Printer Friendly

First description of symbionts, parasites, and diseases of the Pacific geoduck Panopea generosa from the Pacific Coast of Baja California, Mexico.

ABSTRACT The Pacific geoduck Panopea generosa is distributed along the Pacific coast of the peninsula of Baja California, Mexico. Because of its high market value, this species has been under an intensive fishery pressure during the last few years, whereas its experimental aquaculture production is still developing. The fishery and culture practices point to the movement of clams as a risk factor for dispersion of symbionts, parasites, and diseases. Wild geoduck clams from fishery captures are sent to facilities that maintain clams alive, before marketing. Some of them show external abnormalities such as weakness and flaccidity, blisters, and darkening and thickening of the mantle surface and siphon. The objective of this study was to determinate if these abnormalities were related to parasites or diseases through conventional parasitological and histological analyses. The parasitological analysis showed two species of copepods, Pseudomyicola spinosus and a calanoid species in the mantle cavity and gills; additionally, a turbellarian species was also observed in the mantle cavity, none of these symbionts were related to tissue damage. The histological analysis showed that some weak-flaccid clams were in a postspawning condition. The dark and thick areas of the siphon and mantle suffered a dramatic transformation of the periostracum into a cavernous structure with numerous protozoans in different developmental stages. Fungi were occasionally observed in the external area of the periostracum. Unusual mortalities were reported by producers in clams with this abnormality. Rickettsia-like inclusions and trematodes were found in the digestive gland associated with limited damage to the host. The darkening and thickening of the siphon represent a major issue because of the negative appearance of the clams, which prevents its sale and is possibly related to the unusual mortality episodes. Detailed field and laboratory studies are needed to determine the origin of this pathology as well as its distribution and effect on the survival of the host. Moreover, field studies on the distribution, prevalence, and intensity of the other symbionts and parasites here detected are needed. These data constitute the first record for organisms associated with P. generosa in Mexico and a baseline for future studies.

KEY WORDS: Pacific geoduck, Panopea generosa, parasites, diseases, symbionts, sanitary control

INTRODUCTION

The fishery of the Pacific geoduck Panopea generosa (Gould, 1850) in Mexico has been increasing year by year because of its high demand in the international market. Production values have increased from 38 tons in 2002 to 2,000 tons in 2011 (Aragon-Noriega et al. 2012, Ramirez-Felix et al. 2012). The market value of this production is estimated to be around $15 million (SAGARPA 2010). Thus, an increase in fishing pressure is expected in the coming years as well as the development and establishment of repopulation strategies and commercial aquaculture production.

Among fishery practices, the relocation and transportation of live animals between different fishery areas and the transportation of commercial stocks to maintenance facilities before their sale are considered common activities. These practices mixe clams from distinct areas. Similarly, another aquaculture practice is the capture of wild adult clams for use as breeding stock. These practices represent a risk due to the possible dispersion of symbionts, parasites, and diseases. One effective disease management strategy includes knowledge of the symbionts, parasites, and diseases that could be transferred among clams and which of them are susceptible to control efforts.

There are several examples of dispersion of symbionts, parasites, and diseases because of the ignorance on this biological principle. The prevalence of perkinsosis caused by Perkinsus marinus and haplosporidosis caused by Haplosporidium nelsoni, two major oyster diseases which are considered by the World Organization of Animal Health as reportable agents has increased among the American oyster Crassostrea virginica and can be attributed to the relocation of infected stocks along the eastern and southern U.S. coasts (Andrews 1996, Cook et al. 1998, Hofmann et al. 2001). From the east coast of United States and the Gulf of Mexico, P. marinus has been transferred, in infected oysters for commercial and aquaculture purposes, to the Pacific coast of Mexico (Caceres-Martinez et al. 2008). The causal agent of the withering syndrome, Candidatus Xenohaliotis californiensis, which is also considered by the World Organization of Animal Health as reportable, has extended its distribution range in California via transportation of the hatchery-reared red abalone Haliotis rufescens (Friedman & Finley 2003) and has been confirmed in Chile, China, Taiwan, Iceland, Ireland, Israel, Spain, Thailand, and Japan, where infected abalone has been introduced for aquaculture production (Crosson et al. 2014). Several parasites, symbionts, and diseases have been introduced into new areas through increased shipment of host shellfish for marketing and aquaculture (Elston et al. 1986, Bustnes et al. 2000, Caceres-Martinez et al. 2008).

