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Health assessment of the oyster Crassostrea rhizophorae on the southern coast of Bahia, northeastern Brazil

Avaliação da saúde da ostra Crassostrea rhizophorae no Litoral Sul da Bahia, nordeste do Brasil

Abstracts

This study investigated the health of natural stocks of the oysterCrassostrea rhizophorae on the southern coast of Bahia in northeastern Brazil, during summer and winter 2010, at three localities (sampling points) in the estuaries of the Maraú (Camamu Bay) and Graciosa rivers. A total of 180 oysters (30/sampling point/season) were examined macroscopically for the presence of pathogens and anatomical changes. The specimens were subsequently fixed in Davidson solution, processed for paraffin embedding, sectioned and stained with Harris' hematoxylin and eosin. Histological analysis revealed the presence of Rickettsia-like organisms (RLOs), Ancistrocoma,Trichodina, Sphenophrya,Nematopsis, Urastoma,Bucephalus in the sporocyst phase, a nonspecific metacercaria, and a metacestode of genus Tylocephalum. The prevalence of infection was low except for parasitism byNematopsis sp. which also caused histopathological changes. The presence of Bucephalus sp. caused parasitic castration. These two pathogens significantly affect the health of C. rhizophorae.

Oysters; parasitism; pathogen; Bucephalus ; Nematopsis ; Bahia - Brazil


Este estudo investigou a saúde de ostras da espécieCrassostrea rhizophorae de estoques naturais do Litoral Sul do Estado da Bahia, Nordeste do Brasil, durante o verão e o inverno de 2010, em três pontos amostrais distribuídos nos estuários dos rios Maraú (Baía de Camamu) e Graciosa. Um total de 180 ostras (30/ponto amostral/período) foram examinadas macroscopicamente para a presença de patógenos e alterações anatômicas e posteriormente fixadas em solução de Davidson, processadas para inclusão em parafina, seccionadas e coradas com hematoxilina de Harris e eosina. A análise histológica evidenciou a presença de organismos com características similares a Rickettsia(RLOs), Ancistrocoma, Trichodina,Sphenophrya, Nematopsis,Urastoma, Bucephalus em fase esporocística, metacercária inespecífica e metacestóide de Tylocephalum. As prevalências de infecção foram baixas, com exceção do parasitismo por Nematopsis sp., o qual também causou alterações histopatológicas. A presença deBucephalus sp. causou castração parasitária. Esses dois patógenos têm interferência significativa na saúde de C. rhizophorae.

Ostras; parasitismo; patógeno; Bucephalus ; Nematopsis ; Bahia - Brasil


Introduction

Diseases are one of the main limiting factors for the cultivation of marine bivalves (BOWER et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4(1): 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
http://dx.doi.org/10.1016/0959-8030(94)9...
;VILLALBA et al., 1997Villalba A, Mourelle SG, Carballal MJ, López C. Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rías of Galicia (NW Spain). Dis Aquat Org 1997; 31(2): 127-139. http://dx.doi.org/10.3354/dao031127
http://dx.doi.org/10.3354/dao031127...
). On the Brazilian coast, the main pathogens recorded in bivalve mollusks include bacteria, protozoans, fungi and others (MAGALHÃES; FERREIRA, 2006Magalhães ARM, Ferreira JF. Patologias e manejo em malacocultura. In: Souza-Silva AT. Sanidade de Organismos Aquáticos no Brasil. Maringá: ABRAPOA; 2006. p. 79-94.; BOEHS et al., 2012Boehs G, Magalhães ARM, Sabry RC, Ceuta LO. Parasitos e patologias de bivalves marinhos de importância econômica da costa brasileira. In: Silva-Souza AT, Lizama MLA, Takemoto R, organizadores. Patologia e Sanidade de Organismos Aquáticos. Maringá: ABRAPOA; 2012.). The bacterial Rickettsia-like organisms (RLOs) occur in several bivalves (PONTINHA, 2009Pontinha VA. Diagnóstico da saúde da ostra Crassostrea gigas (Thunberg, 1793) cultivada em Florianópolis/SC [Dissertação]. Florianópolis: Universidade Federal de Santa Catarina; 2009.; BOEHS et al., 2010Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
; DA SILVA et al., 2011; SABRY et al., 2011Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
; CEUTA; BOEHS, 2012Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
). The review by Boehs et al. (2012)Boehs G, Magalhães ARM, Sabry RC, Ceuta LO. Parasitos e patologias de bivalves marinhos de importância econômica da costa brasileira. In: Silva-Souza AT, Lizama MLA, Takemoto R, organizadores. Patologia e Sanidade de Organismos Aquáticos. Maringá: ABRAPOA; 2012. listed protozoans of phyla Ciliophora, Apicomplexa, Perkinsozoa and Microspora, and metazoan parasites of the groups Turbellaria, Digenea, Cestoda, Polychaeta, Pinnotheridae and Copepoda.

