Parasitol Res (2006) 99: 566–571 DOI 10.1007/s00436-006-0193-0 ORIGINAL PAPER Francisco Brusa . Rodrigo Ponce de León . Cristina Damborenea A new Paravortex (Platyhelminthes, Dalyellioida) endoparasite of Mesodesma mactroides (Bivalvia, Mesodesmatidae) from Uruguay Received: 4 January 2006 / Accepted: 22 March 2006 / Published online: 3 May 2006 # Springer-Verlag 2006 Abstract Many species of turbellarians (Platyhelminthes) are known to live associated with other organisms, especially invertebrates, as commensals or parasites. The family Graffillidae (Rhabdocoela) includes two genera that parasitize mollusks, Graffílla and Paravortex. Within the latter genus, six species were described as associated with mollusks. In other instances, unnamed Paravortex species were mentioned as parasites of other bivalves and of the body surface of fishes. In the present work, a new Paravortex species that was found in the intestine of Mesodesma mactroides from the Atlantic coast of Uruguay is described. In addition, a bibliographical revision of the known Paravortex species with their respective hosts, location, and distribution is made. Paravortex nicolli, described by Szidat for the Argentinean coast, is mentioned for the first time after the original description, and the authorship and date of description of Paravortex tapetis Noury-Sraïri 1989 are elucidated. Introduction Numerous species of turbellarians are known to live associated with other organisms, especially invertebrates, either as commensals or parasites (Jennings 1971). Among these, some rhabdocoeles are symbiotically associated with marine and freshwater invertebrates (Cannon 1986). The family Graffillidae includes two genera that parasitize mollusks, Graffílla and Paravortex. The latter genus presently comprises six species that are associated with bivalves. In other cases, unnamed Paravortex species were mentioned as parasites of other bivalves and the body surface of fishes (Cannon and Lester 1988). The species of Paravortex are found primarily within the intestine and accessory organs of their bivalve hosts, with only one species known to be associated with the gills of Geukensia demissa, Crassostrea virginica, and Mytilus edulis (Linton 1910; Ball 1916; Fleming et al. 1981). In spite of the fact that numerous works mention turbellarians in general and especially Paravortex sp. as parasites of bivalves, some of which are of major economic importance, species identification of these parasites is seldom provided. This could be explained by the techniques needed for the identification of these species being different from the traditional methodology applied in routine parasitological studies. Recently, the presence of undetermined turbellarians parasitizing different species of commercial bivalves (Mesodesma mactroides and Pododesmus rudis) in the Argentinean Sea has been mentioned (Cremonte and Figueras 2004; Cremonte et al. 2005). To date, the only Paravortex species known for South America was described by Szidat (1965), found in the intestine of M. edulis platensis at Puerto Quequén in Buenos Aires province, Argentina. The existence of this species has passed unnoticed from its original description to the present contribution. In this work, we describe a new species of Paravortex found at the coasts of República Oriental del Uruguay, in the intestine of M. mactroides. In addition, we provide a bibliographical revision of the known Paravortex species with their respective hosts, locations, and geographical distribution. We mention Paravortex nicolli Szidat 1965, described for Argentinean coasts for the first time since its description, and we elucidate the authorship and descrip- tion date of Paravortex tapetis Noury-Sraïri 1989. F. Brusa (*) . C. Damborenea División Zoología Invertebrados, CONICET, Facultad de Ciencias Naturales y Museo (UNLP), Paseo del Bosque s/n°, CP 1900, La Plata, Buenos Aires, Argentina e-mail: fbrusa@fcnym.unlp.edu.ar Tel.: +54-221-4257744 Fax: +54-221-4257527 R. Ponce de León Facultad de Ciencias, Montevideo, Uruguay Materials and methods Specimens of M. mactroides (Mesodesmatidae) were