The movement of clams and intensification of aquatic production of Panopea generosa in Mexico increases the likelihood of symbiont, parasite, and disease dispersal. In this sense, the objective of this study was to identify the different symbionts, parasites, and diseases of geoduck clams from two facilities where producers maintain organisms alive before marketing

MATERIALS AND METHODS

Samplings

In August 2012 and June 2014, 6 and 20 adult geoduck clams from the Pacific coast of Baja California from two facilities, where producers maintain organisms alive before marketing, were sent in portable ice boxes to the laboratories of CICESE and ISA for examination. The initial shipment, from the first facility, included three clams chosen by the producers because these organisms presented weakness and flaccidity of the mantle and siphon, and one organism that had two blisters in the base of the siphon. These clams were considered to have an unhealthy appearance. Another three clams with a vigorous appearance and a hard consistency of the mantle and siphon were also sent for comparison. These clams were considered to have a healthy appearance. External analysis corroborated the weakened appearance, observations showed a slow response in the retraction of the mantle or siphon when physically stimulated. In consequence, the geoduck clams with a vigorous appearance were corroborated by a fast response to retract the mantle or siphon when stimulated.

Organisms of the second shipment were chosen by the producers from another facility, based on a dark coloration or spots that were present in the soft body and siphon, and this characteristic differentiated them from clams that did not have a dark coloration or spots. Producers reported unusual mortalities in clams that presented the dark coloration or spots in the soft body and siphon.

External Examination

Upon arrival to the laboratory, clams were rinsed with running sea water and measured in centimeters from the anterior to the posterior edge of the shell; subsequently, a stereomicroscopic examination of the shell and siphon was carried out. Fractions of tissue with the presence or absence of abnormalities from the siphon surface were taken and processed for histopathology as described below.

Histological Examination

The soft body was separated from the valves and was fixed in Davidson's fluid by a series of injections and immersion in the fixative in separate glass bottles for at least 24 h (Shaw & Battle 1957). In accordance with Howard and Smith (2004), a cross-section of the visceral mass, including gonadal tissue, was taken; additionally, samples of gills and mantle were taken. Tissues from the siphon, visceral mass, gills, and mantle were processed embedded in paraffin wax, sectioned at 5-6 [micro]m, and stained with hematoxylin and eosin. Slides were examined under a compound microscope at 100-1,000 times magnification. A photographic record of abnormalities, symbionts, and parasites was obtained.

Copepods and turbellarians were fixed in 70% ethanol. Symbionts and parasites were identified to the most precise taxonomic level with the aid of taxonomic keys and literature (von Graff 1913, Ho 1980, Do & Kajihara 1986).

RESULTS

External Examination

The mean size of the clams from the first sampling was 13.4 [+ or -] 0.9 cm. The external appearance of the siphon, mantle, and shell was normal with the exception of one weak-flaccid clam that presented two big blisters filled with a clear fluid (Fig. 1A, B). One platyhelminth belonging to the order of turbellarians with two pigmented frontal eyes and an orange-pink coloration (Fig. 1C, D) was found crawling in the fluid in the mantle of a healthy clam. On the mantle and gills, the myicolid copepod Pseudomyicola spinosus (Fig. IE) was observed in one weak-flaccid clam and in one healthy clam.

Clams from the second sampling had a mean size of 12.8 [+ or -] 1.4 cm. All clams showed dark and thickening areas of the external surface of the mantle and siphon. The alteration was located indistinctly over localized areas of the surface of the mantle and siphon. The smallest damaged areas correspond to dark spots of ~ 1 [cm.sup.2] to large damaged areas which extended from the base to the top covering up to 40% of the mantle and siphon (Fig. 2A). Visually, the external aspect was of a dark and parched surface. The periostracum was easily separated from the subjacent tissue and muscle (Fig. 2B, D). Under a stereomicroscope, the tissue showed a dry or burned appearance (Fig. 2B, C).

Histological Examination

The histological analysis of the blisters did not show any particular abnormality. From the three healthy clams, two were males and one was a female in final spawning conditions with residual gametes, whereas the weak-flaccid clams were undifferentiated with empty and contracted follicles.

