Aldana Aranda, D.

Baqueiro Cárdenas, E.

Frenkiel, L.

Aquatic Commons

One More Threat for the Queen Conch Strombus gigas? 
Coccidian (Apicomplexa) Infection of S. gigas Digestive Gland: Preliminary Results 
 
ERICK BAQUEIRO CÁRDENAS1, LILIANE FRENKIEL2, and DALILA ALDANA ARANDA3 
1CICATA IPN  
Altamira, Mexico,  
2Archipel  des Sciences 
Guadeloup, French West Indies, France 
3 CINVESTAV IPN Unidad Mérida 
Laboratorio de Biología y Cultivo de Moluscos,  
Km 6 antigua carretera a Progreso 
C.P. 97310. Mérida, Yucatán, México 
 
ABSTRACT  
An intense and generalized sporozoan infection was detected during reproductive studies of Strombus gigas popula-
tions from various localities of the Caribbean.  The parasite, apparently a Coccidian, was found in the digestive gland (DG) 
of every sampled organism throughout the year, infecting from 70% to 100% of the DG alveoli, with a frequent total 
invasion of every alveolar cell.  This infection is apparently responsible for the low intensity of maturity and spawning 
stages registered at San Andres Archipelago, Colombia, and Alacranes reef, Mexico.  These findings induce several 
questions: Given the generalized infection of the two populations at so distant sites, if the parasite is the same, are S. gigas 
populations more connected than it is supposed?  What are the environmental factors inducing such an intense and general-
ized infection?  What are the life cycle, vectors, and intermediate hosts of this parasite?  Is it a threat to human health?  
What is the impact on recruitment of the consequently attenuated reproduction?   
Now more than ever, concerted actions have to be taken to solve these problems in order to obtain additional informa-
tion on the putative parasites, prevent its expansion which could result in  a collapse of conch populations, as well as a 
possible human health problem. 
 
KEY WORDS:  Strombus gigas, Coccidiasis, sporozoan, conch, disease, reproduction 
 
Una aMenaza más para el Caracol Rosa Strombus gigas? 
Coccidiasis (Apicomplexa) en la Glándula Digestiva de S. gigas: Resultados Preliminares 
 
Una infección intensa y generalizada por esporozoarios fue detectada durante estudios de ciclos reproductores de 
Strombus gigas en San Andrès (Columbia) y arrecife Alacranes (México).  El parásito, aparentemente un Coccidio se 
encontró en la glándula digestiva de los organismos analizados con un grado de infección del 70% al 100%.  Aparentemen-
te, esta infección es responsable de la baja intensidad en la madurez y desove registrados en las localidades del archipiélago 
de San Andrés, Colombia. Estos hallazgos inducen varias preguntas:  Dada la intensidad y amplitud de la infección en tres 
poblaciones tan distantes, si se trata de un mismo organismo, ¿Se encuentran las poblaciones de S. gigas mas interconecta-
das que lo que se presuponía?  Cuales son los factores ambientales que inducen una infección tan intensa y generalizada? 
¿Cual es el ciclo de vida del parásito, cuales son sus vectores u hospederos intermediarios?  ¿Representa este parásito una 
amenaza para la salud humana?  ¿Cual es el impacto en el reclutamiento de esta reproducción atenuada? 
Ahora más que nunca se requiere de acciones concertadas para resolver el problema con el propósito de prevenir la 
expansión del parásito, un colapso en las poblaciones y un probable problema de salud humana. 
 
PALABRAS CLAVES:  Strombus gigas, coccidiasis, esporozoarios, caracol, ciclos reproductores 
 
 
 
INTRODUCTION 
The digestive gland of mollusks has been described for 
bivalves (Andrew 1959, Galtsoff 1964), a few gastropods 
(Andrew 1959) and cephalopods (Andrew 1959, Semmens 
1998).  They all coincide on the basic structure of digestive 
gland, composed of two types of columnar cells with basal 
nuclei, for which several functions have been identified. 
Saint-Hilaire and Young (in Galtsoff 1964) proved the 
ingestion of small food particles by the digestive cells.  A 
role in the fixation of calcium phosphate and calcium 
carbonate for shell formation has been proposed by Jones 
and Saleuddin (1978), and Fournie (1979) among others. 
The controversial work of Semmens (1998) proposes an 
excreting role for nonstructural lipids in cephalopods. 
Andrew (1959) mentions that “the presence of solid bodies 
within the liver cells is common in mollusks”.  Such 
inclusions are considered as residual bodies of lysosomal 
digestion.   
Page 398  58th Gulf and Caribbean Fisheries Institute  
 
