Aquaculture 60 (2011) 43–50

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Aquaculture
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e

Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from
natural stock of Santa Catarina Island, SC, Brazil
Rachel Costa Sabry a,⁎, Patrícia Mirella da Silva b, Tereza Cristina Vasconcelos Gesteira a,
Vitor de Almeida Pontinha c, Aimê Rachel Magenta Magalhães c
a
Instituto de Ciências do Mar, Universidade Federal do Ceará, Av. da Abolição, 3507, Meireles, CEP: 60165-081, Fortaleza, CE, Brazil
b
Universidade Federal da Paraiba, Centro de Ciências Exatas e da Natureza, Departamento de Biologia Molecular, Cidade Universitária — Campus I. CEP, 58059-900, João Pessoa, PB, Brazil
c
Universidade Federal de Santa Catarina, Departamento de Aquicultura, Núcleo de Estudos em Patologia Aquícola, Rodovia Admar Gonzaga, 1346, Itacorubi, CEP 88040-900, Florianópolis,
SC, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: This paper gives an account of the pathogens found in the cultivated Japanese oyster Crassostrea gigas and in
Received 15 April 2011 the mangrove oyster Crassostrea rhizophorae from natural populations of two sites, Sambaqui (27° 29′18″S,
Received in revised form 31 July 2011 48° 32′1″W) and Ribeirão da Ilha (27° 42′51″S, 48° 34′6″W), Santa Catarina Island, Brazil. Oysters were
Accepted 4 August 2011
collected in March 2008 and April 2009, 150 per site, year and condition (rocky shore and culture). For
Available online 10 August 2011
pathological study, the techniques used were: macroscopic examination, histology and tissue culture in fluid
Keywords:
thioglycollate medium specific for Perkinsus. The results showed the presence of the polychaete Polydora sp.
Oysters with high prevalence (up to 100%) in C. gigas; gametic hypertrophy in C. rhizophorae from Ribeirão da Ilha and
Oyster farming in C. gigas from Sambaqui and Ribeirão da Ilha with low prevalence (3.3%); rickettsia-type bacteria, with
Pathogens greater prevalence in C. gigas (30%) than in C. rhizophorae, causing alteration in the epithelium of the stomach.
Histopathology It was not detected the presence of Perkinsus in any oyster sample analyzed of any site. Ciliates of genus
Trichodina were observed among gill lamellae, digestive tubules, and adhered to the gills of oysters from
Ribeirão da Ilha, with higher prevalence in C. rhizophorae (50%) and without causing injury. Protozoa
Sphenophrya-type was found in the gills of C. gigas and C. rhizophorae, with higher prevalence in C. gigas from
Sambaqui (70%), not causing changes in the gills. Protozoa of the genus Ancistrocoma were detected in the
digestive tubules of C. gigas (36.7%) and C. rhizophorae (40%) from Sambaqui at low intensity and without
causing apparent damage. Steinhausia-type microsporidians were observed in the cytoplasm of oocytes of
C. rhizophorae and C. gigas with prevalences up to 33.3%. The intensity of infection in the animals was low,
with only one oyster presenting more than 50 oocytes infected. The sporocysts of the pathogen caused
alteration in the normal structure of the oocytes cytoplasm. Protozoa of genus Nematopsis were observed in
the connective tissue of the gills and mantle with high prevalence (100%) in C. rhizophorae from Sambaqui,
without host defense response. The observed metazoan were: turbellarians Urastoma-type, metacestode of
genus Tylocephalum and copepods possibly of genus Pseudomiycola, all in low prevalence. None of the
pathological occurrences found seems to cause significant damage in oysters, once they were found at low
intensities. However, due to the great socioeconomic importance that the shellfish represent to the State of
Santa Catarina, it's necessary to keep monitoring the health status of these populations.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction
The State of Santa Catarina is the biggest Brazilian producer of
shellfish, contributing with 95% of national production, represented
by the culture of the brown mussel Perna perna (Bivalvia: Mytilidae),
⁎ Corresponding author at: Universidade Federal do Ceará, Instituto de Ciências do
Mar, Av. Abolição, 3207, Meireles, CEP: 60165-081, Fortaleza, CE, Brazil. Tel.: + 55 85
3366 7009.
E-mail addresses: rachelsabry@yahoo.com.br (R.C. Sabry),
mirella_dasilva@hotmail.com (P.M. da Silva), gesteira@ufc.br (T.C.V. Gesteira),
rachel@cca.ufsc.br (A.R.M. Magalhães).
the Japanese oyster Crassostrea gigas (Bivalvia: Ostreidae) and scallop
Nodipecten nodosus (Bivalvia: Pectinidae), which is already being
grown commercially in the state. However, studies on diseases of
these bivalves are scarce when compared to other parts of the world,
where pathologies that affect shellfish commercially harvested are
well known (Bower et al., 1994). Only in last years, researches on the
health of marine bivalves from the Brazilian coast have been
intensified (Boehs and Magalhães, 2004; Boehs et al., 2009; da Silva
et al., 2002; Sabry and Magalhães, 2005; Sabry et al., 2007; Suárez–
Morales et al., 2010) due primarily to the expansion of the cultures.
The summer mass mortality of Japanese oyster (C. gigas) cultured
in Santa Catarina was first-time registered in December 1987. In the