Examination of the lesions from the second clam sample showed a severe alteration of the periostracum (integument with two organic layers placed over epithelial cells and the muscle) in all affected clams. The external layer of the periostracum completely lost its normal structure (Fig. 3A) and it was transformed into a cavernous form (Fig. 3B, C). The second layer also looked altered in some cases (Fig. 3B). The caverns in the periostracum were invaded by many protozoa (Fig. 3C, D). These small round protozoa were present in all cases; these parasites were attached to the inner surface of the cavernous periostracum or in the middle of the cavern and could also be observed alone or inside of an apparent mother cell (Fig. 3E). In two occasions, hyphae of fungi in the external zone of the siphon (Fig. 3F) were observed.

One calanoid copepod species (Fig. IF) was detected in the mantle area. The turbellarian observed in the first sampling (Fig. 1C) was also detected. Other parasites detected by histology were basophilic inclusions of Rickettsia-like organisms inside hypertrophied epithelial cells of the secondary digestive diverticula (Fig. 4A). Apart from the hypertrophic cell, there was no other evidence of the activation of the defense mechanisms of the host. Metacercaria stages of a trematode were observed in the lumen of the intestine (Fig. 4B). No apparent reaction of the defense mechanisms of the host was observed. The histological analysis reveals that the sex proportion was 1:1.

DISCUSSION

Information about the health of the Pacific geoduck Panopea generosa is scarce. The most complete health survey on this species was conducted by Bower and Blackbourn (2003), which sampled wild and cultured P. generosa. The study was carried out on the coast of British Columbia (BC) in Canada in the 1990s and allows a qualitative comparison of similar results and demonstrates a new and broader distribution for some of the symbionts, parasites, and diseases found in BC and now in Baja California. Other results presented here constitute novel records for some species. Recently, Dorfmeier et al. (2015) found new endosymbionts of the geoduck clam P. generosa that had not been detected in Puget Sound, WA. None of the endosymbionts detected in the study by Dorfmeier et al. (2015) were detected in this study with the exception of Rickettsia-like organisms; however, the Rickettsia-like organisms in this study exhibit a distinct tissue distribution.

Blisters in the siphon and mantle of the Pacific geoduck clam Panopea generosa in Canada were recorded by Bower and Blackbourn (2003); these blisters are swellings that contain a clear fluid of unknown origin and effect. No obvious infectious agents were observed in association with these lesions by the mentioned authors or in the present study. Detailed studies are needed to determine the origin and the effect of this alteration on the host.

On the other side, Bower and Blackbourn (2003) report that some geoducks (Panopea generosa) collected in BC had dark thickened integument (periostracum) on the siphon and/or mantle that appeared brown or black. Bower and Blackbourn (2003) named this alteration as the dark leathery surface of geoduck clams (LSGC) because of its external appearance. Their histological analysis showed that the integument was affected but the underlying epithelium and the musculature were always intact. Additionally, Bower and Blackbourn (2003) found that in other geoduck clams with LSGC, the outer acellular layer of the periostracum was inhabited by unknown organisms. In a few cases, the periostracum was full of numerous holes, some of which were occupied by protozoa. In other cases, protozoa and a fungus were present.

Contrary to this, in this study all clams affected by the darkening of the siphon showed a cavernous first layer of periostracum and in some occasions, the second layer was also disrupted. In all cases, numerous protozoans in different developmental stages were observed attached to the caverns or in the middle of the caverns. Moreover, Mexican producers indicate unusual mortality of clams with this alteration. This pathology seems to represent a major issue because it directly alters the appearance of the product which affects its marketing as it is mentioned by Bower and Blackbourn (2003). Furthermore, even when these authors did not relate this condition to important mortalities, information from Mexican producers is contradictory to that of the Canadian producers. The clear deformation of the periostracum, which is one of the first barriers against diseases, is compromised, indicating a greater risk for health problems of clams; thus, the role of this pathology in the survival of the host must be entirely assessed.

