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Cercarias (Orden: Strigeidae, Diplostomidae) en Biomphalaria straminea (Planorbidae) de un campo de arroz en el Nordeste Argentino.

Cercariae (Digenea: Strigeidae, Diplostomidae) in Biomphalaria straminea (Planorbidae) from a rice field in Northeastern Argentina

The rice fields act as temporary artificial wetlands (Ramsar Convention 2011; http:// www.ramsar.org) due to the alternating periods of flooding in summer and drought in winter. Worldwide, several studies have demonstrated its importance in biological conservation, since can improve habitats for many species of aquatic invertebrates, as insects, molluscs, crustaceans; and vertebrates, as fish, amphibians, reptiles and birds (Bambaradeniya, 2000; Czech & Parsons, 2002; Bambaradeniya & Amerasinghe, 2003; Manley, 2008; Elphick, Parsins, Fasola, & Mugica, 2010). In the Neotropical region, different studies have been carried out about the biodiversity of macro-invertebrates, amphibians, birds and macrophytes in the irrigated channels of rice fields (Blanco, Lopez-Lanus, Dias, Azpiroz, & Rilla, 2006; Stenert, Bacca, Maltchik, & Rocha, 2009; Machado & Maltchik, 2010; Maltchik, Rolon, Stenert, Machado, & Rocha, 2011). Specifically in Northeastern Argentina, the macroinvertebrates, planorbids, amphibians, fish and birds diversity has been the subject of studies in rice fields (Rumi & Hamann, 1990; Dure, Kehr, Schaefer, & Marangoni, 2008; Blanco & de la Balze, 2011). However, the larval trematodes that infect molluscs in these temporary artificial wetlands were little studied (Fernandez, Hamann, & Ostrowski de Nunez, 2013, 2014). The fact that the presence of larval trematodes provides indirect information about occurrence of their hosts highlights the importance of their study to contribute to the knowledge of the biodiversity in these environments.

The species of Biomphalaria Preston, 1910 (Gastropoda: Planorbidae) are widely distributed in Argentina, mainly in the Northeast (Rumi & Nunez, 2013). In particular, Biomphalaria straminea (Dunker, 1848) is more restricted to the Northeast and pampean regions, being very frequent in the Rio de La Plata basin, namely in the Parana and Uruguay rivers (Nunez, Gutierrez Gregoric, & Rumi, 2010; Rumi & Nunez, 2013). This species, natural vector of Schistosoma mansoni Sambon, 1907 in Brazil, inhabits a wide variety of environments, favoring shallow, temporary and standing or slow-flowing freshwater bodies. Thus, rice fields provide favorable conditions for the development of dense populations of this planorbid snail.

In Argentina, the larval trematodes diversity of Biomphalaria species, have been studied mainly in natural environments. Recently, Fernandez et al. (2013, 2014) described larval trematodes in B. straminea from a rice field in Corrientes province, Argentina, one of the main rice producers of Argentina (ACPA, 2014). In this context, the goal of the present work was to complete the description of the cercariae found in the sampling of molluscs of this environment. We provide descriptions of new larval trematodes and assign them to taxonomic families and genera. In some cases, we add data about the period of emergence of cercariae and potential second intermediate hosts, and information about their prevalence.

MATERIALS AND METHODS

The study site was an agricultural area with cultivated rice parcels connected or associated to the Parana river basin, located approximately 30 km South from Corrientes city, in Corrientes province, Argentina (27[degrees]40' N - 58[degrees]48'21.6" W).

Snails were collected during the flooding periods (n= 5 510), from the time of sowing to soon after harvesting of the rice, between December 2010 and May 2011 (n= 3 494), and December 2011 and April 2012 (n= 2 016). Samples were taken manually from the border of cultivated parcels and irrigated channels. Two persons sampled in the morning during 1.5 hours, using simple mesh nets, locally named "copos" (25 cm frame diameter). The width of the studied channels (n= 2) was approximately 2 m, and 260 m in length. In the laboratory, the snails were kept individually in vials with 20 mL of tap water, and were observed for the emergence of cercariae. Seemingly uninfected snails were dissected to check for other larval intramolluscan stages (e.g. immature infections and metacercariae).

Cercariae were studied alive, with and without vital dyes (0.01% aqueous solutions of neutral red and Nile blue sulphat). Drawings were made using a camera lucida attached to a Carl Zeiss Jena microscope. Measurements given in the description of each cercaria are based on heat-killed and formalin-fixed specimens and expressed in micrometers (qm), with range followed by the mean [+ or -] SD in parentheses. We adopted the "open nomenclature" recommended by Odening (1971) for new species of cercariae. Cercariae fixed in hot 4% formalin were preserved in vials with 70% ethanol, and deposited in the Helminthological Collection of the Centro de Ecologia Aplicada del Litoral (CECOAL), Corrientes, Argentina.