On the other hand, Coccidian, Apicomplexa are 
frequent parasites of Mollusks.  Unfortunately, most work 
has been done on oysters, and other bivalves. They have 
been confirmed in abalone (Lester and Davis 1981) and 
shipworms (Hillman et al. 1982), as well as in Cephalo-
pods (Gonzalez et al. 2003).  The Apicomplexa are a 
monophyletic group composed almost entirely of parasitic 
species.  Apicomplexa, along with ciliates and dinoflagel-
lates, form a higher order group known as Alveolata. 
Formerly the Apicomplexa were part of a group called 
sporozoa and this name is still sometimes used.  Their 
name is given by reference to a characteristic apical group 
of organelles.  Apicomplexa have a complex life cycle, 
characterized by three distinct processes: sporogony, 
merogony and gametogony.  The various stages may 
involve various hosts, but frequently they can perform their 
whole life cycle within the same or various cells of a single 
host.  The coccidia are characterized by a thick walled 
oocyst stage that is typically excreted with the feces. 
 
MATERIAL AND METHODS 
 
Study Area 
 
San Andres, Colombia ― the Archipelago of San Andres, 
Colombia; between 12º and 16º N and 78º and 82º W 
covers an area of 300,000 km2 of territorial sea and 
exclusive economic zone of Colombia, in the southern 
Caribbean sea. 
 
Alacranes Reef, Mexico ― is an oval-shaped bank reef 
formation, covering an area of 293 km2 with a maximum 
length and width of 26.5 km and 14.8 km, respectively. It 
is located on the north coast of Yucatan, 80 miles off the 
coast, between 22o 21’ and 22o 35’ N and between 89o 38’ 
and 89o 49’ W.  
 
Collection and Histological Procedure 
Thirty specimens (larger and equal to 20 cm of total 
shell length) were collected monthly, during one year, by 
free diving around San Andrès islands for the Colombian 
samples.  For Alacranes, 30 specimens were collected 
monthly by free diving. All organisms had a well formed 
shell lip, independently of their size. 
Specimens were dissected on site.  Extraction of soft 
parts was achieved by boring a hole on the third turn of the 
spire, cutting off the columellar muscle.  A one cubic 
centimeter from the middle region of the visceral mass 
which included a sample of the gonad and digestive gland 
was dissected and pre-fixed for 12 to 15 days in 10% 
buffered formalin prepared in filtered seawater with 
sodium borate.   For transportation, samples were pre-
served in 70% alcohol with 0.1% glycerin (Bondad-
Reantaso et al. 2001). They were post-fixed in the labora-
tory, for seven days in alcoholic Bouin´s fixative; and 
processed by routine histological techniques. Harris’s 
Hematoxylin and Eosin method was used for staining 
(Luna 1968).  
 