Bower and Blackbourn (2003) found that a fungal infection was frequently associated with the LSGC of geoduck clams from the east and west coast of Vancouver Island, but not in clams collected from two areas on the central coast of BC. According to Bower and Blackbourn (2003), the fungus invaded the two acellular layers forming the integument of the siphon and mantle, but did not penetrate into the epithelium or into the musculature. In the present study fungi hyphae were detected in two cases and were observed in the external zone of the external layer of the periostracum. Studies conducted by Bower and Blackbourn (2003), to determine if fungi are the causal agent of the LSGC, have not been conclusive; therefore, it is fundamental to determine if fungi, protozoans or both of them are the causative agent of the disruption, possible secondary invaders, or if these alterations are caused by other factors.

The weak-flaccid appearance, observed in the clams from the first sampling, seems to be related with the postspawning condition of the clams with empty and contracted follicles. In accordance with Calderon-Aguilera et al. (2014), the reproductive cycle of Panopea generosa in the Pacific coast of Baja California begins in late autumn, with a developing phase in winter and continuous proliferation and spawning from April throughout October. This coincides with the time when clams were sent to the laboratory. After spawning organisms lose energy and become exhausted, this condition can be reflected in weakness and flaccidity of the tissues. Handling of the clams from fishery areas to reception facilities before marketing could also contribute to the weakened and exhausted appearance of the clams. Additionally, no infectious agents were found that could be related to the external weak-flaccid appearances of the clams.

Among other symbionts and parasites recorded here is the myicolid copepod Pseudomyicola spinosus that was observed crawling in the mantle cavity and gills of the clam, a finding that represents a new host for this parasite, which has been previously detected in the Pacific coast of Baja California inhabiting in the California mussel Mytilus califomianus and in the blue mussel Mytilus galtoprovincialis (Caceres-Martinez et al. 1996). This copepod has been associated with 54 species of bivalve mollusks in temperate and tropical waters around the world (Humes 1968, Ho & Kim 1991, Ho 1996). Dinamani and Gordon (1974), and Olivas-Valdez and Caceres-Martinez (2002) have described damages in the digestive gland and a negative effect in the condition of oysters and mussels infected by this parasite. The body form of this copepod in adult stages is slender and cannot swim freely supporting its parasitic adaptation. In this study, the presence of this parasite was minimal and no damage was observed. On the other hand, the number of the calanoid copepod found in the second sampling was greater than those recorded for Pseudomyicola spinosus; this copepod can swim freely and it did not present any obvious adaptation to parasitism. No damage was associated to this symbiont. The presence in Panopea generosa must be studied to understand and define the type of interaction between the copepod and the clam.

Several planarians are known to affect bivalve mollusks, and among them turbellarians of the orders Rhabdocoela and Prolecithophora have been detected in the mantle cavity, gills, and alimentary tract of their host. In Modiolus plicatulus, Paravortex gemellipara has been found; Urastoma cyprinae in Mytilus edulis, Mytilus califomianus, and Modiolus modiolus; and Urastoma sp. in Nodipecten subnodosus (Dorler 1900, Jennings 1971, Tyler & Burt 1988, Caceres-Martinez & Vasquez-Yeomans 1999, Caceres-Martinez 2001). Pathological effects of U. cyprinae on the gills of Mytilus galloprovincialis have been described by Robledo et al. (1994a) and Caceres-Martinez et al. (1998), although the negative effect on the condition of the host seems to be limited and some species have been described as commensals without causing any kind of damage to their hosts. An unidentified turbellarian has also been recorded in Panopea generosa from Canada which did not evoke a host response and was not associated with losses (Bower 2002, Bower & Blackbourn 2003). In the geoduck Panopea abbreviata from the Patagonian Gulf, Argentina, Paracortex panopea n. sp. was detected (Brusa et al. 2011), which is similar in shape, form, and color to the turbellarian found in this study, and no evidences of direct physical damage were observed. Detailed studies are needed to identify the turbellarian found in this study and to determine the nature of its relationship with P. generosa.

The presence of Rickettsia-like inclusions is relatively common in marine bivalves and has been associated with disruption of the epithelial cells but not with mortality episodes (Lauckner 1983, Bower et al. 1994, Aguirre-Macedo et al. 2007, Caceres-Martinez et al. 2010). Bower and Blackbourn (2003) recorded the presence of Rickettsiales-like bacterium not associated with host response or losses. Dorfmeier et al. (2015) frequently observed Rickettsia-like inclusions within ctenidial epithelia and found that the prevalence increased in summer, but there was no association with tissue damages or mortalities. The Rickettsia-like inclusions observed in the present study were inside of epithelial cells of the secondary digestive diverticuli in the digestive gland, not within ctenidial epithelia, suggesting possibly different parasites to those described by Dorfmeier et al. (2015). The limited damage associated to this organism does not appear to represent a health problem to the host. On the other hand, the recurrent presence of Rickettsia-like inclusions in various bivalve species indicates the need for more detailed taxonomic and physiological studies of these prokaryotes and of their possible effects on their hosts.