Photographs were taken with a Leica DFC 295 camera mounted on a Leica DM 2500 microscope. Specimens to be studied by scanning electron microscopy (SEM) were dehydrated in an ethanol series, dried using the critical point technique, coated with gold-palladium and examined under a Jeol 5800 LV Scanning Electron Microscope.

To determine the second intermediate host, laboratory-reared Cnesterodon sp. were exposed to the emerged cercariae. The fish were maintained in small aquaria under controlled conditions until dissection, which was carried out five hours post-exposure (PE). Overall prevalence of each trematode taxon and prevalence in each season was calculated following Bush, Lafferty, Lotz and Shostak (1997).

RESULTS

A total of 26 snails were infected with the cercariae here described. The prevalence of individual larval trematodes was lower than 1%; Furcocercaria XX and Furcocercaria XIX were present in one rice cultivation cycle, while Furcocercaria V was present in both rice cultivation cycles, with higher prevalence in the second rice cultivation cycle (Fig. 1). The cercariae described are added to 53 previously reported for Biomphalaria spp. in different aquatic environments of Argentina (Table 1).

Superfamily Diplostomoidea Poirier, 1886 Family Diplostomidae Poirier, 1886

Furcocercaria XIX (Figs. 2-4, 12-13)

Prevalence: 0.04%

Specimen deposited: accession number CECOAL 11031417

Description: Measurements based on ten specimens. Body 166-205 (187 [+ or -] 15) long and 44-62 (54 [+ or -] 6) wide. Tegument covered with large spines distributed in 9-10 transverse rows between anterior organ and ventral sucker, posterior spines smaller and scattered in lateral fields. One pair of sensory hairs at level of excretory vesicle. Anterior organ elongateoval, 41-51 (46 [+ or -] 3) long and 23-30 (26 [+ or -] 2) wide, first third covered with 9-10 rows of spines followed by short spineless area. Prepharynx shorter than pharynx, pharynx oval, 10-17 (14 [+ or -] 2) long and 10-14 (13 [+ or -] 1) wide. Oesophagus shorter than pharynx, intestinal bifurcation in posterior third of forebody; caeca becoming wider in hindbody and terminate fairly close to excretory vesicle. Ventral sucker subspherical, post-equatorial, 28-32 (29 [+ or -] 2) long and 30-34 (33 [+ or -] 2) wide, with 2-3 circles of hooks surrounding its opening. Four big penetration gland-cells coarsely granulated situated anterior to ventral sucker: two glands situated one behind the other between the bifurcation of the esophagus and the ventral sucker, and the other two glands larger, one on either side of the ventral sucker. Flame cell formula: 2[(2+2)+(2+2+[2])]=20. Excretory vesicle small, V-shaped. Caudal excretory duct passes through tail stem, excretory pores at mid-length of furcae. Tail stem 170-198 (183 [+ or -] 11) long and 34-44 (39 [+ or -] 3) wide, with four pairs of caudal bodies and several pairs of sensory hairs. Furcae 166-195 (180 [+ or -] 10) long and 16-28 (23 [+ or -] 3) wide.

Cercariae emerge from sporocysts. At resting position, the cercariae maintained themselves suspended in water with their bodies bent at a characteristic angle, tail stem straight, and furcae spread at an angle of more than 90[degrees] (Fig. 4).

Emerged cercariae penetrated in exposed Cnesterodon sp. Five hours post-exposure (PE) the fish were dissected, showing many free young metacercariae, not yet encysted in the body musculature.

Remarks: Cercariae with four penetration gland-cells (two anterior and two lateral to the ventral sucker), 20 flame cells and absent eyespots have been described in the genus Hysteromorpha Lutz, 1931. These cercariae penetrate primarily into fishes and their definitive hosts are mainly aquatic birds of the families Phalacrocoracidae and Ardeidae and genus Burhinus (Niewiadomska, 2005). Hugghins (1954) described the life cycle of Hysteromorpha triloba (Rudolphi, 1819) whose cercaria is similar to Furcocercaria XIX in the morphology of the penetration gland cells, presence of three circles of spines surrounding the opening of the ventral sucker, number and position of sensory hairs on the body (one pair) and several pairs in the tail stem, resting position, size of the body (168-221/41-50 H. triloba vs. 166-205/44-62 Furcocercaria XIX) and anterior organ (4253/20-28 vs. 41-51/23-30), by penetrating into fishes. However, Furcocercaria XIX differs in the arrangement of the penetration gland-cells (anterior to ventral sucker), the presence of caudal bodies, shorter tail stem (170-198/3444 Furcocercaria XIX vs. 226-260/28-42 H. triloba) and furcae (165-195 vs. 196-227), and larger ventral sucker (30-34 vs. 17-20).