Crassostrea rhizophorae (Guilding, 1828) (Bivalvia: Ostreidae), popularly known as the mangrove oyster, is naturally distributed from the Caribbean to Uruguay. It settles on consolidated substrates, mainly rhizophores of the red mangrove Rhizophora mangle L. in coves, bays and estuaries (RIOS, 2009Rios EC. Compendium of Brazilian Sea shells. Rio Grande: Evangraf; 2009.). This oyster is now being cultivated on the southern coast of Bahia; however, there is little information about potential diseases that can affect this bivalve, either farmed or in the natural environment. This study evaluated the health of natural populations of C. rhizophorae in this region, with the main goal of developing supporting information for oyster farming. The study included identification of pathogens, analyses of prevalence and intensity of infection, and characterization of the infection site and histopathological changes induced by each parasite.

Materials and Methods

The southern coast of Bahia State in northeastern Brazil is approximately 300 km long, extending from Valença to Canavieiras municipalities. Camamu Bay, approximately 384 km2 in area, includes the Maraú River estuary of approximately 119 km2 (SOUZA-LIMA et al., 2003Souza-Lima W, Manso CLC, Andrade EJE, Grillo JL. Bacias Sedimentares Brasileiras, Bacia de Camamu. Rio de Janeiro: Fundação Paleontológica Phoenix, Editora Interciência; 2003. PMid:12941581.); Graciosa River is located to the north (Figure 1). Small oyster farms culturing C. rhizophorae are located in both places.

Figure 1.
Map of Bahia State and indicating the sampling localities on the southern coast (1 = Ilha do Caranguejo; 2 = Maraú; 3 = Graciosa).

The samples were collected at three localities (collection points): Caranguejo Island = Point 1 (13° 58’ 36” S and 39° 00’ 03” W) and Maraú = Point 2 (14° 06’ 55” S and 39° 02’ 08” W) in the Maraú River estuary (Camamu Bay); and Graciosa = Point 3 (13° 29’ 16” S and 39° 05’ 56” W) in the Graciosa River estuary (Figure 1). Together with the biological samples, the temperature and salinity of each locality were measured using, respectively, a standard mercury thermometer and an Atago S/Mill manual optical refractometer. Thirty specimens of C. rhizophoraewere collected at each sampling point in summer (February/March) and winter (July/August) 2010. The oysters were removed from natural beds in mangroves with the aid of a machete, and taken fresh to the Laboratory of Animal Histology of the Universidade Estadual de Santa Cruz (UESC), where they were immediately processed. Initially, with the aid of a digital caliper, the oysters were measured on the longest axis of the body (=height), as proposed by Galtsoff (1964)Galtsoff PS. The American oyster Crassostrea virginica (Gmelin). US Government Printing Office, Washington, D.C. US Fish Wildlife Service 1964; 64(1): 480., and then opened with a knife. Each specimen was inspected macroscopically for the presence of macroparasites or signs of tissue alterations. Then, with the aid of surgical scissors and a scalpel, a diagonal section about 5 mm thick was taken from each specimen, including the mantle, gills, gonad and digestive tract. The sections were immediately fixed in Davidson's solution (SHAW; BATTLE, 1957Shaw BL, Battle HI. The gross and microscopic anatomy of the digestive tract of the oyster Crassostrea virginica (Gmelin). Can J Zool 1957; 35(1): 325-347. http://dx.doi.org/10.1139/z57-026
http://dx.doi.org/10.1139/z57-026...
) and after 24 hours were transferred to 70% ethanol. The tissues were processed by routine histological techniques for paraffin embedding. Histological sections 7 µm thick were stained with Harris' hematoxylin and eosin (H&E) according to the protocol of Howard et al. (2004)Howard DW, Lewis EJ, Keller BJ, Smith CS. Histological techniques for marine bivalve mollusks and crustaceans. NOAA Technical Memorandum NCCOS 2004; 5(1): 1-218. and analyzed by light microscopy.

