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Aggregata Octopiana (Apicomplexa: Aggregatidae) from Octopus Vulgaris Off NW Spain

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Aggregata Octopiana (Apicomplexa: Aggregatidae) from Octopus Vulgaris Off NW Spain DISEASES OF AQUATIC ORGANISMS Published December 12 Dis Aquat Org Aggregata octopiana (Apicomplexa: Aggregatidae) from Octopus vulgaris off NW Spain J. Estevez, S. Pascual, C. Gestal, M. Soto, H. Rodriguez, C. Arias* Laboratorio de Parasitologia, Facultad de Ciencias del Mar, Universidad de Vigo, Ap. 874, E-36200 Vigo, Spain ABSTRACT: Gamogony and sporogony of Aggregata octopiana were commonly observed during histological examination of the digestive tract and the connective tissue sheath of wild Octopus vulgaris (Cuvier, 1798) from hade Vigo (NW Spain). In massive infections, numerous oocysts were found in the muscular tissue. KEY WORDS: Apicomplexa . Aggregata octopiana . Octopus vulgaris INTRODUCTION or fixed in 10 % buffered formalin, embedded in paraf- fin and sectioned using a Microm HM-340 E micro- Coastal octopus have the longest history of human tome (Microm, Walldorf, Germany). Sections (4 to 5 pm) exploitation of any cephalopod (Boyle 1990). The best were stained with haematoxylin-eosin (Culling et known species, Octopus vulgaris Cuvier, 1798, is ex- al. 1985). Measurements of parasitic gamogonal and tremely important in fisheries (Roper et al. 1984).It also sporogonal stages was made using an ocular micro- represents a major protein resource in most Mediter- meter and are expressed in micrometers as ranges ranean countries (Guerra 1992) and is widely used as a followed by the mean and standard deviations in bion~edicalresearch model (Hanlon & Forsythe 1985). parentheses (n = 30). The number of sporocysts was Despite their importance, little information is avail- determined from each individual oocyst by using a able on protozoan-related diseases occurring in wild Burker chamber. Terminology employed for parasitic populations, even in the common Octopus vulgaris. A stages follows Hochberg (1983). notable exception is the coccidian Aggregata Frenzel, 1885 (Apicomplexa: Aggregatidae), which has been reported in the digestive tract of 13 octopus species RESULTS worldwide (Sardella & Re 1988, Hochberg 1990, Poyn- ton et al. 1992). Description of life cycle stages of This paper reports the first description of an apicom- Aggregata octopiana in Octopus vulgaris plexan of the genus Aggregata in Octopus vulgaris from eastern North Atlantic temperate waters. Gamogony. The development of microgamonts was characterized by extensive cytoplasmic membrane folding, cytoplasmic partioning and an increase in the MATERIALS AND METHODS number of peripheral nuclei. Scores to thousands of flagellated microgametes were produced (Fig. 1). Between November 1994 and February 1995,30 wild Macrogamonts became macrogametes after a series octopus were captured in artisanal gear by local fisher- of nuclear changes (Poynton et al. 1992). Macroga- men from the Ria of Vigo (NW Spain). Tissues were metes possessed foamy cytoplasm and a nucleus, con- excised from diverse regions of the digestive tract. taining a compact or ring-like nucleolus (Fig. ID). Then, fresh material was examined by phase contrast Both nlicrogametes and macrogametes were sur- .- -. rounded by a pale homogenous area representing a 'Addressee for correspondence. E-mail: [email protected] parasitophorous vacuole. O Inter-Research 1996 Resale of full article not pernutted ursoa pue u!~Axolemaq~IIM pau!ws url sz = Jeq aless '(1(3)urseldo~ds dweoj pue snloapnu snons~dsuos'(U) snapnu Juluassa qlrM a~awef~oise~((a )urI oz = l~qaless .pauloj d~alalduros(lw) salawe601s!y\r (3)-wrl c = leq apss .(U) !qsnu 1e.rayduad pue (.<S)urse~do~ls pauo~~~r~d ay1 6u1~oys (Bu) luoua6ols!u JO uog~od(g] wrl oz = ~eqaless .aueIquau ~!urs~rdolAsay1 JO Bu~p[oja/i!sualxa Aq pu::!lalseleqs luoure6 -0~21~~(v).salaure6o~sy1 jo uoqeuloj ay1 ur saBels an1ssss~ng(3 01 v)-sr.reBpn sndopo y .1uoijome3 .~uerdoi~oeje6ar66~ 61j Estevez et al.. Aggregata octopiana In Octopus vulgans Fig. 2. Aggregata octopiana. Sporogony in Octopus vulgaris. (A) Sporont showing extensive folding of cytoplasmic membrane, and numerous nuclei at the periphery of the partitions. Scale bar = 25 pm. (B) Sporont segregating into uninucleate sporoblasts (Sb). Scale bar = 10 pm. (C) Immature sporocysts (arrows).Scale bar = 10 pm. (D) Oocyst containing mature sporocysts (Sc) with sporozoites (Sz). Ow: Oocyst wall. Scale bar = 10 pm. Stained with hematoxylin and eosin Dis Aquat Org 27: 227-231. 