collected in the tidal zone at Playa de La Coronilla (33° 51′S, 53°30′W), Departamento de Rocha, Uruguay in August 2004. The turbellarians were fixed in hot Bouin. Some of the specimens were prepared in toto and stained with chlorhydric carmine. Seriated 4-μm sagittal sections were made and stained with hematoxylin–eosin. The materials were deposited at the Helminthological Collec- tions of Museo de La Plata, Argentina (MLP) and Facultad de Ciencias, Montevideo, Uruguay (HCFC). Additional materials from the Collection of Invertebrates of Museo Argentino de Ciencias Naturales (MACN), which we deem to correspond with the specimens described by the original author as P. nicolli Szidat 1965, were also examined. Results The turbellarians found in the intestine of M. mactroides were identified as a new species of Paravortex. Prevalence was 91% (ten infected clams out of 11), and mean intensity of infection was 5.7 (SD 3.81). Minimum infection was two turbellarians per host and maximum was 14 turbellar- ians per host. A total of 51 individuals were found, of which 26 were gravid and 25 were juveniles. Paravortex mesodesma sp. n. (Figs. 1 and 2) Description Shape oval, posterior end slightly thinner than anterior end. Live gravid individuals pink with white embryos visible through body wall. Live juveniles paler. Fixed gravid specimens 0.9–1.2 mm long and 0.5–0.6 mm wide, with numerous embryos within parenchyma. Epithelium high (3–3.5 μm), very densely ciliated. Anterior tip with two visible epithelial papillae. Mouth anterior, terminal, incon- spicuous; opening into small oral cavity continued in a small doliform pharynx (41–59 μm long and 36–59 μm wide). Long narrow esophagus (approximately thrice as long as the pharynx) between pharynx and intestine. Intestine formed by a simple blind sac extending near rear end of body. Intestinal cells high and vacuolated, occluding the intestinal lumen in some specimens. Brain dorsal to the esophagus. Nervous fibers extending into anterior region; no posterior nervous fibers were observed. A pair of small black eyes formed by numerous pigmentary spheres associated with the brain and located at esophagus level. Hermaphroditic, both reproductive systems developed simultaneously. Genital pore opening in the anterior midpart of body. Male reproductive system: a pair of testes, elongated, slightly irregular, anterior, lateroventral with respect to esophagus, reaching eye level anteriorly, posteriorly extending to the region occupied by embryos. Deferent duct entering the seminal vesicle anteriorly. Seminal vesicle spherical, large (54 μm in diameter) filled with spermatozoids, in anterior half of body, communicated with the genital atrium. No penis was observed. Female reproductive system: a pair of ovaries, club- shaped, lateral, posterior to the testes, in the second quarter of body. Proximal portion of each ovary with small ovocytes that increase in size toward the rear. Distal portion of each ovary curved toward the middle region and opening into a transversal oviduct connecting with female genital atrium. Atrium covered by high cells and with associated glands. Vitelline glands branched in the rear half of body. Distal part of each gland connected with the oviducts at each side forming the “vitello-oviduct.” Embryos enclosed in very thin capsules within paren- chyma. Generally one pair of embryos inside each capsule, although three were observed in one capsule. Maximum number of embryos 24–34. Rear body always without embryos, containing only intestine and vitelline glands. Embryos lacking cilia and ocular spots at early develop- ment, these structures becoming visible at advanced development stages. Remarks Of the six described Paravortex species, only two occur in America, Paravortex gemellipara (Linton 1910) Ball 1916, found in G. demissa, Ischadium recurvum, Mytilopsis leucophaeata, C. virginica, M. edulis, and P. nicolli in M. edulis platensis (Table 1). Holotype One specimen in toto, MLP Paratypes One specimen in toto and one specimen sagittally sectioned, HCFC; one specimen in toto and three specimens sagittally