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Previously Unknown Apicomplexan Species Infecting Iceland Scallop, Chlamys Islandica

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Previously Unknown Apicomplexan Species Infecting Iceland Scallop, Chlamys Islandica Journal of Invertebrate Pathology 108 (2011) 147–155 Contents lists available at SciVerse ScienceDirect Journal of Invertebrate Pathology journal homepage: www.elsevier.com/locate/jip Previously unknown apicomplexan species infecting Iceland scallop, Chlamys islandica (Müller, 1776), queen scallop, Aequipecten opercularis L., and king scallop, Pecten maximus L. ⇑ Árni Kristmundsson a, , Sigurður Helgason a, Slavko Helgi Bambir a, Matthías Eydal a, Mark A. Freeman b a Institute for Experimental Pathology at Keldur, University of Iceland, Reykjavik, Iceland b Institute of Biological Sciences & Institute of Ocean and Earth Sciences, University of Malaya, Kuala Lumpur, Malaysia article info abstract Article history: Examination of three scallop species from three separate locations: Iceland scallop from Icelandic waters, Received 14 December 2010 king scallop from Scottish waters and queen scallop from Faroese and Scottish waters, revealed infections Accepted 19 August 2011 of a previously unknown apicomplexan parasite in all three scallop species. Developmental forms Available online 27 August 2011 observed in the shells appeared to include both sexual and asexual stages of the parasite, i.e. merogony, gametogony and sporogony, which suggests a monoxenous life cycle. Meronts, gamonts, zygotes and Keywords: mature oocysts were solely found in the muscular tissue. Zoites, which could be sporozoites and/or mer- Chlamys islandica ozoites, were observed in great numbers, most frequently in muscles, both intracellular and free in the Aequipecten opercularis extracellular space. Zoites were also common inside haemocytes. Examination of the ultrastructure Pecten maximus Iceland scallop showed that the zoites contained all the major structures characterizing apicomplexans. This apicom- Apicomplexa plexan parasite is morphologically different from other apicomplexan species previously described from Parasites bivalves. Presently, its systematic position within the phylum Apicomplexa cannot be ascertained. Bivalves Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction pelsineeri from Donax sp. and Tellina sp., they are poorly studied; this is especially so for scallops. Only few studies on parasites in the scal- Wild populations of Iceland scallop Chlamys islandica, queen lop species examined in the present paper exist in the literature, i.e. scallop Aequipecten opercularis (syn. Chlamys opercularis), and king the king scallop, the queen scallop and the Iceland scallop. One api- scallop Pecten maximus, are all commercially exploited shellfish complexan species, Pseudoklossia pectinis, has been reported from species. Iceland scallop has the most northern distribution, occur- king scallop off the French coast (Léger and Duboscq, 1917), and ring mainly in the sub-arctic transitional zone. In the Atlantic one from Iceland scallop in Icelandic waters, i.e. Margolisiella islan- Ocean it is found around Iceland, Greenland, in the Barents Sea, dica (Kristmundsson et al., 2011). The only parasitic examination off the northern coast of Norway south to Bergen and along the performed on queen scallop seems to be that of Lohrmann et al. east coast of Canada south towards Massachusetts. It has also been (2000), who reported a microsporidian infection in this species. recorded in the N-Pacific Ocean (Brand, 2006). King- and queen Mortenson (1993) published a health survey on selected bivalve scallops have a similar geographic distribution, which extends stocks in Norwegian waters. The king scallop was included in the more south than that of Iceland scallop. The queen scallop occurs survey, but no protozoan parasites were detected. To date, Argopec- in the NE-Atlantic from northern Norway and the Faroe Islands ten irradians is probably the most examined scallop species with re- south to the Iberian Peninsula, the Azores and the Canary Islands. gard to apicomplexan parasites, and several papers have been Its distribution also extends into the Mediterranean and Adriatic published (Karlsson, 1991; Cawthorn et al., 1992; Leibovitz et al., seas. The distribution of king scallop spans from northern Norway, 1984; Whyte et al., 1994). However, none of the apicomplexans along the west coast of Europe and south to North Africa (Nicolaj- encountered in these surveys have been identified to a species level. sen, 1997; Brand, 2006). Most apicomplexan species known to infect bivalves have been Although reports on apicomplexans infecting bivalves date back described from clams. These include Pseudoklossia (syn. Hyalloklos- to 1897, when Léger (1897) described the first species, Hyalloklossia sia) pelsineeri from Donax sp. and Tellina sp. (Léger, 1897), Pseudok- lossia glomerata, from Tapes floridus and Tapes virgineus (Léger and Duboscq, 1915), Pseudoklossia (syn. Merocystis) tellinovum from Tel- ⇑ Corresponding author. Address: Institute for Experimental Pathology, Univer- sity of Iceland, Reykjavik, Keldur v/Vesturlandsveg, IS-112 Reykjavik, Iceland. Fax: lina tenuis (Buchanan, 1979; Levine, 1988) and Margolisiella kabatai +354 567 3979. from the littleneck clam Protothaca staminae (Desser and Bower, E-mail address: [email protected] (Á. Kristmundsson). 