Pathogens were analyzed according to their prevalence (no. of infected individuals/no. of individuals analyzed) and sites of infection. The intensity of the infection by pathogens that occupied large areas of tissue was calculated using the stereology technique of Lowe et al. (1994)Lowe DM, Salkeld PN, Carr MR. The effect of geographical location on the cellular composition of the mantle tissue of the mussel, Mytilus edulis. J Mar Biol Assoc UK 1994; 74(1): 225-232. http://dx.doi.org/10.1017/S0025315400035785
http://dx.doi.org/10.1017/S0025315400035...
, using a Weibel morphometric scale. The tissue area occupied by pathogens (TP) was evaluated in five fields randomly chosen from each infection site (organ) of several specimens, and the mean number in each organ and among the total number of animals were calculated, resulting in Nematopsis sp.: N = 30; Bucephalus sp.: N = 1. The result was classified according to Lowe et al. (1994)Lowe DM, Salkeld PN, Carr MR. The effect of geographical location on the cellular composition of the mantle tissue of the mussel, Mytilus edulis. J Mar Biol Assoc UK 1994; 74(1): 225-232. http://dx.doi.org/10.1017/S0025315400035785
http://dx.doi.org/10.1017/S0025315400035...
: I - light infection = <5% TP; II - moderate = 5-25%; III - high = 25-50%; and IV - very high = >50%. Less intense infections were counted and quantified as no. pathogens/histological section.

Results

The temperature was similar in the sampling points, and slightly lower in winter (Table 1). Salinity was high (29 and 31) at Point 1 near the entrance to Camamu Bay; slightly lower (28 and 24) at Point 2, located farther upstream in the Maraú River; and varied widely (0 and 29) at Point 3 (Table 1).

Table 1.
Temperature (T) and salinity (S) values and pathogens associated with Crassostrea rhizophorae, with respective prevalences (%) in Camamu Bay (points 1 and 2) and Graciosa River (Point 3) in February/March (summer) and July/August (winter) 2010. NI = non-identified; RLOs = Rickettsia-like organisms; N = Number.

There was no macroscopic evidence of pathogens or signs of histopathological changes. Microscopic analysis revealed nine different pathogens including bacteria, protozoans and metazoans. Rickettsia-like organisms (RLOs) and the protozoan Nematopsis sp. were present in all samples from both estuaries. Specimens of three groups of ciliates, a metacercaria, and the cestode Tylocephalum sp. occurred only in oysters from Camamu Bay. Urastoma sp. (Turbellaria) and Bucephalus sp. (Digenea) were found only in oysters from Graciosa estuary (Table 1).

The RLOs were observed as individual colonies in the cytoplasm of epithelial cells of the digestive gland, in prevalence from 3.3% to 13.3%, with slightly higher frequencies at Point 2, especially in summer (Table 1). The round colonies measured between 8 and 10 µm in diameter and occurred in low intensity of infection (1-3 colonies/histological section) (Figure 2a). These bacteria did not cause a hemocyte response, but in all cases the epithelial host cells were hypertrophic, and some were in partial lysis.

Figure 2.
Bacteria and protozoa (indicated by arrows) associated with Crassostrea rhizophorae at three points in two estuaries (Maraú = Camamu Bay and Graciosa) on the southern coast of Bahia. a) Intracellular colony ofRickettsia-like organisms (RLOs) in a cell that is separating from the digestive tubule epithelium. Bar = 20 µm. b) Ancistrocoma sp. in the lumen of the secondary digestive duct. Bar = 20 µm. c) Trichodina sp. in the lumen of a secondary digestive duct. Bar = 10 µm. d)Sphenophrya sp. in the gills, with initial xenoma. Bar = 20 µm. e) Intrahemocytic oocysts ofNematopsis sp. in high infection intensity in gills. Bar: 10 µm. f) Phagocyte containing eight oocysts of Nematopsis sp. Bar = 20 µm.

Among protozoa, ciliates of the genera Ancistrocoma,Trichodina and Sphenophrya were observed in Camamu Bay, and gregarines of the genus Nematopsis(Apicomplexa) were observed in both estuaries, consisting of one morphotype for each genus (Table 1). Ancistrocoma sp. (Ciliophora: Ancistrocomidae) occurred in the lumen of the digestive tubules and between the gill filaments. These rounded to oval ciliates measured between 12 and 20 µm in length (Figure 2b) and occurred in low prevalence (3.3-10%); the highest frequency was recorded at Point 2 during summer (Table 1). The intensity of the infection was low (1-2 individuals/histological section) and caused no evident damage to the host.

