Aldana Aranda, D.

Gros, O.

Volland, J-M.

Aquatic Commons

 Proceedings of the 61st  Gulf and Caribbean Fisheries Institute     November 10 - 14, 2008   Gosier, Guadeloupe, French West Indies 
Detection of Apicomplexa like Parasites in Two Species Belonging to the Family Strombidae: 
Strombus gallus, Linnaeus, 1758 and S. raninus, Gmelin, 1791. 
 
JEAN-MARIE VOLLAND1, DALILA ALDANA ARANDA2, and OLIVIER GROS1 
1UMR-CNRS 7138, SAE, Equipe « Symbiose ». Université des Antilles et de la Guyane. UFR des Sciences Exactes et 
Naturelles, Département de Biologie. B.P. 592. 97159. Pointe-à-Pitre Cedex, Guadeloupe. France 
2CINVESTAV IPN Unidad Mérida, laboratorio de Biología y Cultivo de Moluscos, Merida Yucatan, Mexico 
 
ABSTRACT 
The present study aims to detect the presence of intracellular Apicomplexa in two species of the genus Strombus: Strombus 
gallus and S. raninus.  This parasitic interaction was initially described in S. gigas and extends to both other species of Strombidae 
studied.  Such relationships could occur in the whole Strombidae family.  Further investigations will focus on strombid species from 
other geographic areas to confirm this hypothesis.  Complementary investigations are also scheduled to ascertain the nature of 
relationship between Apicomplexa and the family Strombidae.  
 
KEY WORDS:  Apicomplexan parasite, Caribbean conchs, structure  
 
Puesta en Evidencia de Présencia del Parasito Apicomplexes en dos Especies de la Famillia des 
Strombidae: Strombus galas, Linnaeus, 1758 y S. raninus, Gmelin, 1791 
 
El estudio de la glándula digestiva de S. gigas puso en evidencia la presencia de una infección importante y generalizada. Una 
cantidad importante de estructuras de tipo Apicomplexa fueron detectadas en las células vacuolares de los túbulos digestivos de 
todos los individuos muestreados.  En este estudio, se analizó la glándula digestiva de dos otros Strombidae del Caraïbe: S. gallus y 
S. raninus.  Las glándulas digestivas de los organismos fueron fijadas y el análisis estructural fue realizado con técnicas de histología 
y de microscopia electrónica y a transmisión.  Para las dos especies, los tùbulos digestivos se componen de tres tipos celulares: 
células digestivas, células vacuolares y células crípticas.  Este estudio puso en evidencia la presencia de estructures semejantes a los 
Apicomplexa, parecidos a lo observado en S. gigas, en las células vacuolares de S. gallus y S. raninus.  Para las dos especies, los 
estadios del desarrollo característico del ciclo de vida de los Apicomplexa fue observado:  El estadio trofozoïto (caracterizado por su 
compleja estructura apical), el estadio esporozoïto (con sus esporas internas) y el estadio gamont (caracterizado por una pared fina).  
Los parásitos de S. gallus midieron de 10 à 20 µm de diámetro y los de S. raninus en promedio fueron dos veces más grandes.  Así, 
los dos Strombidae analizados tuvieron la presencia de parásitos que nos recuerdan a los Apicomplexa.  Sin embargo, ningún 
síntoma de mala salud como incipiente desarrollo gonádico o desorganización de los túbulos digestivos fueron observados.  Este 
estudio puso en evidencia que la infección descrita inicialmente en S. gigas, se presenta también en otras dos especies del mismo 
genero Strombus. 
 
PALABRAS CLAVES:  Apicomplexan parásito, caracol, estructura  
 
Mise en Évidence de la Présence de Parsites Apicomplexes chez deux Éspecies de la Famille des 
Strombidae: Strombus gallus, Linnaeus, 1758 et S. raninas, Gmelin, 1791 
 
L’étude de la glande digestive de S. gigas a révélée la présence d’une infection importante et généralisée. Une quantité 
importante de structures rappelant les Apicomplexes a été détectée dans les cellules vacuolaires des tubules digestifs de tout les 
individus échantillonnés.  Dans cette étude, nous avons analysé la glande digestive de deux autres Strombidae de la Caraïbe : S. 
gallus et S. raninus.  Les glandes digestives des individus ont été fixées et des analyses structurelles ont été réalisées en faisant appel 
aux techniques d’histologie et de microscopie électronique à transmission.  Pour les deux espèces, les tubules digestifs se composent 
de trois types cellulaires : les cellules digestives, les cellules vacuolaire et les cellules cryptiques.  Notre étude a mis en évidence la 
présence de structures rappelant des Apicomplexes, semblables à celles observées chez S. gigas, dans les cellules vacuolaires de S. 
gallus et S. raninus.  Pour les deux espèces, les stades de développement caractéristiques du cycle vital des Apicomplexes ont été 
observés : le stade trophozoïte (caractérisé par son complexe apical), le stade sporozoïte (avec ses bourgeonnements internes) et le 
stade gamonte (caracterisé par une paroi fine). Les parasites de S. gallus font de 10 à 20 µm de diamètre et ceux de S. raninus sont 
en moyenne deux fois plus gros.  Ainsi, les deux Strombidae analysés ont révélés la présence de parasites rappelant les Apicom-
plexes.  Cependant, aucun signe de mauvaise santé tel qu’un retard de développement de la gonade ou une désorganisation des 
tubules digestifs n’a été observé. Cette étude a donc mis en évidence que l’infection décrite initialement chez S. gigas, s’étend à 
deux autres espèces du même genre.  
 
MOTS CLÉS:  Parasite Apicomplexe, lambis, structure 
INTRODUCTION 
The five common species of the Strombus genus in the 
Caribbean are: Strombus costatus (Gmelin, 1791), S. gallus 
(Linnaeus, 1758), S. gigas (Linnaeus, 1758),  S. pugilis 
(Linnaeus, 1758) and S. raninus (Gmelin, 1791).  Some of 
them are consumed (S. costatus, S. gigas, and S. pugilis) in 
various countries; however, S. gigas is the only species 
fished throughout the region and object of international 
trade.  Previous observations of S. gigas digestive gland 
have shown several foreign structures in the population of 
Page 504  61st Gulf and Caribbean Fisheries Institute  
 
San Andres Archipelago (Colombia).  These structures 
have been defined as parasitic belonging to the Apicom-
plexa group (Baqueiro-Cárdenas et al. 2005, 2007, Gros et 
al. 2009).   Apicomplexa is a group of Sporozoa containing 
about 5,000 species, all described as parasites.   They are 
characterized by a complex life cycle composed of three 
phases: merogony (asexual reproduction), gametogony 
(sexual reproduction), and sporogony (asexual reproduc-
tion).  Infecting units, formed by the second asexual 
reproduction are called trophozoits.  This stage is charac-
terized by an apical complex (Perkins 1991).  
This study focuses on two Caribbean Strombidae: S. 
gallus and S. raninus.  
 
MATERIALS AND METHODS 
Individuals of S. gallus and S. raninus were collected 
from Guadeloupe (FWI) on Thalassia testudinum seagrass 
beds.  Living materials were brought to the laboratory for 
analysis.  The digestive glands were dissected and fixed in 
5% glutaraldehyde and 2% paraformaldehyde in sea water 
overnight at 4°C.  Samples were then dehydrated through 
an ascending ethanol series and embedded either in 
paraplast wax for histology (5µm thick sections) or in 
epoxy resine for semi thin sections (0.5µm thick) according 
to standard methods.  Histological sections were stained 
using a trichrome  staining (hematoxylin, alcian blue, and 
acid fuchsine).  Semi thin sections were stained using 
toluidine blue in borax.  Thin sections were obtained from 
samples embedded in epoxy resin and contrasted with 
uranyl acetate and lead citrate before observation in a Leo 
912 transmission electronic microscope (TEM). 
 
RESULTS 
The digestive gland of both species was composed by 
an assemblage of digestive tubules and ducts. Digestive 
tubules epithelium was composed by three cell types: long 
and columnar digestive cells, vacuolated cells and smaller 
triangular cells identified as crypt cells (Figures 1, 2).   
Digestive gland of S. gallus and S. raninus was 
infected by a large number of putative Apicomplexa-like 
organisms. For each species, Apicomplexa-like parasites 
occur most frequently in vacuolated cells (Figres 1 - 3, 6) 
but were also found in the lumen of tubules and in the 
collector ducts of the gland (not shown).  Sporocysts are 
spherical to ellipsoidal, they are always included in a 
parasitophorus vacuole.  Their diameter is comprised 
between 10 and 30 µm (21 µm on average) in S. gallus and 
between 20 and 50 µm (36 µm on average) in S. raninus 
with a thick, hard wall which is often damaged by section-
ing (Figres 5, 8).  Three different stages of Apicomplexa 
life cycle were usually observed in the digestive gland. The 
most frequent is the sporocyst stage with a thick wall 
described above (Figures 5, 8).  Some thin walled stages 
may be considered as gamont.  Last but not least, typical 
bottle shaped organisms were observed.  This morphotype 
could be assimilated to the trophozoite stage, because of 
the presence of an apical complex characteristic of this 
stage and of the Apicomplexa group (Figures 4, 7).  
 
DISCUSSION 
Apicomplexa have already been described in several 
molluscan species: Nematopsis gigas is a parasite of Nerita 
ascencionis (Azevedo and Padovan 2004).   Pseudoklossia 
haliotis is a parasite of Haliotis spp (Friedman et al. 1995). 
Similar morphotypes as those observed here (thick walled 
sporocysts, thin walled gamonts, and trophozoits) have 
previously been described as different stages of Apicom-
plexa life cycle (Perkins 1991).  
We emphasize that the parasitic interaction described 
in S. gigas extends to both other species of Strombidae 
studied.  Such relationship could occur in the whole 
Strombidae family.  Further investigations will focus on 
strombid species from other geographic areas to confirm 
this hypothesis.  Previous studies have highlight the 
presence of the Apicomplexa-like parasites in the digestive 
gland of all S. gigas sampled individuals (n > 1000 for S. 
gigas) from different Caribbean sites (Baqueiro-Cárdenas 
et al. 2005, 2007, Gros et al. 2009).  We add two other 
species at the list of infected Strombidae: S. gallus and S. 
raninus.  This suggests to re-evaluate the assumption of 
parasitism, and we propose to consider the possibility of a 
non-virulent relationship like commensalisms or even 
mutualism. 
Phylogenetic analysis is in progress in our laboratory 
in order to confirm that these Apicomplexa-like structures 
belong to the Apicomplexa group.  Moreover, physiologi-
cal studies should be performed to clearly determine the 
nature of the interaction between conchs and their Apicom-
plexa-like. 
 
LITERATURE CITED 
Azevedo, C. and I. Padovan.  2004.  Nematopsis gigas  sp. 
(Apicomplexa), a parasite of Nerita ascencionis (Gastropoda, 
Neritidae) from Brazil. Journal of Eukaryotic Microbiology 51
(2):214-219 
Baqueiro-Cárdenas, E., L. Frenkiel, and D. Aldana Aranda.  2005.  One 
more threat for the Queen conch Strombus gigas? Coccidian 
(Apicomplexa) infection of S. gigas digestive gland: preliminary 
results. Proceedings of the Gulf Caribbean Fisheries Institute 
58:421-426 
Baqueiro-Cárdenas, E., L. Frenkiel, A. Zetina Zarate, and D. Aldana 
Aranda.  2007.  Coccidian (Apicomplexa) parasite infecting 
Strombus gigas linné, 1758 digestive gland. Journal of Shellfish 
Research 26(2):319-321 
Friedman, C.S., G.R. Gardner, R.P. Hedrick, M. Stephenson, R.J. 
Cawthorn, and S.J. Upton.  1995.  Pseudoklossia haliotis sp. n. 
(Apicomplexa) from the kidney of california abalone, Haliotis spp. 
(Mollusca). Journal of Invertebrate Pathology 66(1):33-38 
Gros, O., Frenkiel, L., and D. Aldana Aranda.  [2009].  Structural analysis 
of the digestive gland of the Queen conch Strombus gigas 
(Linnaeus, 1758) and its intracellular Apicomplexa parasites. 
Journal of Molluscan Studies [In press] 75(1).  
Perkins, F.O.  1991.  "Sporozoa": Apicomplexa, Microsporidia, 
Haplosporidia, Paramixea, Myxosporidia, and Actinosporidia. Pages 
261-331 in: F.W. Harrison (Ed.) Microscopic Anatomy of 
Invertebrates. Volume 1 Protozoa. FW Harrison and Corliss New 
York, Chichester, Brisbane, Toronto, Singapore 
   Volland, J. - M. et al.    GCFI:61   (2009) Page 505 
 
Figures 1-8 .   Observations of S. gallus and S. raninus digestive gland.  
1-2: Histological observation of S. raninus (1) and semi-thin section of S. gallus (2) digestive gland showing digestive 
tubules mostly composed by digestive cells (DC). Parasites (arrows) are grouped in vacuolated cells (VC) between 
digestives cells. They are often damaged by sectioning. CC: crypt cells. L: lumen of the tubule. 3: TEM views of S. raninus 
digestive gland showing Apicomplexa-like parasites in vacuolated cells. Note the presence of two crypt cells interspersed 
with vacuolated cells. 4-5: TEM view of S. raninus digestive gland showing a trophozoite (4) characterized by the presence 
of an apical complex (double arrow) and a sporocyst (5) with its inner budding. 6: TEM view of S. gallus digestive gland. 
Note the presence of different life stages (trophozoite: T and sporocyst: S) in vacuolated cells. 7-8: TEM detail of S. gallus 
trophozoite (7) and sporocyst (8). 


Detection of Apicomplexa like parasites in two species belonging to the Family Strombidae: Strombus gallus, Linnaeus, 1758 and S.raninus, Gmelin, 1791

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Detection of Apicomplexa like parasites in two species belonging to the Family Strombidae: Strombus gallus, Linnaeus, 1758 and S.raninus, Gmelin, 1791

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