sectioned, MLP Additional material Several specimens preserved in ethanol 70%, MLP Host M. mactroides Deshayes 1854 Locality Playa de La Coronilla, La Coronilla, Departamento de Rocha, Uruguay (33°51′S, 53°30′W) Site of infection Intestine Etymology The specific name refers to the genus of its host species 567 P. gemellipara is the species most similar to P. mesodesma sp. n. Both are similar in general body shape, position of the pharynx and the genital pore, and shape and position of the ovaries. However, P. gemellipara is white; it reaches a total length of 2 mm. The pharynx is almost circular and approximately 90 μm in diameter (Linton 1910), larger than described in the new species. It has a short esophagus, about 50 μm long, whereas the esophagus of P. mesodesma sp. n. is approximately thrice the length of the pharynx; the seminal vesicle is larger, pyriform, 48 μm long by 51 μm wide dorsally and 34 μm wide ventrally. In addition, a strong muscular sphincter between the female atrium and the common atrium has been described for P. gemellipara (Ball 1916), and such a structure does not appear in P. mesodesma. In P. gemellipara, the female atrium is layered with delicate cells and presents glands that converge at the distal end of the atrium, whereas in P. mesodesma, the cells are high and the glands open along the entire length of the atrium, similar to the condition described by Hallez (1909) for Paravortex cardii (Hallez 1908) Hallez 1908. The vitelline glands of P. gemellipara are generally described as “enormous” (Ball 1916) and each of them originates anterior and posterior branches. On the contrary, in the studied specimens of P. mesodesma sp. n., the vitelline glands are less developed and have only some posterior branches. As described by Ball (1916) for P. gemellipara, in P. mesodesma sp. n. the oviduct is connected with the vitellaria so that they are fused in a “vitello-oviduct,” with vitelline cells in the proximal female atrium. Both species also differ in the arrangement of the embryo capsules. In P. gemellipara, these are distributed throughout the body, from one end to the other (Linton 1910), with records of 22–24 capsules, whereas in P. mesodesma sp. n., embryos are never present in the rear part of the body and the maximum number of capsules observed was 17. Revision and discussion Six species of Paravortex that parasitize marine and estuarine bivalves have been described to date (Table 1). The first three species were described during the late 19th century and the beginning of the 20th century. Paravortex scrobiculariae (von Graff 1882) Wahl 1906 and P. cardii are the best known species, occurring in the intestine and associated glands of European bivalves. P. gemellipara, although originally described as associated with the gills and mantle cavity of G. demissa (Linton 1910; Ball 1916), is currently considered as a parasite of the digestive tract of bivalves of the Atlantic coast in USA and Canada (Jennings and Phillips 1978; Pike and Burt 1981). Two additional species associated with European bivalves were described during the late 20th century: Paravortex karlingi Pike and Burt 1981 and P. tapetis. The latter was described by Noury-Sraïri in 1988 in her doctoral thesis; thus, it was not a valid species according to the requirements of the International Code of Zoological Nomenclature (2000). In view of that, a formal description of the species was provided in a paper by Noury-Sraïri et al. (1989), and its authorship was expressly assigned to Noury- Sraïri (Art. 50.1 of ICZN 2000). Szidat (1965) studied the parasites ofM. edulis platensis in the Argentinean coast, and among these, he described P. nicolli found in the intestine of this mussel. This was the first mention of a Paravortex species for the Neotropical region and in association with a Mytilus species. Exami- nation of the material deposited at MACN did not provide relevant data. The specimens are mounted in toto and stained with carmine. Two of the specimens are juvenile and one is gravid. The latter exhibits the general characters of the genus, with at least two capsules