: Portunidae) at Volturno River. Journal of Aquaculture Research & Development, 4, 191 doi:10.4172/2155-9546.1000191

Messick, G.A., 1994. Hematodinium perezi infections in adult and juvenile blue crabs Callinectes sapidus from coastal bays of Maryland and Virginia, USA. Disease of Aquatic Organisms, 19, 77-82.

Messick, G.A., Shields, J.D., 2000. Epizootiology of the parasitic dinoflagellate Hematodinium sp. in the American blue crab Callinectes sapidus. Disease of Aquatic Organisms, 43, 139-152.

Nehring, S., 2011. Invasion history and success of the American blue crab Callinectes sapidus in European and adjacent waters. p. 607-624.

In: The Wrong Place - Alien Marine Crustaceans: Distribution, Biology and Impacts. Galil, B.S., Clark, P.F., Carlton, J.T. (Eds). Springer-Verlag, Berlin-Heidelberg.

Panek, F.M., 2005. Epizootics and disease of coral reef fish in the Tropical Western Atlantic and Gulf of Mexico. Reviews in Fisheries Science, 13, 1-21.

Pérez-i-García, D., Constenla, M., Soler-Membrives, A., Cartes, J.E., Solé, M. et al., 2017. Natural variability of parasite communities of Macrouridae of the middle and lower slope of the Mediterranean Sea and their relation with fish diet and health indicators. Deep Sea Research Part I: Oceanographic Research Papers, 124, 1-17.

Prenter, J., MacNeil, C., Dick, J.T.A., Dunn, A.M., 2004. Roles of parasites in animal invasions. Trends in Ecology & Evolution 19, 385-390.

Shields, J.D., Taylor, D.M., Sutton, S.G., O'Keefe, P.G., Ings, D.W. et al., 2005. Epidemiology of bitter crab disease (Hematodinium sp.) in snow crabs Chionoecetes opilio from Newfoundland, Canada. Disease of Aquatic Organisms, 64, 253-264.

Shields, J.D., Sullivan, S.E., Small, H.J., 2015. Overwintering of the parasitic dinoflagellate Hematodinium perezi in dredged blue crabs (Callinectes sapidus) from Wachapreague Creek, Virginia. Journal of Invertebrate Pathology, 130, 124-132.

Söderhäll, K., Cerenius, L., Johansson, M.W., 1994. The prophenoloxidase activating system and its role in invertebrate defence. Annals of the New York Academy of Sciences, 712, 155-161.

Söderhäll, K., Cerenius, L., 1998. Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology, 10 (1), 23-28.

Sritunyalucksana, K., Soderhall, K., 2000. The proPO clotting system in crustacean. Aquaculture, 191, 53-69.

Stentiford, G.D., Evans, M., Bateman, K., Feist, S.W., 2003. Co-infection by a yeast-like organism in Hematodinium-infected European edible crabs Cancer pagurus and velvet swimming crabs Necora puber from the English Channel. Disease of Aquatic Organisms, 54, 195-202.

Stentiford, G.D., Feist, S.W., Bateman, K.S., Hine, P.M., 2004. Hemolymph parasite of the shore crab Carcinus maenas: pathology, ultrastructure and observations on crustacean haplosporidians. Disease of Aquatic Organisms, 59, 57-68.

Stentiford, G.D., Neil, D.M., 2011. Diseases of Nephrops and Metanephrops: a review. Journal of Invertebrate Pathology, 106, 92-109.

Stentiford, G.D., Neil, D.M., Peeler, E.J., Shields, J.D., Mall, H.J. et al., 2012. Disease will limit future food supply from the global crustacean fishery and aquaculture sectors. Journal of Invertebrate Pathology, 110, 141-157.

Stentiford, G.D., Bateman, K.S., Stokes, N.A., Carnegie, R.B., 2013. Haplosporidium littoralis sp. nov.: a crustacean pathogen within the Haplosporida (Cercozoa, Ascetosporea). Disease of Aquatic Organisms, 105, 243-252.

Sung, H.H., Kuo, P.A., Kao, W.Y., 2000. Effect of lipopolysaccharide on in vitro phagocytosis by hemocytes from giant freshwater prawn (Macrobrachium rosenbergii). Fish Pathology, 35(3), 109-116.

Vivares, C.P., 1971. Etude des parasites des crustacés décapodes brachyoures: némertes et larves de cestodes. Annales de Parasitologie Humaine et Comparée, 46, 1-9.

Zhang, Z.F., Shao, M., Ho Kang, K., 2006. Classification of haematopoietic cells and haemocytes in Chinese prawn Fenneropenaeus chinensis. Fish & Shellfish Immunology, 21 (2), 159-169.


Refbacks

  • There are currently no refbacks.