0044-8486/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2011.08.006
44 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50
summer of 89/90s summer mortality reached 89.5% (Silveira, 1997).
The phenomenon was associated to stress caused by the breeding
season, high water temperatures and perhaps by the presence of
bacteria of the genus Nocardia (Silveira, 1997). Bacteria, like viruses,
when at high intensities can cause mortality in shellfish (Gulka et al.,
1983; Paillard, 2004; Renault and Novoa, 2004; Villalba et al., 1999),
but they not cause mortality at low intensities (Carballal et al., 2001;
Cremonte et al., 2005).
Protozoa are important pathogens and can cause mortality in
several species of shellfish in worldwide. With respect to protozoa,
Nematopsis spp. (Apicomplexa: Porosporidae) use marine bivalves as
intermediate hosts (Azevedo and Cachola, 1992; Carballal et al.,
2001), but there is controversy regarding to its pathogenicity
(Lauckner, 1983). Nematopsis sp. was described in oysters C. gigas
and Crassostrea rhizophorae grown in Ponta do Sambaqui Beach, Santa
Catarina Island, Brazil (Sabry and Magalhães, 2005). Trichodina
(Ciliophora: Trichodinidae) can cause destruction of gill filaments
and compromise weight gain of the animals (Bower et al., 1994;
Figueras and Villalba, 1988). Trichodina sp. was observed in
C. rhizophorae (Sabry and Magalhães, 2005) and in Anomalocardia
brasiliana (Bivalvia: Veneridae) from Santa Catarina Island (Boehs and
Magalhães, 2004), but without causing serious damage to the host.
Recently, for oysters of this region were recorded protozoa of the
genera Sphenophrya, Ancistrocoma (Ciliophora) and Steinhausia
(Microspora) (Pontinha, 2009; da Silva et al., 2010). Sphenophrya
can cause cellular hypertrophy in the host and form tumors called
xenoma (Boehs et al., 2009; Winstead et al., 2004). However, there are
no reports of mortality associated to infection by this pathogen
(Bower et al., 1994; Lauckner, 1983; Winstead et al., 2004).
Ancistrocoma infection also has not been associated to pathologies
(Bower et al., 1994). In the case of parasitism by Steinhausia
(microsporidian that infects the cytoplasm of oocytes), it is observed
inflammatory or immunological reaction by the host, characterized by
intense infiltration of hemocytes (Green et al., 2008). Steinhausia has
already been detected in populations of Cerastoderma edule (Bivalvia:
Cardiidae) from Galicia coast, Spain, without significant pathologic
damage in infected animals (Carballal et al., 2001).
Metazoan of genus Tylocephalum (Cestoda: Tetragonocephalidae)
were observed in low prevalence and intensity of infestation in
C. gigas (Sabry and Magalhães, 2005) and in A. brasiliana from Santa
Catarina Island (Boehs and Magalhães, 2004). The turbellarian
Urastoma cyprinae was recorded in mussels Mytilus galloprovincialis
from the Black Sea (Murina and Solonchenko, 1991) and Spain
(Robledo et al., 1994) and in Mytilus edulis from Portugal (dos Santos
and Coimbra, 1995) causing severe alterations in the gills. Polychaetes
of the genus Polydora (Polychaeta: Spionidae) are commonly found in
the Japanese oyster C. gigas (da Silva et al., 2010; Ibbotson, 2002;
Pontinha, 2009; Sabry and Magalhães, 2005) and in other bivalves
such as the mussel P. perna (da Costa, 2007) and the cockle
A. brasiliana (Boehs and Magalhães, 2004) from Santa Catarina Island.
Among the copepods, Pseudomyicola spinosus (Copepoda: Myicolidae)
is commonly found in marine bivalves (Cáceres-Martínez et al., 2005;
Ho and Kim, 1991) and when at low prevalence and intensity does not
cause pathologies (Bower et al., 1994). In Brazil, histopathological
analysis in the mussel P. perna cultured in Santa Catarina, revealed
that the presence of copepods of genus Monstrilla caused changes in
the structure of the mantle edge with intense hemocytic infiltration
(Suárez–Morales et al., 2010). None of the pathogens listed above
is notifiable to the World Organization for Animal Health (OIE).
Currently, according to this organization, notifiable pathogens for
shellfish are the protozoa Haplosporidia: Bonamia ostreae and
B. exitiosa; Paramyxea: Marteilia refringens; Perkinsozoa: Perkinsus
marinus and P. Olseni; bacteria Xenohaliotis californiensis and Herpes-
type virus which affects abalones. Considering the socioeconomic
importance of bivalves for the State of Santa Catarina, this paper gives
a report of the pathogens found in the cultured oyster C. gigas and in
the mangrove oyster C. rhizophorae from cliffs next to cultures in
Santa Catarina Island, SC, Brazil.
2. Materials and methods
2.1. Sampling of oysters
Samples of the mangrove oyster C. rhizophorae (n = 600) and of
the Japanese oyster C. gigas (n = 600) were collected at two sites of
the Santa Catarina Island, in Sambaqui (North Bay, 27° 29′18″S, 48°
32′12″ W) and Ribeirão da Ilha (South Bay, 27° 42′51 ″ S, 48° 34′6 ″
W). Samples were collected in March 2008 and April 2009. In each
month 150 oysters were collected from each species and site. Oysters
C. rhizophorae were removed from the rocky shore, located in the
intertidal zone, far 70 and 200 m from the culture of oysters C. gigas at
Sambaqui and Ribeirão da Ilha, respectively. Specimens of C. gigas
were collected from culture lanterns hanging at Sambaqui in long-
lines belonging to the Laboratory of Culture of Mollusks, Federal
University of Santa Catarina, and from Ribeirão da Ilha, belonging to a
shellfish farmer. The oysters had market size, corresponding to a
cultivation time of 9–12 months. The oysters were measured (shell
height according to Galtsoff, 1964), and opened for macroscopic
observation of the shell and internal organs (mantle, gills, gonad and
digestive gland), in order to verify the occurrence of pathological
changes. All animals collected at each point (n = 150) were submitted
individually to cultivation technique in Ray's Fluid Thioglycollate
Medium (RFTM), item 2.2, and 30 individuals were randomly selected
for histopathological analysis, item 2.3.
The temperature and salinity of sea water were measured at each
site and date of collection using a thermometer and refractometer,
respectively. The water temperature in Sambaqui was 24 °C in 2008 and
2009 and in Ribeirão da Ilha, 22 and 26 °C for the years 2008 and 2009,
respectively. The salinity was 32‰ (2008) and 35‰ (2009) in Sambaqui
and 26‰ (2008) and 34‰ (2009) in Ribeirão da Ilha (Table 1).
2.2. Incubation of tissues in Ray's Fluid Thioglycollate Medium (RFTM)
Two demibranch and the rectum of each animal were incubated in
thioglycollate liquid medium for 7 days in darkness and at room
temperature (±28 °C). After the incubation period, tissues were
collected, macerated on a slide and stained with Lugol solution,
according to the method described by Ray (1954). The preparation
was observed under an optical microscope to verify the presence of
Perkinsus hypnospores, which are spherical and its walls stains blue or
bluish black.
2.3. Histological preparations
From each oyster (n = 30 per site, specie and year), a cross section
of the animal was removed, it being sampled several organs,
including: gills, gonad and digestive gland. The tissues were fixed in
Davidson's solution (Shaw and Battle, 1957) for 24 h, dehydrated in a
graded series of alcohol up to 100%, cleared in xylene and
impregnated in histological paraffin at 60 °C. Cuts of 5 μm thickness
were made and stained with hematoxylin and eosin (Howard et al.,
2004). The sections were analyzed under optical microscope. The
prevalence of pathogens was calculated as being the number of
parasitized animals over the total number of oysters collected in each
collection point (Bush et al., 1997).
3. Results
3.1. Biometry
The biometry of oysters C. rhizophorae (rocky shore) and C. gigas
(culture) from Sambaqui and Ribeirão da Ilha aimed to verify the size
 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50 45

of animals that would be submitted to pathological analysis, without,
however, make comparisons on the growth of animals in the two
sampled sites and not aimed to relate the size of the animals with the
presence or absence of parasitism. The mean heights (mm) of oysters
in 2008 and 2009 are shown in Table 1.
3.2. Macroscopic analysis
Macroscopic observations did not reveal the presence of pustules or
abscesses in any organs examined in both species. The prevalent
macroscopical change was the parasitism by the polychaete of genus
Polydora in the valves of oysters. The infestation by Polydora was
characterized by the presence of horizontal and vertical tubes.
Eventually the tubes drilled the tissue reaching the digestive gland. It
was also observed bubbles covered by layers of conchioline occupying a
representative part of the inner region of the animal valves.
The highest prevalences of Polydora in C. rhizophorae were observed in
the collections of 2008 in Sambaqui (81.3%) and Ribeirão da Ilha (67.3%)
(Table 1). With respect to C. gigas, the prevalence reached maximum
values (100%) in both study sites and in the two sampling years (Table 1).
3.3. Incubation of tissues in ray's Fluid Thioglycollate Medium (RFTM)
For both species of oysters investigated for the presence of
Perkinsus by the RFTM method, all results were negative, i.e., there
was no presence of this protozoan. The technique of cultivation of
tissues in liquid thioglycollate (RFTM) was effective for the detection
of the protozoan Nematopsis. Although Nematopsis had not been
stained by Lugol, it performed quite refractional and was easily
observed among cells of the gills of oysters in a 20x objective.
Nematopsis prevalence by RFTM in C. rhizophorae from Sambaqui was
high and ranged from 90 to 96% (Table 1).
3.4. Histopathological analysis
Histological analysis showed: hypertrophy of the male gametes,
presence of rickettsia-type bacteria and protozoa of the genera Trichodina,
Sphenophrya, Ancistrocoma, Steinhausia and Nematopsis. Among the
metazoan were observed the turbellarian Urastoma, the cestode Tyloce-
phalum and a copepod possibly of genus Pseudomiycola (Table 1).
However, none of the histopathological changes found in this study
presented risk to the health of oysters.
3.4.1. Hypertrophy of the gametes
In the male gonadal follicles of both oysters species were found
hypertrophied cells with a diameter ranging from 15 to 36 μm. These
cells presented an acidophilic content and a basophilic peripheral
region (Fig. 1A). Only three oysters showed such pathology: one
oyster C. rhizophorae from Ribeirão da Ilha, collected in 2009, one
oyster C. gigas from Ribeirão da Ilha, collected in 2008 and another
from Sambaqui in 2009, resulting in a low prevalence (3.3%) (Table 1).
3.4.2. Rickettsia-type bacteria
Rickettsia-type bacteria were seen in C. rhizophorae and C. gigas from
Sambaqui and Ribeirão da Ilha in 2008 and 2009. The bacteria formed
intracytoplasmic colonies of basophilic character and size ranging from
7 to 30 μm in epithelial cells of digestive tubules (Fig. 1B). In the most of
the investigated oysters the intensity of infection was low (1–5
colonies). In just one oyster C. rhizophorae were also observed five
colonies of these bacteria in the stomach epithelium, causing changes in
epithelial cell cytoplasm (Fig. 1C). The higher prevalence of the bacteria
was 30% in C. gigas from Ribeirão da Ilha, in 2009 (Table 1).
3.4.3. Protozoa
Ciliates of genus Trichodina were observed adhered to the gill
lamellae and free in the lumen of digestive tubules of C. rhizophorae
and C. gigas, from Ribeirão da Ilha (Fig. 1D and E). In the gills, it was
observed until 4 ciliates/histological section and in digestive tubules
more than 5 per oyster. Trichodina appeared disk-shaped and with an
evidently basophilic nucleus (Fig. 1D). In the gills, these ciliates had
sizes ranging from 12 to 47 μm and in digestive tubules, 10 to 20 μm.
At the ends of the pathogens were observed structures (hooks) used
to anchorage in the host (Fig. 1E). The highest prevalence in C. gigas
was 13.3% in 2008. In C. rhizophorae, these ciliates were only observed
in 2009 in Ribeirão da Ilha, with high prevalence (50%) (Table 1).
Another ciliate, Sphenophrya sp. was seen at the base of gill filaments
(Fig. 1F). The ciliate had an oval or round shape, containing a basophilic
macronucleus, a cytoplasm with character eosinophilic and size ranging
from 9 to 17 μm. The highest prevalence of Sphenophrya was observed in
C. gigas from Sambaqui in 2009 (70%) and the lowest (6.7%) in
C. rhizophorae from Sambaqui in 2008 (Table 1). In general, the intensity

Table 1
Prevalence (%) of pathogens and pathological changes in the oysters Crassostrea gigas (G) and C. rhizophorae (R) at two points of the Santa Catarina Island, Sambaqui (SAM) and
Ribeirão da Ilha (RIB) in March–April, 2008 and 2009. Macroscopic analysis (MA, N = 150), incubation of tissues in Ray's Fluid thioglycollate Medium (RFTM, N = 150) and
histological cuts (HC, N = 30). It's also showed the average height of the oysters (mm) and standard deviation (SD).

Pathogens and 2008 2009

pathological change
SAM RIB SAM RIB

G R G R G R G R

Height (mm) ± SD

96.7 ± 14.3 55.3 ± 10.3 84.2 ± 15.8 49.6 ± 6.4 98.1 ± 10 59.6 ± 5.1 104.9 ± 12 58.2 ± 5.4

T. 24 °C; Sal. 32‰ T. 22 °C; Sal. 26‰ T. 24 °C; Sal. 35‰ T. 26 °C; Sal. 34‰

Gamet hypertrophy – – 3.3 – 3.3 – – 3.3

Rickettsia-type bacteria 16.7 10.0 6.7 13.3 10.0 13.3 30.0 10.0
Protozoa
Trichodina sp. – – 13.3 – – – 3.3 50.0
Sphenophrya sp. 46.7 6.7 20.0 26.7 70.0 33.3 13.3 46.7
Ancistrocoma sp. 36.6 6,7 36.7 10.0 – 40.0 6.7 23.3
Steinhausia sp. 26.7 16.7 – 23.3 16.7 33.3 3.3 30.0
Nematopsis sp. (HC) – 96.6 23.3 – 100 – 50.0
Nematopsis sp.(RFTM) 4.7 90.0 1.3 35.3 – 96.0 – 88.0
Metazoan
Polydora sp. (MA) 100 81.3 100 67.3 100 18.7 100 22.7
Urastoma sp. – 6.7 6.7 – – 3.3 – 6.7
Tylocephalum sp. 3.3 – – – 3.3 – – –
Copepod – – – 3,3 – – – –
46 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50

Fig. 1. Pathological changes and pathogens detected in tissues of Crassostrea gigas and C. rhizophorae from Sambaqui and Ribeirão da Ilha (Santa Catarina Island, Brazil) in March–
April, 2008 and 2009. (A) Hypertrophied cells in the wall of male follicle (arrow); (B) Colony of Rickettsia-type bacteria (arrow) in the cytoplasm of digestive tubule epithelial cell;
(C) Colonies of Rickettsia-type bacteria in the cytoplasm of epithelial cells of the stomach; (D) Trichodina sp. (arrow) in the gill filaments, showing evident nucleus; (E) Detail of
fastening structures (arrow) of Trichodina; (F) Ciliated Sphenophrya sp. (arrow) in contact with the gills. Bar = 20 μm.

was low with the exception of only three animals (C. rhizophorae from
Sambaqui) which presented each one more than 250 ciliates in the whole
examined gill/histological cut. No change was detected in the gills neither
host reactions.
Ciliates of the genus Ancistrocoma were observed in the lumen of
digestive tubules. The ciliates showed an oval shape, with basophilic
nucleus and eosinophilic cytoplasm (Fig. 2A), with sizes ranging from
12 to 26 μm. The highest prevalences were observed in C. rhizophorae
from Sambaqui in 2009 (40%) and in C. gigas from Sambaqui (36.7%)
and Ribeirão da Ilha (36.7%) in 2008. The intensity of this ciliate was
low, with a maximum of 4 ciliates/histological section.
Steinhausia microsporidian was detected in the cytoplasm of
oocytes of the oysters (Fig. 2B). The vacuoles containing the pathogen
cells sometimes occupied a representative portion of the cytoplasm.
The highest prevalences of these protozoa were observed in 2009, in
C. rhizophorae from Sambaqui (33.3%) and Ribeirão da Ilha (30%). The
intensity of infection in the most animals ranged from 1 to 35 infected
oocytes/histological section. However, in one oyster C. gigas from
Sambaqui, it was observed more than 50 oocytes containing the
spores of the pathogen, without host defense response.
Protozoa of the genus Nematopsis were observed infecting the
connective tissue of various organs such as gills and mantle (Fig. 2C).
The oocysts Nematopsis densely basophilic had sizes ranging from
8 to 14 μm, hyaline wall and were found 1 to 4 oocysts/phagocyte.
The found prevalences after observation of histological sections
were high in C. rhizophorae from Sambaqui (96.6% in 2008 and 100%
in 2009). In C. gigas, this pathogen was not detected in any of the
studied locations. Despite the high prevalences of Nematopsis sp. in
C. rhizophorae, it was not observed host response. The intensity of
infection was low, with few oocysts/histological section.
3.4.4. Metazoan
Turbellarians of the genus Urastoma were found close to the gills of the
oyster C. gigas from Ribeirão da Ilha, and C. rhizophorae from Sambaqui
and Ribeirão da Ilha. They presented sizes ranging from 162.5 to 245 μm
(Fig. 2D). The highest observed prevalence was 6.7% (Table 1). The
intensity of infestation was low, having been registered at the most two
turbellarians/oyster and without causing apparent damage in the gills.
Larvae of cestodes of the genus Tylocephalum were recorded only
in the Japanese oysters from Sambaqui with a prevalence of 3.3% in
collections from March to April of the years 2008 and 2009. The larvae
were encapsulated by several layers of flattened cells. Besides the
encapsulation reaction, it was not observed other change in the host
tissue (Fig. 2E). A copepod, possibly of the genus Pseudomiycola, was
 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50 47

Fig. 2. Pathogens observed in tissues of Crassostrea gigas and C. rhizophorae from Sambaqui and Ribeirão da Ilha (Santa Catarina Island, Brazil) in March–April, 2008 and 2009.
(A) Ancistrocoma sp. (arrow) in the lumen of a digestive tubule; (B) Vacuole with parasitic spores of Steinhausia sp. (arrow) in the cytoplasm of an oocyte; (C) Oocysts of Nematopsis
sp. in the digestive gland; (D) Urastoma sp. among gill filaments; (E) Tylocephalum sp. in connective tissue around digestive tubules. (F) Copepod (arrow) causing disruption of the
wall of a digestive tubule. See details of the appendages (arrow). Bar = 20 μm (Figs. A, B, C); Bar = 50 μm (Figs. D, and F).

detected in the lumen of a secondary digestive tubule of the oyster
C. rhizophorae from Ribeirão da Ilha (Fig. 2F). This parasite had a size of
900 μm and caused the rupture of the wall of this tubule.
4. Discussion
The present study registered several pathogens with different
prevalences and intensities in the two species of studied oysters. However,
none of these organisms represented risk to the populations of oysters.
The polychaete of genus Polydora has been present with high
prevalence (100%) in C. gigas from the two studied sites. However,
producers did not report mortalities during the periods of collection,
showing that, despite its high prevalence, the possible damages do not
lead to oyster death. For the same sites, it has already been docu-
mented similar prevalences (Ibbotson, 2002; Sabry and Magalhães,
2005) of this polychaete. Infestations by Polydora sp. are common in
bivalves from several parts of the world and seem to be the biggest
cause of loss for the producer, since the horizontal and vertical tubes
of dark color and mud bubbles in the shell influence negatively
the market value of the mollusks. In the present study, the oyster
C. rhizophorae collected in 2009 showed prevalence of Polydora below
than those found in the Japanese oysters C. gigas in the same period.
This might suggest that C. rhizophorae were more resistant to attack of
polychaetes. However, for the year 2008 in both places (Sambaqui and
Ribeirão da Ilha), the prevalences of Polydora in C. rhizophorae were
high, deserving so constant monitoring to better understanding about
the susceptibility of C. rhizophorae to the attack of these polychaetes.
The results obtained by the technique of tissue culture in
thioglycollate medium for diagnosis of Perkinsus showed that the
oysters from natural beds as well as the cultured Japanese oysters
are not affected by this pathogen. Studies in populations of mollusks
from Santa Catarina Island, using this specific technique for diagnosis
of protozoa of the genus Perkinsus are recent. The first researches
with RFTM were performed in 2008 by da Silva et al. (2010), for
C. rhizophorae and A. brasiliana, which also obtained negative results.
In Brazil, only one study with C. rhizophorae in Bahia State refers to the
use of this technique and also not detected Perkinsus sp. in the analyzed
oysters (Nascimento et al., 1986). In the soft-clam (Tagelus plebeius)
from Pontal da Daniela Beach, SC, it was also not detected the presence
of Perkinsus sp. when this technique was used (da Silva et al., 2009).
48 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50
The hypertrophies of male gametes observed in oysters C. rhizophorae
(Ribeirão da Ilha) and in C. gigas (Ribeirão da Ilha and Sambaqui) were
possibly caused by a virus. The presence of hypertrophied nucleus with
granules intensely basophilic in the cell periphery, suggests viruses
presence of the families Papillomaviridae and Polyomarviridae that
cause the disease known as Viral Gametocytic Hypertrophy (VGH),
(Bower et al., 1994). This disease was recorded in bivalve mollusks,
including oysters C. gigas and C. rhizophorae (Bower et al., 1994). The first
report of this disease was made by Farley (1976). Since then, this disease
has been documented in several mollusks (Choi et al., 2004; Garcia et al.,
2006; Meyers et al., 2009; Winstead et al., 2004). The prevalence of
gametocytic hypertrophy detected in oysters of the present study was
low and were not observed hemocytes infiltrations or tissue damage,
besides alterations of the infected gamete. In C. gigas from South Korea,
the prevalences of VGH ranged from 3.3 to 7.1%, the intensity of infection
was low, not being detected defense responses of the host (Choi et al.,
2004). In C. gigas studied in France, the prevalence of VGH was low (3.3 to
13.3%) as well the intensity of infection. The authors observed lesions in
the gonads of some animals, but with no hemocytic reaction and without
lethal effects on oysters (Garcia et al., 2006).
In the present study, colonies of Rikettsia-type bacteria were
observed in epithelia of digestive tubules, and only in one oyster
C. rhizophorae it was detected in the epithelium of the stomach. Despite
the found prevalences have been up to 30%, there was no considerable
damage in animals. In cockles C. edule from Spain, the infection by
Rikettsia-type bacteria colonies were of low intensity and there was not
observed response of the host to infection (Carballal et al., 2001),
opposite to what was reported in oysters C. gigas from the Atlantic coast
of France, when a severe infection caused lesions and changes in the
normal gill structure (Renault and Cochennec, 1994). Rikettsia-type
bacteria caused intense infections and severe damage in epithelial cells
of gill, digestive gland and mantle of the oyster Crassostrea ariakensis
from the Guangdong Province, China (Sun and Wu, 2004). However, the
harm caused by these bacteria in host cells seem to differ among
mollusks (Boehs et al., 2010; Cremonte et al., 2005; da Silva et al., 2005;
Green et al., 2008; Villalba et al., 1999; Wu and Pan, 2000).
Ciliates are organisms that inhabit the paleal cavity of bivalves
without causing harm to the host (McGladdery and Bower, 2001).
In the present study, the prevalence of the ciliate Trichodina in
C. rhizophorae was high (50%) but lower than that observed in the
scallop Aequipecten tehuelchus (100%) from Patagonia, Argentina,
(Cremonte et al., 2005). The highest prevalence of Trichodina observed
only in oysters from natural stocks of Ribeirão da Ilha, possibly may
be related to the high concentration of organic matter and, in con-
sequence, inadequate water quality conditions (Akşit et al., 2008). The
occurrence of Trichodina seems to be greater in hosts of polluted
areas, it being therefore, a pathogen biological indicator of pollution
(Lauckner, 1983). In addition, the fact of Trichodina has been observed
in a larger amount free in the digestive tubules of investigated oysters,
could indicate a high amount of this protozoan in the environment,
in the collection day. Ciliates of genus Trichodina occur worldwide in
several bivalves mollusks (Boehs and Magalhães, 2004; Bossaïd et al.,
1999; Carballal et al., 2001; Cremonte et al., 2005). However, the
pathogenicity of Trichodina is controversial (Bower et al., 1994). High
infections by Trichodina sp. were associated to erosions in the gills of
Crassostrea angulata from France and were responsible for malfunc-
tion of this organ (Lauckner, 1983). In the scallop A. tehuelchus
from natural northeastern stocks of Patagonia, Argentina (Cremonte
et al., 2005) and in the cockle C. edule from the coast of Galicia,
Spain (Carballal et al., 2001), Trichodina also not caused damages
or responses of the hosts. However, in C. gigas very infected by
Trichodina, it was detected inflammatory response and alterations in
the gill epithelium (Bossaïd et al., 1999).
Ciliates of genus Sphenophrya were found in the gills of C. gigas
and C. rhizophorae in both studied locations. Sometimes the detected
prevalences were high, reaching up to 70% in C. gigas from Sambaqui,
but the intensity was generally low and any inflammatory response
was observed in affected oysters. Ciliates of this genus are found in
a great variety of species of bivalves, being able to cause hypertrophy
of the cell and its nucleus (xenoma) (Bower et al., 1994). In
C. rhizophorae from Todos os Santos Bay, Salvador, Bahia State (BA),
Sphenophrya was observed without causing any damage (Nascimento
et al., 1986). However, for the same species of oyster collected in
Camamu Bay, BA, it was observed the formation of xenoma (Boehs
et al., 2009) and the authors concluded that this pathological effect
was associated to the presence of this ciliated. In the mussel Dreissena
polymorpha (Bivalvia: Mytilidae) highly infected by Sphenophrya
dreissenae, was observed hyperplasia, cell hypertrophy and epitheli-
um vacuolization (Laruelle et al., 1999).
Ancistrocoma sp. is other ciliate that was observed in oysters of the
present study in low intensity and caused no damages or host defense
responses. Nascimento et al. (1986), also reported no damage in
C. rhizophorae from Bahia affected by Ancistrocoma sp.
Steinhausia sp. was observed in oocytes of C. gigas and of
C. rhizophorae in both locations. The presence of the sporocysts with
pathogen spores caused damage to the normal structure of the
cytoplasm of oocytes, but it was not observed defense cells close to the
infected oocytes. In M. galloprovincialis (Bivalvia: Mytilidae) infected
with Steinhausia, it was not also observed infiltration of hemocytes
(Robledo et al., 1994). Instead, the cockle C. edule infected by
Steinhausia-type microsporidia showed a light hemocytic response
without, however, causing significant pathologic damage to the host
(Carballal et al., 2001). Oysters Saccostrea glomerata from Australia,
infected with this microsporidian, showed a complete reabsorption of
the oocytes with infection of germinal epithelium and high hemocytes
infiltration (Green et al., 2008). The prevalences of Steinhausia
observed in the present work was considered high (up 33.3%) when
compared to 6.6% detected in Mytella guyanensis from Amazon
River (Matos et al., 2005), 9% for C. gigas (Pontinha, 2009) and 7.5%
for A. brasiliana in Santa Catarina (da Silva et al., 2010). However, the
highest prevalence found in this study was similar to that recorded
in Brachidontes solisianus from Santa Catarina (37.5%) (Pontinha et al.,
2010).
Gregarines of genus Nematopsis were detected in 100% of the
oysters C. rhizophorae from Sambaqui. However, it was not observed
defense response of the oysters. The protozoan Nematopsis uses
bivalves as intermediate host and completes its life cycle in marine
arthropods (Lauckner, 1983; McGladdery et al., 2006). The higher
prevalence of Nematopsis in oysters from the rocky shore could be
related to the closer proximity of crustaceans in the shores. On the
other hand, the lower prevalence of this pathogen would be
associated to a small amount of these animals in the cultivation
lanterns. Boehs et al. (2010) found higher prevalences of Nematopsis
in M. guyanensis collected in mangrove areas when compared to those
found in A. brasiliana, and reported that the abundance of crustaceans
in the estuary could have contributed to the differences in the found
prevalences. High prevalences of Nematopsis in scallops A. tehuelchus
in Argentina (100%) did not induce host defense reactions (Cremonte
et al., 2005). In C. rhizophorae from Jaguaribe River, Ceará State,
defense reactions were observed as evidenced by the infiltration of
hemocytes (Sabry et al., 2007). High intensities of infection by
Nematopsis sp. also caused changes in the morphology of the gills
and mantle of M. guyanensis from the estuarine region of Cachoeira
River, BA (Pinto and Boehs, 2008). In the cockle A. brasiliana from the
same estuary, it was not observed tissue damage or infiltration of
hemocytes in infected animals (Boehs et al., 2010). Nematopsis sp.
was associated to complete destruction of gills cells and mortality in
the cockle C. edule from the south region of Portugal (Azevedo
and Cachola, 1992). In these cockles from Spain, the presence of
Nematopsis caused mild lesions in the gill filaments and induced a
light hemocytic response without, however, causing mortality
(Carballal et al., 2001). It is noteworthy that in the present study
 R.C. Sabry et al. / Aquaculture 60 (2011) 43–50
the RFTM technique proved to be useful for diagnosing Nematopsis.
The analysis of gills revealed high prevalence of this protozoan,
proving to be a sensitive technique, helping the histology.
Metazoan of genus Urastoma (Turbellaria) were detected free
among the gill filaments of the oysters C. gigas and C. rhizophorae in
this study and did not cause any apparent damage in the gills. The
prevalence as well as the levels of infestation by this organism was
low. In Atlantic coast of Canada, infestations by Urastoma cyprinae in
oysters Crassostrea virginica were very high: up to 1,000 parasites by
individuals with prevalences up to 100%. However, there was no
histopathological damage in the gills (McGladdery et al., 2006). In
oysters C. gigas from Sambaqui infected by a cestode larva of
Tylocephalum, there was a host response, as evidenced by a layer of
cells of fibrous nature, besides the infiltration of hemocytes forming
encapsulation of the parasite. The host response against the parasite
may vary among the affected species (Lauckner, 1983). According to
Figueras and Villalba (1988), the response of C. gigas when infested by
Tylocephalum seems to be less intense than in other bivalves. In
bivalves of genus Pinctada, the capsule formation is not so pronounced
and so it is believed that the oysters belonging to this genus are
normal intermediate hosts of this parasite since the host defense
response is less intense (Lauckner, 1983). In oysters C. rhizophorae
from Bahia, Tylocephalum larvae were responsible for damage of
mechanical nature evidenced by disruption of tissues during the
penetration of the cestodes (Nascimento et al., 1986).
The copepod found in the mangrove oyster C. rhizophorae from
Ribeirão da Ilha, possibly belonged to the genus Pseudomyicola. This
copepod caused damage to the epithelial tissue of the stomach of the
oyster C. rhizophorae, probably due to its large size and the presence of the
animal appendages. In the Pectinidae Argopecten ventricosus from Mexico,
Cáceres-Martínez et al. (2005) also observed erosions in the epithelium of
the stomach and gill, light infiltration of hemocytes and alterations in the
basal membrane of ephitelium caused by the appendages of P. spinosus.
The prevalence of copepods in A. ventricosus (100%) and in M.
galloprovincialis (93.3%) from Mexico (Cáceres-Martínez et al., 2005;
Cáceres-Martínez and Váquez-Yeomans, 1997) was quite high when
compared to the prevalence of 3.3% observed in the present study.
None of the pathogens found in this study seem to cause
significant damage in the oysters, taking into account the low
intensity of infection and infestation that were observed and, in the
most animals, absence of pathological effects. Although the found
pathogens are not in the list of obligatory notification of OIE, it's
necessary a constant monitoring of shellfish populations in order to
assess more accurately the effects of these pathogens in their hosts,
mainly in stressful situations that could serve as factor for triggering
non-apparent infections. Furthermore, bivalve mollusks have great
socioeconomic importance for the State of Santa Catarina, deserving
special attention regarding the health of these animals.
Acknowledgments
The authors are grateful to the National Council for Scientifical and
Technological Development (CNPq) for financial support, through the
annoucement of MCT/CNPq/MAPA/SDA, for the Post-Doctoral Schol-
arship to Patricia Mirella da Silva and to the Improvement Coordina-
tion of Personnel of Superior Level (CAPES) for the Doctoral
Scholarship of the Amazônia Azul Program to Rachel C. Sabry. To
Dr. Jaime F. Ferreira and to shellfish farmer Rita C. Rodrigues for the
support and oysters supply. To MSc. Maximiano P. Dantas Neto for
editing this English version.
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