Trematodes in the digestive tract of bivalve mollusks is common and can be associated with true damages depending on the species; for example, sporocyst containing cercariae of Proctoeces macidatus or Cercaria tapidis may induce castration in the blue mussel Mytilus galloprovincialis and in the Manila clam Ruditapes philippinarum, respectively (Robledo et al. 1994b, Lee et al. 2001), whereas others are considered innocuous to their host (Bower et al. 1994). In the present study, trematode larvae seem to have a low negative effect on the clam because of the low number of parasites and absence of visible damages to the host. No relationship was observed in any case between the sex of the host and symbionts, parasites, or diseases; although evidently, the small size of sample limits this observation.

The qualitative data shown here constitute new records for the presence and distribution of parasites and abnormalities of Panopea generosa as well as records of new symbionts and parasites for this species, which constitute a baseline for more detailed studies on parasites and diseases for the Pacific geoduck clam.

ACKNOWLEDGMENTS

This study was partially funded by projects from CICESE (no. 623106) and from ISA (no. Pg586587). We thank Jose Carlos Garduno Franco from Marino Pacifico S. A. and Mrs. Leonor Mazuda Mora for providing us with samples; and M. C. Yanet Guerrero Renteria and Gissel Tinoco Orta for technical assistance in histological processing and measurement procedures.

LITERATURE CITED

Andrews, J. D. 1996. History of Perkinsus marinus, a pathogen of oysters in Chesapeake Bay 1950-1984. J. Shellfish Res. 15:13-16.

Aguirre-Macedo, M. L., R. A. Sima-Alvarez, M. K. Roman-Magana & J. I. Guemez-Ricalde. 2007. Parasite survey of the eastern oyster Crassostrea virginica in coastal lagoons of the southern Gulf of Mexico. J. Aquat. Anim. Health 19:270-279.

Aragon-Noriega, E. A., E. Alcantara-Razo, L. E. Calderon-Aguilera & R. Sanchez-Fourcade. 2012. Status of geoduck clam fisheries in Mexico. J. Shellfish Res. 31:733-738.

Bower, S. M. 2002. Synopsis of infectious diseases and parasites of commercially exploited shellfish: Gregarine parasitism of clams and cockles. Available at: http://www.pac.dfo-mpo.gc.ca/sci/shelldis/ pages/gregpcc_e.htm.

Bower, S. M. & J. Blackbourn. 2003. Geoduck clam (Panopea abrupta): anatomy, histology, development, pathology, parasites and symbionts: lesions of unknown cause on geoduck clams. Available at: http://www-sci.pac.dfo-mpo.gc.ca/geoduck/warts_e.htm.

Bower, S. M., S. E. McGladdery & I. M. Price. 1994. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu. Rev. Fish Dis. 4:1-199.

Bustnes, J. O., K. V. Galaktionov & S. W. B. Irwin. 2000. Potential threats to litoral biodiversity: is increased parasitism a consequence of human activity? Oikos 90:189-190.

Brusa, F., N. Vazquez & F. Cremonte. 2011. Paravortex panopea n. sp. (Platyhelminthes: Rhabdocoela) on clams from the northern Patagonian coast, Argentina: pathogeny and specificity. Helminthologia 48:94-100.

Caceres-Martinez, J. 2001. Parasitology of Iberoamerican scallops. In: A. Maeda-Martinez, editor. Los Moluscos Pectinidos de Iberoamerica: Ciencia y Acuicultura. Editorial Noriega-Limusa, Mexico, pp. 343-356.

Caceres-Martinez, J., R. Vasquez-Yeomans & E. Suarez-Morales. 1996. Two parasitic copepods, Pseudomyicola spinosus and Modiolicola gracilis associated with edible mussels, Mytilus galloprovincialis and Mytilus californianus from Baja California NW Mexico. J. Shellfish Res. 15:45-49.