RESULTS 
Large inclusions in the digestive diverticular cells have 
been interpreted as an intense and generalized Sporozoan 
infection.  The parasite, apparently a Coccidian, Apicom-
plexa was found in the digestive gland (DG) of every 
organism analyzed throughout the year from the archipel-
ago of San Andres, Colombia and Alacranes reef, Mexico. 
Figures 1 through 5 present different levels of cysts and 
spores infestation.  A low intensity infestation is presented 
in figure1 where a few digestive diverticula are free from 
parasites, and only some cells are infected in others.  It 
points out the presence of typical bottle shaped and 
spherical cysts in ducts.  Figure 2 presents bottle shaped 
and spherical cysts, pointing out the isolating reaction of 
the cell around a foreign body, and a microspore forming 
cyst.  A detailed view of spherical cysts and isolating 
reaction is presented in Figure 3.  Figure 4 presents a 
bottle-shaped cyst, macro and micro cysts, pointing out the 
hyaline wall of macrospores, and spores.  Clear circles are 
the location of displaced cysts.  Detailed views of spore-
forming cysts and just released spores are presented in 
Figure 5. The presence of cysts in the digestive gland is 
constant through the year at both localities, with a striking 
similarity in intensity.  Table 1 presents the main character-
istics observed. Incidence of cysts is lower from January to 
May, with a minimum during March and April and 
maximum during October and November.  From August to 
December, two types of spores could be detected. Micro-
spores are about the diameter of the columnar cell nucleus; 
they are very dense and stain in deep red with the Hema-
toxyline – Eosin technique used. Macrospores are about 
twice as large in diameter; they present a granular cyto-
plasm and frequently “U” shape granular structure can be 
seen (Figures 6 - 7). The diagrammatic representation of 
various cyst shapes detected is presented in Figure 8.  
Bottle shape cysts frequently have a complex structure 
associated to the ring on what is assumed to be the apical 
zone.  This end of cyst (a, b and d) was usually the only 
portion of the cyst in contact with the cell cytoplasm. 
Round macro and micro cysts were so dense that any 
structures could be seldom identified inside, except for 
spore forming cysts in which a various number of hyaline 
structures could be seen (f).  Structures h and i had the 
same size and shape as a spore-forming cyst, but two rings 
were clearly identified.  However, no structures could be 
detected inside. 
 
 
 
 
 
 
  Baquero Cárdenas, E. et al.  GCFI:58   (2007) Page 399 
 
 
 
Figure 1.   Sampling sites, a) Alacranes reef, Mexico; b) San Andres archipelago, Colombia. 
C
Hd
Ct
Figure 2.  General vew of a partialy infected digestive gland 
of S. gigas. C, cysts of sporozoa; Hd, healthy digestive di-
verticula; Ct, connective tissue (10 x). 
Ct
Vc
Ir
Cn
Sc
Figure 3.  Detail of digestive diverticula, where cyst can be 
seen with a clear alo showing isolating reaction from the 
cell.; Cn, Cell nucleus; Ct, Connective tissue; Ir, Isolating 
reaction; Sc. Spore forming cyst,  c, Vacuolar cytoplasm (40 
x). 
Cn
Ir
Ct
Vc
S
Figure 4.  Detail of digestive diverticula showing different 
development stage of the parasite.  Cn, cell nucleus; Ct, 
connective tissue; Ir, isolating reaction; S, spores. Vc, 
S
A Cw
Figure 5.  Detail of cysts where the typical Apicomplexa 
shape can be seen, with apical region. A, Apicomplexa like 
cyst; Cw, cyst wall; S, spores. (40 x). 
Page 400  58th Gulf and Caribbean Fisheries Institute  
 
ZsMs
Cn
S
Ir
Figure 6.  Digital image of cysts and spores. Cn, cell nu-
cleus; Ir, Isolating reaction; S, spores. (100 x) 
Figure 7.  Digital image of digestive diverticula of Strombus 
gigas with two types of spores. Ms, microspores;  
Zs, zoospores or macrospores (10 x)  
 Table 1.  Principal characteristics observed on the digestive gland of S. gigas  from San Andrès, Co-
lombia and Alacranes , Mexico. A, Abundant(>50); F, few (<50); S, scarce; B, bottle-like cyst; BC, big 
spherical cyst; SC, small spherical cyst; BS, big spore; SS, small spore. 
  Localities         
Months Alacranes San Andrés       
January F, B, BC, SC   Cysts in different segmentation stages. Cysts in lumen of digestive gland ducts and digestive track. 
February F, B, BC, SC   Few cysts in segmentation. Cysts in lumen of digestive gland ducts and digestive track 
March F, B, BC, SC F, B, BC, SC 
Cysts in different segmentation stages, more abundant 
than in January and February 
Cysts in lumen of digestive gland ducts and digestive track 
April A, B, BC, SC A, B, BC, SC 
Few cysts in segmentation. 
Over 70% of healthy hepatic tissue Cysts in lumen of diges-
tive gland ducts and digestive track 
May F, B, BC, SC F, B, BC, SC 
Few cysts in segmentation. 
Over 70% of healthy digestive tissue Cysts in lumen of 
digestive gland ducts and digestive track 
June   A, B, BC, SC Numerous cysts in lumen of digestive gland ducts and di-gestive track 
July           
August A, B, BC, SC, BS, A, B, BC, SC Cysts in different segmentation stages 
September A, B, BC, SC A, B, BC, SC Few healthy digestive gland cells, all diverticula with cysts 
October F, BS, Ss A, B, BC, SC Few healthy digestive gland cells, all diverticula with cysts 
November A, B, BS, SS A, B, BC, SC, BS, SS Few healthy digestive gland cells, all diverticula with cysts 
December A, B, BC, SC, BS, SS 
A, B, BC, SC, BS, 
SS Few healthy digestive gland cells, all diverticula with cysts 
  Baquero Cárdenas, E. et al.  GCFI:58   (2007) Page 401 
 
ZsMs
Figure 8.  Detail view of spores, Ms, microspores;  
Zs, zoospores o macrospores 
 
Figure 9.  Mycroscopic characteristics of diferent cysts. a 
and b Apicomplexa like cysts; c, fuciform cyst; d, e, g,  smal 
spherical cysts; f, large cyst with two large spores forming 
inside; h and y atipical shape cysts. 
Mollusks (Perkins 1998, Gestal et al. 2002).  As stated by 
some of these authors, Apicomplexa usually have a 
complex live cycle, including different hosts, but it is not 
unusual that the whole life cycle takes place within the 
same host.  Apparently this is the case for the Strombus 
gigas parasite, but a specific study should be undertaken, 
given the apparent impact that it seems to have on the 
reproductive efficiency of the affected populations and its 
apparent wide distribution.  
 
ACKNOWLEDGMENTS 
The ichthyology laboratory of CINVESTAV-IPN 
Mérida for its logistic support of this histology study and 
histological assistant Teresa Colás Marrufo. 
 
LITERATURE CITED 
Andrew W. 1959. From food vacuole to complex digestive 
structure in the invertebrates. Pages 138-226 in: 
Textbook of Comparative Histology. Oxford Univer-
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Bondad-Reantaso, M., S.E. McGladdery, I. East, and R.P. 
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Fournie, J. 1979.  Études des cellules libres présentes à la 
surface de la coquille d’Agrililmax reticulatus (Muller) 
origine et rôle dans la mise en place de l’hipostracum, 
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DISCUSSION  
Slides for microscopic observation were not intended 
for the study of the parasite, but for the study of gonad 
development. Therefore, the staining techniques did not 
allow for a clear interpretation of the different stages 
found.  Even though, enough information is available to 
ascertain that a Coccidian Apicomplexa is infecting the 
digestive gland of Strombus gigas from San Andres and 
Alacranes reef.  The various structures identified coincide 
with different stages of the life cycle of other Coccidians 
parasites from Vertebrates (Lom 1970, Levine 1985, 
Paperna and Lainson 2000) among others and from 
Page 402  58th Gulf and Caribbean Fisheries Institute  
 
Lom, J. 1970.  Protozoa causing diseases in marine fishes. 
Pages 1j01-121 in: S.F. Snieszko (ed.) A sympo-
sium on Diseases of Fishes and Shellfishes. 
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Paperna, I and R. Lainson. 2000.  The fine structure of the 
Endogenous stage of Isospora hemidactyli Carini, 
1936 in the Gecko Hemidactylus mabouia from 
North Brazil. Memoirs of the Institute Oswaldo 
Cruz, Rio de Janeiro, Brazil 95(1):43-47 
Perkins, O.F., 1988.  Parasite morphology, strategy and 
evolution. Pages 93-111 in: Disease Processes in 
Marine Bivalve Mollusks. American Fisheries 
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Semmens, J.S. 1998.  An examination of the role of the 
digestive gland of two Loliginid squids, with 
respect to lipid: storage or excretion? Proceedings 
of the Royal Society of London  265:1685-1690. 


One more threat for the Queen Conch Strombus gigas? Coccidian (Apicomplexa) infection of S. gigas digestive gland: preliminary results

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One more threat for the Queen Conch Strombus gigas? Coccidian (Apicomplexa) infection of S. gigas digestive gland: preliminary results

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