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Coccidian (Apicomplexa) parasite infecting Strombus gigas Linne, 1758 digestive gland.

ABSTRACT This study reports on a new parasite of the digestive gland of the queen conch, Strombus gigas. An intense and generalized sporozoan infection was detected during a reproductive study of S. gigas in San Andres island (Colombia). The parasite was found in the digestive gland of every sampled S. gigas, with a heavy intensity of infection (invasion of every cell) in many animals. The infection of the digestive gland began in the cryptic cells and later secretory cells were also infected, giving way to discharge of sporocysts to the stomach through the digestive gland ducts. Apicomplexa-like trophozoites were embedded in the digestive gland epithelial cells and attached to host cell wall by their conoid end. Several stages were detected: trophozoites, sporocysts, and gamonts containing macrogametes or microgametes. Given the presence of multiple stages at the same time, the entire life cycle of the parasite is assumed to occur within the same host and tissue. The taxonomic position of the parasite should be ascertained by DNA analysis.

KEY WORDS: Strombus gigas, Coccidiasis, Apicomplexa, parasite, queen conch

INTRODUCTION

Given the regional importance of Strombus gigas Linne, 1758 in the Caribbean, and the critical state of some of its populations (Appeldoorn 1987, Aldana Aranda et al. 2003a), different research programs have been undertaken to understand its populations dynamics and reproductive biology (Reed 1995a, Reed 1995b, Aldana Aranda et al. 2003b, Aldana Aranda et al. 2003c, Aldana Aranda et al. 2003d, Delgado et al. 2004, Castro et al. 2005). It was during the reproduction study that the presence of a parasite was detected in the digestive gland of a S. gigas population.

Apicomplexa parasites are a common occurrence in invertebrates and especially in Molluscs (Lester & Davis 1981, Hillman et al. 1982, Perkins 1988, Duszynski et al. 1999, Duszynski et al. 2004). Here we identify various stages of a new Apicomplexa-like parasite, from the digestive gland of S. gigas. This parasite is apparently affecting the reproductive potential of this host (Baqueiro Cardenas et al. 2005).

MATERIAL AND METHODS

Queen conchs were sampled at San Andres island (Colombia) in the southern Caribbean sea for histological study of the reproductive cycle. Thirty organisms were sampled monthly during a whole year; all of them were adults with a shell lip over 6 mm thick. A slice including digestive gland (DG) and gonad (G) was fixed in 10% formalin in sea water, and then processed through standard histological techniques (Gabe 1968). Sections were stained with Goldner trichrome method (in Gabe 1968), modified by including Alcian blue at pH 2.5 to stain the proteoglycans, to reveal molluscan secretions (personal modification). Digital images were taken with a Sony CCD-IRIS video-camera mounted on the Carl Zeiss microscope or a Nikon DXm 1200F digital camera mounted on the Nikon microscope.

RESULTS

The digestive gland is composed of an array of tubules connected by small ducts to larger ducts, which connect to the stomach. Digestive tubules are constituted by two cell types: secretory ceils (Sc) characterized by large granules stained by Alcian blue and crypt cells (Cc) characterized by vacuolar cytoplasm (Fig. 1a, b). Infection starts within the crypt cells of the digestive gland (Fig. 2a), and later may also infect the secretory cells (Fig. 2c). Physiological apocrine secretion gives rise to an abundant duct granular content devoid of parasites when the secretory cells are not invaded (Fig. 2b) and with several cysts when they are invaded (Fig. 2d). The various stages of the parasitic organisms were pigmented in light to dark brown and black without any histological staining. Moreover, the pigment appeared to be partially washed away by the fixative.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Apicomplexa-like, bottle shaped trophozoites, 25-30 [micro]m long and 15-20 [micro]m wide, with conic apical structure were found within infected cells (Fig. 3a, b). The apical structure was implanted in the cellular wall (Fig. 3b). These trophozoites become cysts (Fig. 3c). Sporocysts (Fig. 3d), 15[micro]m in diameter with a thick wall are the most frequent stages whereas thin walled gamonts (Fig. 4b, c) producing macrogametes or microgametes were uncommon. An oocyst with a single trophozoite was also observed (Fig. 4d) in the digestive gland of S. gigas and dark microspores have also been identified in the cell cytoplasm (Fig. 4b, c). All the stages usually occur inside the crypt cells but also, less frequently, inside the secretory cells.