1996 Fig. 3. Aggregata octopiana in Octopus vulgaris. Fresh microscopic examination of squash preparation, with phase contrast illu- mination. (A) Isolated sporozoites of A. octopiana. Scale bar = 10 pm. (B) Sporocysts of atypical size 'giants' containing from 20 to 26 sporozoites. Scale bar = 10 pm Sporogony. The union of a mjcrogamete and macro- and 60 000. Approximately 10% of the oocysts ex- gamete produced a zygote, which then became an amined possessed one or more atypically sized sporo- early sporont that was characterized by cell membrane cysts ('giants') (Fig. 3B) with diameters of 23 to 32 pm folding and alignment of numerous nuclei on the sur- (28.83 + 2.73) containing 20 to 26 sporozoites of sizes face of the partitioned cytoplasm (Fig. 2A). Individual 27.5 to 31.5 pm (29.83 + 1.44) long by 2.75 to 3.5 pm nuclei with accompanying cytoplasm later budded (2.97 rt 0.23) wide. off, forming uninucleate spherical sporoblasts (Fig. 2B). The development of sporoblast into sporocyst was characterized by an increase in the number of nuclei, Prevalence and site of infection and the further partitioning of nuclei and cytoplasm formed sporozoites (Fig. 2C, D). In fresh preparations, Routine histological examination of the digestive the sporocysts were spherical in shape, 11 to 15 pm tracts of wild Octopus vulgaris from NW Spain demon- (13.34 & 1.63) in diameter, and possess a smooth sur- strated that gamogony and sporogony were present in face and a residual body. The sporocysts, which were all specimens examined (prevalence loo%), most fre- composed of 2 equal halves joined together by a equa- quently in the digestive tract. The highest percentage torial suture, opened at the suture, and released the of infection was found in spiral caecum, intestine, crop, sporozoites. The number of sporozoites for both fresh digestive gland, oesophagus and connective tissue and sectioned material ranged from 6 to 12 per sporo- sheath. In one case of massive infection we also found cyst. They were arranged in a spiral fashion inside the oocysts of Aggregata octopiana in the muscle tissue. sporocyst with all nuclei at one pole. Isolated sporo- zoites were 16 to 23.5 pm (19.77 * 2.46) long by 2 to 2.5 pm (2.18 2 0.25) wide (Fig. 3A). DISCUSSION Oocysts were mainly oval but sometimes almost spherical in morphology and ranged in size from 200 Several authors (Sprague & Couch 1971, Levine to 1050 pm (612.5 * 316.75) In length by 150 to 700 pm 1985, 1988) have suggested that most species of (402.5 + 155.99) in width. Multiple sporocysts were Aggregata in Europe require redescription to deter- found within each oocyst, numbering between <l000 mine their validity. Synonymy-related problems have Table 1. Aggregata octopiana. Comparative data on morphology and dimensions of coccidia in Octopus vulgaris Sporocysts (Sc) Sporozoites Reference Surface Diameter (pm) Number/Sc Length (pm) I Smooth 12-15 9-16 7 Moroff (1908) 20 16 ? Wurmbach (1935) 12-15 8-16 25-30 Hochberg (1990) Smooth 11-15 6-12 16-23.5 Present study I Estevez et a1 : Aggregata octoplana in Octopus vulgans surfaced because Aggregata species have usually LITERATURE CITED been differentiated on the basis of host, size and sur- face appearance of sporocysts, and number and length Boylc PR (1990) Ccphalopod biology in the fishenes context. FIS~R?s 8-303-321 of sporozoites. With these diagnostic characters, Culllng ('F!\, Allison RT, Barr WT (1985) Cellular pathology Hochberg (1990) and Poynton et al. (1992) recognize technique Butterworth & CO,London 6 species of the genus Aggregata that are associated Dobell (' (1925) The llfe-history and chromosome cycle of with cephalopod hosts: A. eberthi in Sepia officinalis Aggregata eberthl (Protozoa Sporozoa: Coccidia). Para- sitology 17 1-136 (Dobell 1925),A. kudoi in S. elliptica (Narasimhamurti Estcvei. J, Iglesias R, Lelro J, Ubeira FM, Sanmartin ML 1979),A. dobelli and A. millerorum in Octopus dofleini (1992) An unusual site of infection by a microsporean in and 0.bimaculoides respectively (Poynton et al. 1992), the turbot Scophthalmus maximus Dis Aquat Org 13: and A. octopiana and A, splnosa in 0. vulgaris (Moroff 139-142 1908). Guerra A (1992) Mollusca, Cephalopoda. In Ramos MA (eds) Fauna Ibenca, Vol. 1 Museo Nacional de Ciencias Natu- The characteristic morphological features of our rales CSlC, Madrid species of Aggregata resemble those of the group Hanlon RJ, Forsythe JW (1985) Advances in the laboratory formed by A. octopiana (Moroff 1908, Wurmbach 1935, culture of Octopus for biomedical research. Lab Anim Sci Hochberg 1990) (Table l),all having similar gamogo- 35(1):33-40 Hochberg FG (1983) Parasites of cephalopods: a review. Mem nal and sporogonal stages. Both the diameter measure- Natl Mus Victoria 44:109-145 ments of the sporocyst and the number of sporozoites Hochberg FG (1990)Diseases of Mollusca Cephalopoda. Dis- were close to those described previously for this spe- eases caused by protistans and metazoans. In: Kinne 0 cies. Sporozoite length, however (16 to 23.5 pm), was (ed) Dlseases of manne animals, Vol. 111. Biologische less than the length described by Hochberg (1990) Anstalt Helgoland, Hamburg, p 47-202 Levine ND (1985) Phylum 11. Apicomplexa Levine. 1970. In: (25 to 30 pm), but this may be explained by the pres- Lee JJ, Hutner SH, Bovee EC (eds)An illustrated guide to ence of abnormally sized 'giant' sporocysts, found in the Protozoa Society of Protozoologists, Lawrence, KS, 10% of the oocysts examined, measuring 27.5 to 31.5 pm p 322-374 in diameter. The occasional presence of giant sporo- Levine ND (1988)The protozoan Phylum Apicomplexa, Vol I CRC Press, Boca Raton, FL cysts had previously been observed by Dobell (1925rin h4oroff T (1908) Die bei den Cephalopoden vorkommenden A.
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