within the parenchyma, the ovary, and part of the male reproductive system. It is worth mentioning that most of the species of this genus exhibit Palearctic geographical distributions (P. scrobiculariae, P. cardii, P. karlingi, and P. tapetis), whereas P. gemellipara is Nearctic, and P. nicolli and P. mesodesma sp. n. are exclusively Neotropical. This predominance of Holarctic species is probably not due to any intrinsic characteristics of the genus, but rather to the Fig. 1 Ventral view of a gravid specimen of Paravortex mesodesma sp. n. Scale, 100 μm. d Deferent duct, e embryo, ey eye, ov ovary, p pharynx, sv seminal vesicle, t testes, v vitellaria, vo vitello-oviduct 568 considerable knowledge of the bivalve fauna in that region, as well as the significant exploitation of bivalves as a fisheries resource. The data presented in this work underline the necessity of further studies of this group within the Neotropical region. Most of the descriptions of the genital system of Paravortex species state its protandry. According to Ball’s (1916) description, in the medium-sized P. gemellipara specimens he studied, the male organs were completely developed, with visible testes, deferent ducts, and a large seminal vesicle; in larger individuals, the testes and their ducts were degenerate, although they remained identifiable. Patterson (1912) affirms that these structures are hardly recognizable in adult specimens. On the contrary, Hallez (1909) states that the testes of P. cardii produce spermatozoids throughout its entire life, even when numerous embryos are found in the parenchyma. In P. mesodesma sp. n., the testes are visible in all the specimens examined. According to the available information, there is no evidence of Paravortex species causing direct damage to their bivalve hosts (Woods and Hayden 1998). Jennings and Phillips (1978) studied aspects of feeding and nutrition in P. scrobiculariae and P. cardii. These species obtain nutrition from the partially digested food of the host and the latter’s enzymes. These remain active inside the intestine of the turbellarians and play an important part in its digestive processes. On the other hand, these parasites are frequently found inside the ducts of the digestive glands and may obstruct them. The yellow clam, M. mactroides, is a bivalve occurring in sandy beaches of the South Atlantic from southern Brazil to Buenos Aires province in Argentina. This bivalve was commercially very important in the area during the decades of 1940 and 1950. Successive mass mortality events occurred first in Brazil, then in Uruguay, and posteriorly in Argentina (Defeo et al. 1992; Fiori and Cazzaniga 1999). Cremonte and Figueras (2004) described the parasitic communities found inside this bivalve at the seashore in Buenos Aires province, with the goal of establishing the sanitary status of the mussel population. In their study, they concluded that the presence of parasitic species could not have caused the mass mortalities. This work is a contribution to the knowledge of the associated fauna of Fig. 2 Microphotographs of Paravortex mesodesma sp. n. Sagittal sections. a detail of female reproductive system; b pharyngeal region; c seminal vesicle and capsule with three embryos; d detail of male re- productive system. Whole mount; e ventral view of a gravid specimen. Scale in a–d, 100 μm. Scale in e, 200 μm. b Brain, d deferent duct, e em- bryo, g gonopore, gl glandules, i intestine, o esophagus, ov ovary, p pharynx, sv seminal vesicle, t testes, v vitellaria, vo vitello-oviduct 569 the yellow mussel; further studies of the turbellarian populations found in other mussel populations could contribute significant information concerning the nature of this association and its importance for the population dynamics of M. mactroides. Acknowledgements We thank Lic. Alejandro Tablado (Museo Argentino de Ciencias Naturales) for making available the specimens of Paravortex nicolli Szidat 1965, Dr. Guido Pastorino and Dr. Florencia Cremonte, who provided specific bibliography. References Atkins D (1934) Two parasites of the common cockle Cardium edule; a rhabdocoele Paravortex cardii Hallez and copepod Paranthessius rostratus (Canu). J Mar Biol Assoc UK 19:669–676 Ball SC (1916) The development of Paravortex gemellipara (Graffilla gemellipara Linton). J Morphol 27:453–558 Belofastova I, Dimitrieva EV (1999) The turbellarians of genus Paravortex (Rhabdocoela: Graffillidae)—parasites of the Black Sea bivalves. Ecol Sea 48:76–78 Cannon LRG (1986) Turbellaria of the world. A guide to families and genera. Queensland Museum, Queensland Cannon LRG, Lester RJG (1988) Two turbellarians parasitic in fish. Dis Aquat Organ 5:15–22 Table 1 Paravortex species known to date with their respective hosts, site of infection, and locality Worm Host Site of infection Locality Paravortex cardii Cerastoderma edule Stomach and intestine English channel (France) (Hallez 1909), English channel (UK) (Atkins 1934) C. edule Digestive gland English channel and North Sea (UK) (Jennings and Phillips 1978), North Sea (UK) (Pike and Burt 1981), Atlantic Ocean (UK) (Noury-Sraïri et al. 1989) C. edule Intestine Atlantic Ocean (Spain) (Carballal et al. 2001) C. edule # Baltic Sea (Zander and Reimer 2002) Cerastoderma lamarki # Black Sea (Ukraine) (Belofastova and Dimitrieva 1999) C. lamarki # Baltic Sea (Zander and Reimer 2002) Macoma balthica # Baltic Sea (Zander and Reimer 2002) Paravortex gemellipara C. edule Mantle cavity English channel (UK) (Leigh-Sharpe 1933) Crassostrea virginica Gills Atlantic Ocean (Canada) (Fleming et al. 1981; Fleming 1986) Geukensia demissa Gills Atlantic Ocean (USA) (Linton 1910; Ball 1916) G. demissa Kidney Atlantic Ocean (USA) (Patterson 1912) G. demissa Intestine and stomach Gulf of Mexico (USA) (Wardle 1980) Ischadium recurvum Intestine and stomach Gulf of Mexico (USA) (Wardle 1980) Mytilopsis leucophaeata Intestine and stomach Gulf of Mexico (USA) (Wardle 1980) Mytilus edulis Gills Atlantic Ocean (Canada) (Fleming et al. 1981) Paravortex karlingi C. edule Intestine North Sea (UK) (Jennings and Phillips 1978), Atlantic Ocean (UK) (Noury-Sraïri et al. 1989) Paravortex nicolli M. edulis platensis Intestine Atlantic Ocean (Argentina) (Szidat 1965) Paravortex scrobiculariae Abra ovata # Black Sea (Ukraine) (Belofastova and Dimitrieva 1999) Abra tenuis # English channel and North Sea (UK) (Gibbs 1982) Ruditapes decussatus Intestine Mediterranean Sea (Italy) (Wahl 1906) Scrobicularia plana Intestine Adriatic Sea (Italy) (Wahl 1906), North Sea (UK) (Freeman 1957) S. plana Intestine and digestive gland North Sea (UK) (Jennings and Phillips 1978) S. plana # English channel and Bristol channel (UK) (Gibbs 1982) Paravortex tapetis R. decussatus Intestine Mediterranean (France) (Noury-Sraïri et al. 1989) R. decussatus Digestive tract Mediterranean (France) (Noury-Sraïri et al. 1995) Number symbols denote data that are not available in the literature 570 Carballal MJ, Iglesias D, Santamarina J, Ferro-Soto B, Villalba A (2001) Parasites and pathologic conditions of the cockle Cerastoderma edule populations of the coast of Galicia (NW Spain). 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Parasitology 124:119–135 571 A new Paravortex (Platyhelminthes, Dalyellioida) endoparasite of Mesodesma mactroides (Bivalvia, Mesodesmatidae) from Uruguay Abstract Introduction Materials and methods Results Description Remarks Revision and discussion References << /ASCII85EncodePages false /AllowTransparency false /AutoPositionEPSFiles true /AutoRotatePages /None /Binding /Left /CalGrayProfile (None) /CalRGBProfile (sRGB IEC61966-2.1) /CalCMYKProfile (ISO Coated) /sRGBProfile (sRGB IEC61966-2.1) /CannotEmbedFontPolicy /Error /CompatibilityLevel 1.3 /CompressObjects /Off /CompressPages true /ConvertImagesToIndexed true /PassThroughJPEGImages true /CreateJDFFile false /CreateJobTicket false /DefaultRenderingIntent /Perceptual /DetectBlends true /ColorConversionStrategy /sRGB /DoThumbnails true /EmbedAllFonts true /EmbedJobOptions true /DSCReportingLevel 0 /EmitDSCWarnings false /EndPage -1 /ImageMemory 524288 /LockDistillerParams true /MaxSubsetPct 100 /Optimize true /OPM 1 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