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

DISCUSSION

The digestive gland tubules of S. gigas are composed of two cell types as described for other Molluscs but they are not similar to those described for other prosobranch species (Voltzow 1994). Unlike the small triangular cells reported from most prosobranchs, the crypt cells of S. gigas are large vacuolar cells, which are often infected by various stages of an intracellular parasitic protist. However, the intensity of infection in the digestive gland varies between individual S. gigas. The presence of this parasite in the lumen of the digestive gland ducts is much more variable, and corresponds to the intensity of the infection and discharge cycle of the secretory cells.

The constant presence of cysts all the year round implies that infection is permanent. The presence of spore-producing cysts and these spores infecting healthy cells in the same animal is interpreted as evidence of self reinfection. Some Apicomplexa have a complex life cycle, including various hosts, but for others, the whole life cycle takes place within the same host (Duszynski et al. 2004). The intracellular characteristic of the infection, the presence of an apical feeding structure in the trophozoite, and stages indicative of macro and microgamonts and sporocyst suggest that this parasite may be a Coccidia. Figure 4a and 4d appear similar to stages of Nematopsis sp.. No reference has been found of such large intracellular trophozoites similar only to parasites of the family Eimeridae. However, parasites of this family are often characterized for having more than one host (Bower 2001). The taxonomic position of this parasite should be ascertained by electron microscopy studies and DNA analysis.

In S. gigas, auto infection is evident from the presence of bursting cysts of all stages within the digestive gland epithelial cells. The first parasitic invasion may be self sustainable and evacuation of parasites with the feces may be responsible for the reinfection of whole population. Then, the extent of digestive gland tubules destruction within the digestive physiological cycle increases the number of parasites that may be exported to the stomach and gut via the digestive ducts.

The presence of such high prevalence and intensity of infection and its coincidence with reduced reproductive activity (Baqueiro et al. 2005), raises several questions: What are the environmental factors inducing such an intense and generalized infection? What is the geographic extension of the infection and its putative impact on recruitment and long term health of impacted populations? Is it really a disease? And last but not least, what is the putative danger of transmission to natural predators and humans when the queen conchs are eaten raw?

ACKNOWLEDGMENTS

Project No. 003/april, 2003 (SAI, Colombia and Laboratorio de Biologia y Cultivo de Moluscos CINVESTAV-IPN, Merida, Mexico). Project CONACYT--SAGARPA-2002-C01-1530. The authors thank Erick Castro for sampling of conchs, to Ichthyology laboratory of CINVESTAV-IPN, Merida for its support for histology processing, Teresa Colas for help in histological techniques and digital images, and the anonymous reviewers for their very helpful comments.

LITERATURE CITED

Aldana Aranda, D., E. Baqueiro Cardenas & S. Manzanilla Naim. 2003a. Mexican marine parks as a fishery management tool for the queen conch Strombus gigas. In: D. Aldana-Aranda, editor. El caracol Strombus gigas: conocimiento integral para su manejo sustentable en el Caribe, Mexico. Espana: CYTED. pp. 101-108.

Aldana-Aranda, D., E. R. Baqueiro-Cardenas, I. Martinez-Morales, R. I. Ochoa & T. Brule. 2003b. Reproductive Patterns of Strombus gigas from Alacranes Reef versus Chinchorro Bank of Mexico. Gulf and Caribbean Fisheries Institute 54:202-225.

Aldana-Aranda, D., E. R. Baqueiro-Cardenas, I. Martinez-Morales, A. Zetina-Zarate & T. Brule. 2003c. A review of the reproductive patterns of gastropods mollusks from Mexico. Bull. Mar. Sci. 73:629-641.

Aldana-Aranda, D., E. R. Baqueiro-Cardenas, I. Martinez-Morales, R. I. Ochoa & T. Brule. 2003d. Gonad behavior during peak reproduction period of Strombus gigas from Banco Chinchorro. Bull. Mar. Sci. 73:241-248.