Caceres-Martinez, J., R. Vasquez-Yeomans & R. Sluys. 1998. The turbellarian Urastoma cyprinae (Platyhelminthes: Urastomidae) associated with natural and commercial populations of Mytilus galloprovincialis and Mytilus californianus from Baja California, NW Mexico. J. Invertebr. Pathol. 72:214-219.

Caceres-Martinez, J. & R. Vasquez-Yeomans. 1999. Metazoan parasites and pearls in coexisting mussel species: Mytilus californianus, Mytilus galloprovincialis and Septifer bifurcatus, from an exposed rocky shore in Baja California, NW Mexico. Veliger 42:10-16.

Caceres-Martinez, J., R. Vasquez-Yeomans, G. Padilla-Lardizabal & M. A. del Rio-Portilla. 2008. Perkinsus marinus in pleasure oyster Crassostrea corteziensis from Nayarit, Pacific Coast of Mexico. J. Invertebr. Pathol. 99:66-73.

Caceres-Martinez, J., R. Vasquez-Yeomans & G. Padilla-Lardizabal. 2010. Parasites of the pleasure oyster Crassostrea corteziensis cultured in Nayarit, Mexico. J. Aquat. Anim. Health 22:141-151.

Calderon-Aguilera, L., E. A. Aragon-Noriega, E. Morales-Bojorquez, E. Alcantara-Razo & J. Chavez-Villalba. 2014. Reproductive cycle of the geoduck clam Panopea generosa at its southernmost distribution limit. Mar. Biol. Res. 10:61-72.

Cook, T., M. Folli, J. Klinck, S. Ford & J. Miller. 1998. The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar. Coast. Shelf Sci. 46:587-597.

Crosson, L. M., N. Wight, G. R. VanBlaricom, I. Kiryu, J. D. Moore & C. S. Friedman. 2014. Abalone withering syndrome: distribution, impacts, current diagnostic methods and new findings. Dis. Aquat. Organ. 108:261-270.

Dinamani, P. & D. B. Gordon. 1974. On the habits and nature of association of the copepod Pseudomyicola spinosus with the rock oyster Crassostrea glomerata in New Zealand. J. Invertebr. Pathol. 24:305-310.

Do, T. T. & T. Kajihara. 1986. Studies on parasitic copepod fauna and biology of Pseudomyicola spinosus, associated with the blue mussel Mytilus edulis galloprovincialis in Japan. Bull. Ocean Res. Inst. Univ. Tokyo 23:1-65.

Dorfmeier, E.M., B.Vadopalas, P. Frelier & C. S. Friedman. 2015. Temporal and spatial variability of native geoduck (Panopea generosa) endosymbionts in the Pacific Northwest. J. Shellfish Res. 34:81-90.

Dorler, A. 1900. Neue und wenig bekannte rhabdocole Turbellarien. Z. Wiss. Zool. 68:1-42.

Elston, R. A., C. A. Farley & M. L. Kent. 1986. Occurrence and significance of bonamiasis in Europena flat oysters Ostrea edulis in North America. Dis. Aquat. Organ. 2:49-54.

Friedman, C. S. & C. A. Finley. 2003. Anthropogenic introduction of the etiological agent of withering syndrome into northern California abalone populations via conservation efforts. Can. J. Fish. Aquat. Sci. 60:1424-1431.

Ho, J. S. 1980. Origin and dispersal of Mytilus edulis in Japan deduced from its present status of copepod parasitism. Publ. Seto Mar. Biol. Lab. 25:293-313.

Ho, J. S. 1996. Myicolid copepods and mass mortality of cultured hard clams (Merethrix). Phuket Mar. Biol. Ctr. Spe. Publ. 16:61-70.

Ho, J. S. & I. H. Kim. 1991. Copepod parasites of commercial bivalves in Korea. II. Copepods from cultured bivalves. Bull. Korean Fish. Soc. 24:369-396.

Hofmann, E., S. Ford, E. Powell & J. Klinck. 2001. Modeling studies of the effect of climate variability on MSX disease in eastern oyster (Crassostrea virginica) populations. Hydrobiologia 460:195-212.

Howard, D. W. & C. S. Smith. 2004. Histological techniques for marine bivalve mollusks. NOAA Technical Memorandum NMFS-F/NEC-25. Woods Hole, MA: U.S. Department of Commerce. 218 pp.