1997). In addition, Morado et al. (1984) and Nakayama et al. 0022-2011/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.jip.2011.08.003 148 Á. Kristmundsson et al. / Journal of Invertebrate Pathology 108 (2011) 147–155 (1998) reported unidentified apicomplexans from the littleneck the following methods: (1) Fresh mounts: samples from each organ clam P. staminae and the giant clam Tridacna crocea, respectively. pressed between a glass slide and a coverslip, (2) Stained imprints: Some apicomplexan species infecting bivalves have direct life tissue imprints of organs (i.e. adductor muscle, heart and kidney) cycles, i.e. both asexual and sexual stages are present in the same were air dried, fixed in methanol for 3 min and stained with host (e.g. Desser and Bower, 1997), while in others, only sexual May–Grünwald–Giemsa, (3) Davidson’s fixed histological sections stages have been found, which could suggest the need for an addi- of all organs prepared by conventional methods and stained with tional host (Desser et al., 1998). Another possibility is that the Giemsa. Parasites present were described and their tissue distribu- asexual forms are present in the same host, but have not been de- tion analysed. All dimensions were measured (lm) and photo- tected. However, in some cases, such as Nematopsis spp., an indi- graphs taken using a Leica DMLB microscope equipped with a rect life cycle has been confirmed where sexual stages are found digital camera (Leica DC300F). in various bivalve species and schizogonic multiplication occurs For examination of parasite ultrastructure, small pieces in crustaceans (Lauckner, 1983; Soto et al., 1996; Darriba et al., (1mm3) of infected muscles were fixed in 2.5% buffered glutaral- 2010). Finally, there are documentations of apicomplexan parasites dehyde in 0.1 M sodium cacodylate buffer (pH 7.4) for 24 h at 4 °C, in bivalves where certain parasitic forms have been detected, washed three times in cacodylate buffer, post-fixed for 1 h in 1% which could not be identified as either asexual- or sexual forms OsO4, rinsed again with buffer, dehydrated in a graded alcohol ser- (Nakayama et al., 1998; Hine, 2002). According to papers published ies, sectioned, stained for 10 min in 5% uranyl acetate and for 6 min to date on apicomplexans of bivalves, it seems there are no exam- in 5% lead citrate. Ultrathin sections were examined using a FEI, ples where only the asexual reproduction, i.e. schizogony, occurs in Tecnai G2 Spirit Biotwin, Transmission Electron Microscope (at bivalves. 120 kV) at the Institute of Aquaculture, University of Stirling, In the year 2002 live scallops were sent to the Fish Disease Lab- Scotland. oratory at the Institute for Experimental Pathology at Keldur for examination due to abnormal mortality in the stock. Observations 3. Results revealed infections with two previously unknown apicomplexan species. All Iceland scallops and the queen scallops sampled in Faroese In this paper one of the apicomplexan species is described, but waters were infected with an apicomplexan parasite. Infections the second one is the subject of a separate paper (Kristmundsson were commonly intense. Identical developmental forms were also et al., 2011). Due to abnormal conditions of queen scallops off found in both queen scallops (detection frequency 40%) and king the Faroe Islands at that time, a Faroese company in the Scallop scallops (90%) from Scottish waters, but infections were very light fishery industry requested an observation of the scallops with re- in all cases. gard to diseases. In addition, queen- and king scallops from Scot- tish waters were sampled at a later stage and examined to further check the geographic distribution of the parasites. 3.1. Fresh mount observations Various types of large cysts at different developmental stages 2. Materials and methods are present in the adductor muscle. Their size and outer and inner morphology is quite variable. Thin walled elongated cysts, 2.1. Scallop collection 320 ± 50 lm  75 ± 25 lm(n = 10) (Fig. 2a), with granular cyto- plasm are common. Sometimes, these have membranous protru- Live Iceland scallops from two locations in the Bay of Breidafjör- sions at each end. In other cases, similar cysts contain a clear dur were sampled in November 2002 (n =2 30; size 3.0–9.0 cm). area, which resembles a formation of spindle apparatus,
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