Appeldoorn, R. S. 1987. Considerations and preliminary calculations of maximum sustainable yield for the queen conch (Strombus gigas) resource of Puerto Rico and the U.S. Virgin Islands. Rep. Caribb. Fish. Manage. Counc. Dec.:1-20.

Baqueiro Cardenas, E., L. Frenkiel & D. Aldana Aranda. 2005. One more threat for the Queen conch Strombus gigas: coccidian (Apicomplexa) infection of S. gigas digestive gland (preliminary results). Gulf and Caribbean Fisheries Institute 58:17-18.

Bower, S. M. 2001. Synopsis of infectious diseases and parasites of commercially exploited shellfish: kidney coccidia of clams. URL: http:// www.pac.dfo-dfo-mpo.gc.ca/sci/shelldis/pages/kidcocc_e.htm Castro, E., L. Frenkiel, E. Baqueiro & D. Aldana Aranda. 2005. Atypical reproductive cycle of the queen conch Strombus gigas (Mollusca: Gastropoda). Gulf and Caribbean Fisheries Institute (in press).

Delgado, G. A., C. T. Bartels, R. A. Glazer, N. J. Brown-Peterson & K. J. McCarthy. 2004. Translocation as a strategy to rehabilitate the queen conch (Strombus gigas) population in the Florida Keys. Fish. Bull. (Wash. DC) 102:278-288.

Duszynski, D. W., S. J. Upton & L. Couch. 1999. Coccidia (Eimeria and Isospora) of Invertebrates. USA: University of New Mexico: Department of Biology. (Supported by NSF-PEET DEB 9521687). http://biology.unm.edu/biology/coccidia/invert.html (14/03/2007).

Duszynski, D. W., S. J. Upton & L. Couch. 2004. The Coccidia of the World USA: University of New Mexico: Department of Biology. (Supported by NSF-PEET DEB 9521687) http://biology.unm.edu/ biology/coccidia/table.html (14/03/2007).

Gabe, M. 1968. Technique histologique Masson, Paris. 1168 pp.

Hillman, R. E., N. J. Maciolek, J. I. Lahey & C. I. Belmore. 1982. Effects of haplosporidian parasite, Haplosporidium sp. on species of the molluscan woodborer Teredo in Barnegat Bay, New Jersey. J. Invertebr. Pathol. 40:307-319.

Lester, R. J. F. & G. H. Davis. 1981. A new Perkinsus species (Apicomplexa, Perkinsea) from the abalone Haliotis rubber. J. Invertebr. Pathol. 37:208-209.

Perkins, O. F. 1988. Parasite morphology, strategy and evolution. In: W. S. Fisher, editor. Disease Processes in Marine Bivalve mollusks. US: American Fisheries Soc. Special Publication 18. pp. 93-111.

Reed, S. E. 1995a. Reproductive anatomy and biology of the genus Strombus in the Caribbean: I. Males. J. Shelfish Res. 14:325-330.

Reed, S. E. 1995b. Reproductive anatomy and biology of the genus Strombus in the Caribbean: II. Females. J. Shellfish Res. 14:331-336.

Voltzow, J. 1994. Gastropoda: Prosobranchia. In: F. W. Harrison & A. J. Kohn, editors. Microscopic anatomy of invertebrates, Vol 5, Mollusca I. New York: John Wiley and Sons Ltd. pp. 111-252.

ERICK BAQUEIRO CARDENAS, (1) LILIANE FRENKIEL, (2) ADRIANA ZETINA ZARATE (3) AND DALILA ALDANA ARANDA (3) *.

(1) CICATA IPN Altamira, Mexico, Km 14.5 Carr. Tampico--Puerto Ind. Altamira, Corredor Industrial, Altamira, Tamaulipas, Cp. 89600, Mexico; (2) Archipel des Sciences, Lamentin, Guadeloupe, FWI, France; (3) CINVESTAV IPN Unidad Merida, laboratorio de Biologia y Cultivo de Moluscos, Merida Yucatan Mexico

* Corresponding author. E-mail: daldana@mda.cinvestav.mx
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Author:Cardenas, Erick Baqueiro; Frenkiel, Liliane; Zarate, Adriana Zetina; Aranda, Dalila Aldana
Publication:Journal of Shellfish Research
Geographic Code:3COLO
Date:Aug 1, 2007
Words:1843
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