Trichodina sp. (Ciliophora: Trichodinidae), was observed in prevalence from 3.3% to 13.3%, and similarly toAncistrocoma, had the highest prevalence recorded at Point 2 during summer (Table 1). This ciliate measured between 5 and 40 µm in diameter, occurred near the mantle and in the lumen of the digestive-gland tubules, with low infection intensity (1-3 individuals/histological section) and caused no evident damage to the host (Figure 2c).

Sphenophrya sp. (Ciliophora: Sphenophryidae) was found in the gills of only two oysters from Point 1 (Table 1) and in both it formed a xenoma (Figure 2d), a hypertrophy of the epithelial cells and their nuclei. In both cases only one xenoma/histological section was observed. Apart from the effect at the cell level, apparently the xenomas did not cause significant damage to the host.

Intrahemocytic oocysts of Nematopsis sp. (Eugregarinida: Porosporidae) (Figures 2e, f) were observed at all three sampling points and in both seasons, in prevalences from 20 to 100%; the highest prevalence occurred at Point 3 (Table 1). The highest frequency of these pathogens was observed in the mantle and digestive gland, but they also occurred in the gills and gonads. The number of oocysts/phagocytes varied between 1 and 8 (Figures 2e, f). The intensity of the infection was usually light (<5% TP). In most cases this protozoan did not cause a hemocytic reaction or tissue damage. However, one oyster with high infection intensity in the mantle (TP = 47.6%) and gills (TP = 50.5%) showed extensive hemocyte infiltration and tissue destruction, especially in the gills (Figure 2e).

Among metazoans, only representatives of the phylum Platyhelminthes were observed: helminthes of genus Urastoma (Turbellaria), a trematode in the sporocyst phase of the genus Bucephalus, an unidentified metacercaria, and a cestode of the genus Tylocephalum. Urastoma sp. (Turbellaria: Urastomidae) (Figure 3a) was present only in oysters from Point 3, with prevalences of 6.7% in summer and 16.6% in winter (Table 1). This turbellarian was found in the gills and mantle connective tissue, with 1-2 individuals/histological section, measuring between 150 and 200 µm in length. No tissue immunological response or apparent histological damage was observed.

Figure 3.
Metazoans (indicated by arrows) associated withCrassostrea rhizophorae at three localities (sampling points) in two estuaries (Maraú = Camamu Bay and Graciosa) on the southern coast of Bahia. a) Urastoma sp. in connective tissue surrounding the digestive gland. Bar = 50 µm. b) Sporocyst ofBucephalus sp. containing germ masses and cercariae. Bar = 50 µm. c)Bucephalus sp. in high infection intensity, with destruction of reproductive follicles and connective tissue of the mantle. Bar = 50 µm. d) Nonspecific metacercaria in the mantle. Bar = 20 µm. e)Tylocephalum sp. reabsorbed between acini of the digestive gland. Bar = 50 µm.

The digenetic trematode Bucephalus sp. (Digenea: Bucephalidae), in the sporocyst phase – with germ masses and cercariae (identifiable by the forked tail with a very short and wide base) was observed in only one oyster from Point 3, during winter. The infection intensity was high in the gills (TP = 36.2%) and very high in the gonads (TP = 86.7%); the parasite caused castration, with complete destruction of follicles and germ cells, and made it impossible to determine the sex (Figures 3b, c).

Organisms with morphological characteristics of metacercariae (15 and 20 µm in diameter) were observed; however, taxonomic identification was not possible (Figure 3d). Metacercariae were observed in the mantle of one oyster and in the digestive gland of another, both at Point 2, in low infection intensity (1-2 individuals/histological section), in winter. Histopathological changes were not observed.

Metacestodes of Tylocephalum sp. (Cestoda: Tetragonocephalidae), measuring between 120 and 200 µm diameter, including the encapsulation reaction, were seen in oysters at points 1 and 2 in prevalence from 3.3% to 13.3%, with low infection intensity (1-2 individuals/histological section). The larvae were observed in the connective tissue between the acini of the digestive gland. All oysters parasitized by this cestode showed an intense hemocytic reaction and fibrosis of the connective tissue, encapsulation of the parasite and in some cases its reabsorption (Figure 3e).

Discussion

With the exception of Bucephalus sp. andNematopsis sp., all pathogens found in this study caused no evident histopathological changes in the oysters. The high prevalence ofNematopsis coincided with observations by Jones (1975)Jones JB. Nematopsis n. sp. (Sporozoa: Gregarina) in Perna canaliculus. NZ J Mar Freshw Res 1975; 9(4): 567-568.http://dx.doi.org/10.1080/00288330.1975.9515590
http://dx.doi.org/10.1080/00288330.1975....
in Perna canaliculus (Gmelin, 1791) from New Zealand; Cáceres-Martínez et al. (2010)Cáceres-Martínez J, Vásquez-Yeomans R, Padilla-Lardizábal G. Parasites of the pleasure oyster Crassostrea corteziensis cultured in Nayarit, México. J Aquat Anim Health 2010; 22(3): 141-151. PMid:21192543. http://dx.doi.org/10.1577/H09-052.1
http://dx.doi.org/10.1577/H09-052.1...
in Crassostrea corteziensis(Hertlein, 1951) from Mexico; Nascimento et al. (1986)Nascimento IA, Smith DH, Kern II, Pereira SA. Pathological findings in Crassostrea rhizophorae from Todos os Santos Bay, Bahia, Brazil. J Invertebr Pathol 1986; 47(3): 340-349. http://dx.doi.org/10.1016/0022-2011(86)90105-9
http://dx.doi.org/10.1016/0022-2011(86)9...
(Bahia, Brazil),Sabry et al. (2007)Sabry RC, Gesteira TCV, Boehs G. First record of parasitism in the mangrove oyster Crassostrea rhizophorae (Bivalvia: Ostreidae) at Jaguaribe River estuary - Ceará, Brazil. Braz J Biol 2007; 67(4): 755-758. PMid:18278331. http://dx.doi.org/10.1590/S1519-69842007000400024
http://dx.doi.org/10.1590/S1519-69842007...
(Ceará, northeastern Brazil) and Sabry et al. (2011)Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
(Santa Catarina, southern Brazil) in C. rhizophorae; and by Pinto and Boehs (2008)Pinto TR, Boehs G. Nematopsis sp. (Apicomplexa: Eugregarinida) em Mytella guyanensis (Lamarck, 1819) (Bivalvia: Mytilidae) da região estuarina do Rio Cachoeira, Ilhéus, Bahia, Brasil. Braz J Vet Res Anim Sci 2008; 45(2): 95-100. and Ceuta and Boehs (2012)Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
inMytella guyanensis (Lamarck, 1819) from the Cachoeira River in Bahia and from Camamu Bay, respectively. Azevedo and Cachola (1992)Azevedo C, Cachola R. Fine structure of the Apicomplexa oocyst of Nematopsis sp. of two marine bivalve molluscs. Dis Aquat Org 1992; 14(1): 69-73. http://dx.doi.org/10.3354/dao014069
http://dx.doi.org/10.3354/dao014069...
observed a high prevalence of Nematopsis sp. in Cerastoderma edule(Linnaeus, 1758) from Portugal, and related it to high mortality of this bivalve. According to Bower et al. (1994)Bower SM, McGladdery SE, Price IM. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4(1): 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
http://dx.doi.org/10.1016/0959-8030(94)9...
, when present in low infection rates in the mollusk, this protozoan causes only hemocytic infiltration; however, at high levels it may cause gill destruction, tissue degeneration and death. In this study, one heavily infected oyster showed histopathological changes, consisting of destruction of gill filaments and connective tissue, which may have compromised the physiology of the gills. Ceuta and Boehs (2012)Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
observed tissue alteration in the labial palps of heavily infected M. guyanensis, suggesting functional impairment of this organ. In this study, due to obvious histopathological changes in at least one specimen ofC. rhizophorae and its high prevalence in the region, we suggest that this pathogen should be monitored, especially in oyster farms.

Although the digenetic Bucephalus sp. showed low prevalence, the oyster infected by this pathogen showed destruction of gonad tissue, causing parasitic castration. Castration caused by this parasite was also observed in C. rhizophorae (NASCIMENTO et al., 1986Nascimento IA, Smith DH, Kern II, Pereira SA. Pathological findings in Crassostrea rhizophorae from Todos os Santos Bay, Bahia, Brazil. J Invertebr Pathol 1986; 47(3): 340-349. http://dx.doi.org/10.1016/0022-2011(86)90105-9
http://dx.doi.org/10.1016/0022-2011(86)9...
; ZEIDAN et al., 2012), M. guyanensis (BOEHS et al., 2010Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
; CEUTA; BOEHS, 2012Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
; ZEIDAN et al., 2012), Anomalocardia brasiliana (Gmelin, 1791) (BOEHS et al., 2010Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
) and Perna perna (Linnaeus, 1758) (DA SILVA et al., 2002, 2011; GARCIA; MAGALHÃES, 2008Garcia P, Magalhães ARM. Protocolo de identificação e quantificação de bucefalose (enfermidade laranja) em mexilhões Perna perna. Bol Inst Pesca 2008; 34(1): 11-19.). These last authors observed moderate (TP = 5-50%) to high (TP > 50%) infection intensity.