Humes, A. G. 1968. The cyclopoid copepod Pseudomyicola spinosus (Raffaele and Monticelli) from marine pelecypods, chiefly in Bermuda and the West Indies. Beaufortia 14:203-226.

Jennings, J. B. 1971. Parasitism and commensalism in the Turbellaria. Adv. ParasitoI. 9:1-32.

Lauckner, G. 1983. Diseases of Mollusca: Bivalvia. In: O. Kinne, editor. Diseases of marine animals. Vol. II, Introduction, Bivalvia to Scaphopoda.Hamburg: Biologische Anstalt Helgoland, pp. 630-632.

Lee, M.-K., B.-Y. Cho, S.-J. Lee, J.-Y. Kang, H. D. Jeong, S. H. Huh & M.-D. Huh. 2001. Histopathological lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture 201:199-209.

Olivas-Valdez, J. & J. Caceres-Martinez. 2002. Infestation of the blue mussel Mytilus galloprovincialis by the copepod Pseudomyicola spinosus and its relations with size, density and condition index of the host. J. Invertebr. Pathol. 79:65-71.

Ramirez-Felix, E., J. F. Marquez-Farias, J. A. Masso-Rojas, E. Vazquez-Solorzano & S. G. Castillo-Vargasmachuca. 2012. La pesca de almeja Panopea. Cienc. Pesq. 20:57-66.

Robledo, J. A. F., J. Caceres-Martinez & A. Figueras. 1994a. The parasitic turbellarian Urastoma cyprinae (Platyhelminthes: Urastomidae) from blue mussel Mytilus galloprovincialis in Spain: occurrence and pathology. Dis. Aquat. Organ. 18:203-210.

Robledo, J. A. F., J. Caceres-Martinez & A. Figueras. 1994b. Mytilicola intestinalis and Proctoeces maculatus in mussel (Mytilus galloprovincialis Lmk.) beds in Spain. Bull. Eur. Assoc. Fish Pathol. 14:89-91.

SAGARPA. 2010. Anuario estadistico de acuicultura y pesca 2008. Secretaria de Agricultura, Ganaderia, Desarrollo Rural, Pesca y Alimentacion.Mexico: Comision Nacional de Acuicultura y Pesca. 213 pp.

Shaw, B. L. & H. I. Battle. 1957. The gross microscopic anatomy of the digestive gland of the oyster Crassostrea virginica (Gmelin). Can. J. Zool. 35:325-346.

Tyler, S. & M. D. B. Burt. 1988. Lensing by mitochondrial derivative in the eye of Urastoma cyprinae (Turbellaria, Prolecithophora). Fortschr. Zool. 36:229-234.

von Graff, L. 1913. Platyhelminthes. Turbellaria. II Rhabdocoelida. In: F. E. Schulze, editor. Das Tierreich. Eine Zusammenstellung und Kennzeichnung der rezeten Tierformen, 35. Lieferung. Berlin: Friedlander. 484 pp.

JORGE CACERES-MARTINEZ, (1,2) * REBECA VASQUEZ-YEOMANS (2) AND ROBERTO CRUZ-FLORES (1)

(1) Centro de Investigation Cientifica y de Education Superior de Ensenada, Carretera Ensenada-Tijuana No. 3918, Zona Playitas, 22860, Ensenada, Baja California, Mexico; (2) Instituto de Sanidad Acuicola, A.C. Calle de la Marina S/Nesq. Caracoles, Fracc. Playa Ensenada, 22880, Ensenada, Baja California, Mexico

* Corresponding author. E-mail: jcaceres@cicese.mx

DOI: 10.2983/035.034.0304
COPYRIGHT 2015 National Shellfisheries Association, Inc.
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2015 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Caceres-Martinez, Jorge; Vasquez-Yeomans, Rebeca; Cruz-Flores, Roberto
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1MEX
Date:Dec 1, 2015
Words:4651
Previous Article:Quality indices as potential markers indicating the origin of cultured scallop (Argopecten irradians) in the North China Sea.
Next Article:Assessing potential benthic impacts of harvesting the Pacific geoduck clam Panopea generosa in intertidal and subtidal sites in British Columbia,...
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters |