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New Data on Perkinsus Mediterraneus in the Balearic Archipelago: Locations and Affected Species

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New Data on Perkinsus Mediterraneus in the Balearic Archipelago: Locations and Affected Species Vol. 112: 69–82, 2014 DISEASES OF AQUATIC ORGANISMS Published November 13 doi: 10.3354/dao02795 Dis Aquat Org New data on Perkinsus mediterraneus in the Balearic Archipelago: locations and affected species J. M. Valencia1, M. Bassitta2, A. Picornell2, C. Ramon2, J. A. Castro2,* 1Laboratori d’Investigacions Marines i Aqüicultura (LIMIA), Av. Ingeniero Gabriel Roca, 69, Port d’Andratx, Illes Balears, 07158, Spain 2Laboratori de Genètica, Departament de Biologia, Universitat de les Illes Balears, Campus de la UIB, Palma de Mallorca, Illes Balears, 07122, Spain ABSTRACT: Perkinsus mediterraneus, a protozoan parasite that can cause perkinsosis (marine mollusc disease), was first detected in oysters Ostrea edulis from Mahon (Minorca, Balearic Islands, Spain) in 2004. Several years later it was also found in Andratx Harbour (Majorca, Balearic Islands) and in the Gulf of Manfredonia (Adriatic coast of Italy) in oyster populations. Since 2007, Perkinsus surveys have been conducted in different localities and shellfish species in the Balearic Archipelago. In the present work, we found P. mediterraneus in the Balearic Islands infecting oyster and other shellfish species. We describe infection with P. mediterraneus for the first time in Arca noae and Mimachlamys varia. The detection was carried out using Ray’s fluid thioglycolate medium (RFTM), histology and polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) methodologies. The internal transcribed spacer (ITS) region (including ITS1, 5.8S and ITS2) of P. mediterraneus ribosomal DNA was sequenced from infected bivalve gills (or from the body in Chamelea gallina) from Balearic Archipelago localities. Twelve haplotypes with a strong genetic similarity between them (97−100%) were observed in our sam- ples. These data were completed with 12 more haplotypes from GenBank sequences. The phylo- genetic relationship between Balearic P. mediterraneus haplotypes found in this study, those pre- viously obtained in Mahon Harbour, and the Perkinsus spp. sequences available in GenBank clearly grouped the different Perkinsus spp. in distinct clades supported by strong bootstrap val- ues. Moreover, these analyses detected different P. mediterraneus groups in O. edulis from Minorca Island. No abnormal mortalities or decline in populations were detected during the sur- vey, except for C. gallina, which is also affected by Marteilia refringens. KEY WORDS: Perkinsus mediterraneus · Arca noae · Chamelea gallina · Mimachlamys varia · Ostrea edulis · Balearic Islands · Internal transcribed spacer Resale or republication not permitted without written consent of the publisher INTRODUCTION Canada (Bower et al. 1998), along the Atlantic coast of SW Europe (Azevedo 1989), in the Mediterranean Sea Perkinsosis is a marine mollusc disease caused by (Da Ros & Canonzier 1985, Santmartí et al. 1995), in Perkinsus spp. protozoan parasites. It has been associ- southern Australia (Lester & Davis 1981, Goggin & ated with elevated mortalities of commercially impor- Lester 1995), and along the south and west coasts of tant molluscs in the Gulf of Mexico, along the Atlantic Korea (Choi & Park 1997, Park & Choi 2001). coast of North America (Andrews & Hewatt 1957, Several Perkinsus species have been found in mol- Mackin & Hopkins 1962, Burreson & Ragone Calvo luscs, but to date, only 7 are recognized as valid. The 1996, Ford 1996, Soniat 1996), in British Colum bia, first described species was P. marinus in USA in the *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 70 Dis Aquat Org 112: 69–82, 2014 1940s; it affects the American oyster Crassostrea vir- internal transcribed spacer (ITS) sequences. The ginica and induces severe mortalities (Ray 1966b). phylogenetic relationships between P. mediterraneus P. olseni, the second named species of Perkinsus, was lineages from this area with other Perkinsus spp. described in 1981 in the abalone Haliotis ruber in were also established. Australia, and was also found to be responsible for important mortalities of the abalone H. laevigata (Lester & Davis 1981, Goggin & Lester 1995). It is also MATERIALS AND METHODS believed to occur in a wide variety of mollusc species from the Great Barrier Reef (Goggin & Lester 1995). Mollusc tissue samples In 1989, P. atlanticus was detected in the carpet shell clam Ruditapes decussatus following mass mortali- A total of 314 wild and cultivated European flat oys- ties in Portugal (Azevedo 1989). Other clams and ters Ostrea edulis, Noah’s Ark shells Arca noae, areas have also revealed the presence of these spe- striped Venus shells Chamelea gallina, cultivated var- cies (Villalba et al. 2004). In the meantime, molecular iegated scallops Mimachlamys varia and mussels systematics demonstrated that P. olseni was a senior Mytilus galloprovincialis were collected from coastal synonym of P. atlanticus (Murrell et al. 2002). Two locations in Minorca, Majorca and Ibiza-Formentera, other Perkinsus species were proved to be synony- Spain, in September from 2007 to 2013 (Table 1, mous on the basis of molecular analysis: P. chesa- Fig. 1). One gill from each individual was preserved in peaki, a parasite of the soft-shell clam Mya arenaria 95% (v/v) ethanol for DNA extraction and PCR analy- (McLaughlin et al. 2000), and P. andrewsi, a parasite sis, except for C. gallina, in which half of the body was of the Baltic clam Macoma bal thica (Coss et al. 2001). used, due to their small size. Visceral mass sections P. qugwadi, res ponsible for mortalities of the Japan- were also preserved for histological examination. ese scallop Patinopecten yessoensis in Canada, is distinguished from the other species so far identified because of its distinct characteristics: it does not RFTM assays enlarge in Ray’s fluid thioglycollate medium (RFTM) or stain blue-black with Lugol’s iodine (no develop- For these assays, the other gill from each individual ment in prezoosporangia); its zoospores can develop or a quarter of the C. gallina whole body was individ- within the interstitial space of its living host; it can ually incubated in RFTM (Ray 1966a) supplemented proliferate and be a pathogen at cold temperatures, with chloramphenicol and nystatin for a week at and its molecular characteristics are considerably dif- room temperature in the dark, to induce transfor - ferent from other species of Perkinsus (Bower et al. mation of the parasite’s trophozoites into hypno - 1998, Blackbourn et al. 1998). Currently, its classifi- spores of Perkinsus. These samples were then par- cation in the Perkinsus genus is controversial (Casas tially crushed on a slide using a scalpel, stained with et al. 2002b). Other new Perkinsus species have been Lugol’s iodine solution and observed under light characterized: P. mediterraneus in the flat oyster microscopy to estimate the intensity of Perkinsus Ostrea edulis from the Balearic Islands, Spain (Casas infection according to the following scale (Ray 1954, et al. 2004), P. honshuensis in Manila clam R. philip- modified in Andrews & Hewatt 1957)–0 = null infec- pinarum from Japan (Dungan & Reece 2006), and tion: no Perkinsus sp. detected in the whole slide P. beihaiensis in the oysters C. hong kong ensis and (40×); 1 = very light infection: from 1 Perkinsus sp. C. ariakensis from southern China (Moss et al. 2008). hypnospore observed in the whole slide (40×); 2 = In Mediterranean waters, only 2 species, P. olseni light infection: at least 1 Perkinsus sp. hypnospore and P. mediterraneus, have been described (Casas et observed in every one of 10 random fields scattered al. 2004, Abollo et al. 2006, Elandaloussi et al. 2009, throughout the preparation (40×); 3 = moderate Valencia 2010, Ramilo et al. 2010). Polymerase chain infection: at least 10 Perkinsus sp. hypnospores reaction-restriction fragment length polymorphism observed in every one of 10 random fields (40×), scat- (PCR-RFLP) and in situ hybridization have been used tered throughout the preparation; 4 = heavy infec- for differential diagnosis between them. tion: at least 10 Perkinsus sp. hypnospores observed In the present study, we report the presence of in every one of 10 random fields (100×), scattered P. mediterraneus found in several mollusc species throughout the preparation; and 5 = very heavy (O. edulis, Mimachlamys varia, Chamelea gallina infection: at least 50 Perkinsus sp. hypnospores ob - and Arca noae) from the Balearic Islands, based on served in every one of 10 random fields (100×), scat- RFTM assay, histology, PCR-RFLP and analysis of tered throughout the preparation. Valencia et al.: Perkinsus mediterraneus in the Balearic Archipelago 71 Table 1. Ray’s fluid thioglycolate medium (RFTM) assay results obtained for Perkinsus infection. All bivalves (N = 314) were sampled in September except once in 2013. Mackin’s scale was used to determine the degree of infection. The average value for each assay is represented. Oysters from Ibiza-Formentera were frozen, so RTFM results were obviously negative; however, PCR results indicated that 11 of them were infected, but no data were obtained concerning degree of infection. Size is mean ± SD Location Bivalve sp. N Year Infected Detection Degree of Size (%) infection (mm) 1 Mahon Harbour Ostrea edulisa 32 2007 25 78.10 2.01 99.14±11.64 2 Fornells Bay Ostrea edulis 13 2010 8 61.50 0.77 86.52±11.98 3 Andratx Harbour Ostrea edulis 8 2011 5 62.50 1.37 74.66±9.96 6 2012 3 50.00 1.75 69.96±18.55 6 2013 4 66.70 0.67 87.40±14.56 Mimachlamys variaa 25 2011 15 60.00 0.87 34.52±7.81 25 2012 21 84.00 2.44 33.16±4.71 30 2013 25 83.30 2.4 41.97±6.66 14 2013b 14 100 2.36 34.49±4.69 Arca noae 20 2011 8 40.00 1.26 44.55±5.15 30 2012 16 53.30 0.8 50.29±5.88 Mytilus galloprovincialisa 30 2012 0 0 0 50.29±5.88 4 Palmanova Ostrea edulis 18 2010 5 27.80 1.14 90.67±19.00 5 Porto Cristo Ostrea edulis 15 2010 9 60.00 0.78 33.03±4.23 6 Ibiza-Formentera Ostrea edulis 18 2011 11a 61.10 No data 84.79±33.83 7 Arenal Beach Chamelea gallina 24 2012 6 25.00 0.25 20.40±0.82 aCultivated bivalves bSampled in October Fig.
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