Rickettsia-like organisms (RLOs) have been previously observed in the digestive epithelial cells of several species of bivalves from the Brazilian coast: the mussel M. guyanensis (BOEHS et al., 2010Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
; CEUTA; BOEHS, 2012Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
) and the oysters C. rhizophorae (DA SILVA et al., 2011; SABRY et al., 2011Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
; ZEIDAN et al., 2012) andCrassostrea gigas (Thunberg, 1793) (PONTINHA, 2009Pontinha VA. Diagnóstico da saúde da ostra Crassostrea gigas (Thunberg, 1793) cultivada em Florianópolis/SC [Dissertação]. Florianópolis: Universidade Federal de Santa Catarina; 2009.; DA SILVA et al., 2011), with similar low prevalences (except for SABRY et al., 2011Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
, who observed a prevalence of up to 30%) and low infection intensities, without causing disease, as reported in a review by Bower et al. (1994)Bower SM, McGladdery SE, Price IM. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4(1): 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
http://dx.doi.org/10.1016/0959-8030(94)9...
for oysters in general. These organisms can also be found, apart from digestive tubules (primary and secondary, as recorded in the present study) in the epithelium of the intestine and stomach (CÁCERES-MARTÍNEZ et al., 2010Cáceres-Martínez J, Vásquez-Yeomans R, Padilla-Lardizábal G. Parasites of the pleasure oyster Crassostrea corteziensis cultured in Nayarit, México. J Aquat Anim Health 2010; 22(3): 141-151. PMid:21192543. http://dx.doi.org/10.1577/H09-052.1
http://dx.doi.org/10.1577/H09-052.1...
), as reported by Sabry et al. (2011)Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
, who observed changes in the gastric epithelium affected. The results of this study also resemble those found by Boehs et al. (2010)Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
in M. guyanensis, with the occurrence of these bacteria in the same anatomical region and low prevalence and degree of infection; and by Pontinha (2009)Pontinha VA. Diagnóstico da saúde da ostra Crassostrea gigas (Thunberg, 1793) cultivada em Florianópolis/SC [Dissertação]. Florianópolis: Universidade Federal de Santa Catarina; 2009., Da Silva et al. (2011) and Ceuta and Boehs (2012)Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
, in C. gigas, C. rhizophorae and M. guyanensis, respectively, with the occurrence of hypertrophy of cells infected by RLOs.

With respect to the ciliates observed in this study (Sphenophrya, Trichodina andAncistrocoma), the proximity between points 1 and 2 and the similarity of the abiotic conditions of temperature and salinity explain their presence in both locations. No histopathological alteration caused by them was noticeable, and it is possible that these are, for mollusks, closer to commensals than parasites, as suggested by Lauckner (1983). However, if present in large quantity, these ciliates possibly may affect the functioning of the gills, causing changes in the respiratory and feeding functions. Specifically,Sphenophrya can cause a tumor called xenoma, i.e., a hypertrophy of the infected cell, including its nucleus (BOWER et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4(1): 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
http://dx.doi.org/10.1016/0959-8030(94)9...
). The first report of xenoma formation in C. rhizophorae was by Boehs et al. (2009)Boehs G, Lenz TM, Villalba A. Xenomas in Crassostrea rhizophorae (Ostreidae) from Camamu Bay, Bahia, Brazil. Braz J Biol 2009; 69(2): 457-458. PMid:19675953. http://dx.doi.org/10.1590/S1519-69842009000200032
http://dx.doi.org/10.1590/S1519-69842009...
in Camamu Bay in an area close to points 1 and 2 of this study, and was associated with this ciliate by the authors. As in this study, the authors reported a low prevalence.Sphenophrya sp. was previously recorded in Todos os Santos Bay (Bahia) in C. rhizophorae, by Nascimento et al. (1986)Nascimento IA, Smith DH, Kern II, Pereira SA. Pathological findings in Crassostrea rhizophorae from Todos os Santos Bay, Bahia, Brazil. J Invertebr Pathol 1986; 47(3): 340-349. http://dx.doi.org/10.1016/0022-2011(86)90105-9
http://dx.doi.org/10.1016/0022-2011(86)9...
, in low prevalence and intensity of infection, but these authors did not report the formation of xenomas. In C. rhizophorae and C. gigas at the Island of Santa Catarina, even at sites with a high prevalence (70%), there were no reports of defense reaction or formation of xenomas (DA SILVA et al., 2011; SABRY et al., 2011Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
).

With respect to Trichodina, although it has been associated with mortality of marine animals (BOWER et al., 1994Bower SM, McGladdery SE, Price IM. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 1994; 4(1): 1-199. http://dx.doi.org/10.1016/0959-8030(94)90028-0
http://dx.doi.org/10.1016/0959-8030(94)9...
), this ciliate did not cause damage in the oysters analyzed here. The horseshoe-shaped basophile nucleus was similar to previous observations for other host species, with varying prevalences (BOEHS; MAGALHÃES, 2004Boehs G, Magalhães ARM. Simbiontes associados com Anomalocardia brasiliana (Gmelin) (Mollusca, Bivalvia, Veneridae) na Ilha de Santa Catarina e região continental adjacente, Santa Catarina, Brasil. Rev Bras Zool 2004; 21(4): 865-869. http://dx.doi.org/10.1590/S0101-81752004000400021
http://dx.doi.org/10.1590/S0101-81752004...
; PONTINHA, 2009Pontinha VA. Diagnóstico da saúde da ostra Crassostrea gigas (Thunberg, 1793) cultivada em Florianópolis/SC [Dissertação]. Florianópolis: Universidade Federal de Santa Catarina; 2009.; DA SILVA et al., 2011; SABRY et al., 2011Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
). There are indications that localities with high levels of organic pollution have increased the abundance of this ciliate, and accordingly some investigators believe that it has potential for use as a bioindicator (MARCOGLIESE; CONE, 1997Marcogliese DJ, Cone DK. Parasite communities as indicators of ecosystem stress. Parassitologia 1997; 39(3): 227-232. PMid:9802071.; PALM; DOBBERSTEIN, 1999Palm HW, Dobberstein RC. Occurrence of trichodinid ciliates (Peritricha: Urceolariidae) in the Kiel Fjord, Baltic Sea, and its possible use as a biological indicator. Parasitol Res 1999; 85(8-9): 726-732. PMid:10431740. http://dx.doi.org/10.1007/s004360050622
http://dx.doi.org/10.1007/s004360050622...
; OGUT; PALM, 2005Ogut H, Palm HW. Seasonal dynamics of Trichodina spp. on whiting (Merlangius merlangus) in relation to organic pollution on the eastern Black Sea coast of Turkey. Parasitol Res 2005; 96(3): 149-153. PMid:15856300. http://dx.doi.org/10.1007/s00436-005-1346-2
http://dx.doi.org/10.1007/s00436-005-134...
; AKŞIT et al., 2008Akşit D, Falakali-Mutaf B, Göçmen B, Gürelli G. A preliminary observations on Trichodina sp. (Ciliophora: Peritricha) on the gills of limpets (Patella spp.) in Antalya (Turkey). North-West J Zool 2008; 4(2): 295-299.). The low prevalence of this protozoan in the study region may suggest a low environmental impact by domestic sewage and other pollutants. The absence of damage and host defense response were also observed with respect to the ciliate Ancistrocoma, according to studies by Pontinha (2009)Pontinha VA. Diagnóstico da saúde da ostra Crassostrea gigas (Thunberg, 1793) cultivada em Florianópolis/SC [Dissertação]. Florianópolis: Universidade Federal de Santa Catarina; 2009. and Sabry et al. (2011)Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
in C. gigas; and for C. rhizophorae by Sabry et al. (2011)Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
and Zeidan et al. (2012).

Metacercariae, observed in low prevalence in oysters only at Point 2, were present in the gills and digestive gland. Boehs et al. (2010)Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
observed unidentified metacercariae in the digestive gland of A. brasiliana and in the gonad ofIphigenia brasiliana (Lamarck, 1818), and Da Silva et al. (2011) in the kidney of A. brasiliana, in low prevalences. In the bivalve Tagelus plebeius(Lightfoot, 1786) studied at the Island of Santa Catarina, metacercariae of the genus Parvatrema (Cable, 1953) were observed in the mantle and labial palps, with high prevalence (up to 100%) and induced hyperplasia; metacercariae of the family Echinostomatidae were observed with lower prevalence, infecting the gonad connective tissue (DA SILVA et al., 2009). Tegumentary spines were seen on the metacercariae in this study, as reported elsewhere (CREMONTE et al., 2005Cremonte F, Balseiro P, Figueras A. Occurrence of Perkinsus olseni (Protozoa: Apicomplexa) and other parasites in the venerid commercial clam Pitar rostrata from Uruguay, southwestern Atlantic coast. Dis Aquat Org 2005; 64(1): 85-90. PMid:15900692. http://dx.doi.org/10.3354/dao064085
http://dx.doi.org/10.3354/dao064085...
; BOEHS et al., 2010Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
), but it was not possible to identify this trematode.

Regarding the cestode Tylocephalum, the pathogen encapsulation response by the host was observed in all oysters parasitized. Ceuta and Boehs (2012)Ceuta LO, Boehs G. Parasites of mangrove mussel Mytella guyanensis (Bivalvia: Mytilidae) of Camamu Bay, Bahia, Brazil. Braz J Biol 2012; 72(3): 421-427. PMid:22990810. http://dx.doi.org/10.1590/S1519-69842012000300002
http://dx.doi.org/10.1590/S1519-69842012...
observed the same response in M. guyanensis from Camamu Bay, but no other histopathological damage to the host. These same authors also found that the parasite occurred in the mantle connective tissue. In addition to the mantle, in the present study the metacestode was also found in the connective tissue between the acini of the digestive gland, as observed by Sabry et al. (2007)Sabry RC, Gesteira TCV, Boehs G. First record of parasitism in the mangrove oyster Crassostrea rhizophorae (Bivalvia: Ostreidae) at Jaguaribe River estuary - Ceará, Brazil. Braz J Biol 2007; 67(4): 755-758. PMid:18278331. http://dx.doi.org/10.1590/S1519-69842007000400024
http://dx.doi.org/10.1590/S1519-69842007...
in C. rhizophorae, Boehs et al. (2010)Boehs G, Villalba A, Ceuta LO, Luz JR. Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). J Invertebr Pathol 2010; 103(1): 43-47. PMid:19850046. http://dx.doi.org/10.1016/j.jip.2009.10.008
http://dx.doi.org/10.1016/j.jip.2009.10....
in A. brasiliana and I. brasiliana, Da Silva et al. (2011) in Perna perna and Sabry et al. (2011)Sabry RC, Da Silva PM, Gesteira TCV, Pontinha VA, Magalhães, ARM. Pathological study of oysters Crassostrea gigas from culture and C. rhizophorae from natural stock of Santa Catarina Island, SC, Brazil. Aquaculture 2011; 320(1-2): 43-50. http://dx.doi.org/10.1016/j.aquaculture.2011.08.006
http://dx.doi.org/10.1016/j.aquaculture....
in C. gigas.

In this study, although certain pathogens occurred at only some of the sampling points and estuaries, it was not possible to make inferences about the existence of a spatial-temporal pattern, or to establish correlations with temperature and salinity, given the specific character of the sampling. The ecology of parasitic infections of mollusks in Brazil is still in an initial phase, and many aspects need to be further researched for a better understanding, not only of the relationship of pathogens to the environment, but also to the host.

Conclusion

The low prevalence and infection intensity found in this study indicate that the natural population of C. rhizophorae is in good general health on the southern coast of Bahia. This is most likely associated with the good environmental quality in this region. However, we believe that the digenetic trematode Bucephalus sp. and the protozoanNematopsis sp., when at high levels of infection, may threaten the health of C. rhizophorae. Constant health monitoring can promote the sustainability of local oyster farming. Studies are needed to clarify the ecological relationships between these pathogens and this host; seek possible control methods; and evaluate possible zoonotic aspects associated with the consumption of this oyster.

Acknowledgements

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for financing the project (ID 477317/2008-1); Coordenação de Pessoal de Nível Superior (CAPES, Brazil) for the master's degree scholarship awarded to the first author; Guidomar Soledade and Mariane Aguiar Luz for their help in laboratory processing; and Janet W. Reid for revising the English.

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Publication Dates

  • Publication in this collection
    19 Mar 2013
  • Date of issue
    Jan-Mar 2013

History

  • Received
    24 June 2012
  • Accepted
    29 Oct 2012
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br