In Argentina, two cercariae have been reported that could be comparable to Furcocercaria XIX in number and arrangement of the penetration gland-cells: Furcocercaria sp. A (cf. Tylodelphys sp.) Ostrowski de Nunez & Quaggiotto, 1995 from Chilina sp. of Rio Negro province and Austrodiplostomum mordax Szidat & Nani, 1951 from B. peregrina of Buenos Aires. However, both cercariae differ from Furcocercaria XIX in having fewer flame cells (16), more caudal bodies (five pairs), fewer circles of hooks surrounding the opening of the ventral sucker (one circle of hooks), and different arrangement of spines in the body.

In Belo Horizonte, Minas Gerais, Brazil Pinto (2013) described the cercaria of H. triloba parasitizing B. straminea, which is similar to Furcocercaria XIX in the morphology of penetration gland-cells, resting position in water and size of the anterior organ (3358/23-28 H. triloba vs. 41-51/23-30 Furcocercaria XIX). However, the cercaria of H. triloba differs from Furcocercaria XIX in the arrangement of the penetration gland-cells (one pair anterior and one pair lateral to the ventral sucker), the absence of caudal bodies in tail stem, smaller body (175 [+ or -] 15/44 [+ or -] 4 vs. 187 [+ or -] 15/54 [+ or -] 6) and ventral sucker (18 [+ or -] 1/18 [+ or -] 2 vs. 29 [+ or -] 2/33 [+ or -] 2), larger tail stem (236 [+ or -] 16/38 [+ or -] 3 vs. 183 [+ or -] 11/39 [+ or -] 3) and furcae (213 [+ or -] 15/22 [+ or -] 3 vs. 180 [+ or -] 10/23 [+ or -] 3). In Santos, Sao Paulo, Brazil Ruiz (1953) described the Cercaria amplicocecata from Australorbis immunis (= B. tenagophila) which is similar to Furcocercaria XIX in the arrangement of spines in the body, the arrangement of penetration gland-cells, number of flame cells (20) and resting position in water. However, the Cercaria amplicocecata differs from Furcocercaria XIX in having more penetration gland-cells (6), fewer transverse rows of spines between anterior organ and ventral sucker (7-8), more caudal bodies (8) and fewer sensory hairs (two pairs) in tail stem, having numerous setae in furcae, smaller body (187 [+ or -] 15/54 [+ or -] 6 vs. 172/43), larger tail stem (183 [+ or -] 11 vs. 216) and furcae (180 [+ or -] 10 vs. 328).

Family Strigeidae Railliet, 1919 Furcocercaria V (Figs. 5-7, 14-18)

Prevalence: 0.40%

Specimen deposited: accession number CECOAL 12032218

Description: Measurements based on 25 specimens. Body 120-195 (155 [+ or -] 19) long and 46-96 (56 [+ or -] 7) wide. Tegument covered with spines, except spineless area ventrally anterior and posterior to ventral sucker. Sensory button papillae distributed on ventral and dorsal surface of body (Figs. 14, 15) and ventral sucker (Fig. 17). One pair of sensory hairs at level of the excretory vesicle. Anterior organ elongate-oval, 32-44 (38 [+ or -] 3) long and 25-39 (31 [+ or -] 4) wide, first third covered with ten rows of spines larger than body spines. Prepharynx shorter than pharynx, pharynx oval, 11-16 (14 [+ or -] 2) long and 14-16 (14 [+ or -] 1) wide. Oesophagus shorter than pharynx, intestinal bifurcation in posterior third of forebody; caeca septated, terminate at some distance from excretory vesicle. Colourless eye-spots between level of intestinal bifurcation and ventral sucker. Ventral sucker subspherical, post-equatorial, 20-30 (25 [+ or -] 2) long and 23-30 (26 [+ or -] 2) wide, with five circles of spines surrounding its opening. Two pairs of coarsely granulated penetration gland-cells situated one behind the other, anterior and lateral to ventral sucker. Flame cell formula: 2[(2+2)+(2+2+[2])]=20, up to three ciliary patches in common collecting ducts. Excretory vesicle small, V-shaped, with round stem. Transverse commissure present anterior to ventral sucker. Caudal excretory duct passes through tail stem, excretory pores somewhat anterior at mid-length of furcae. Tail stem 140235 (209 [+ or -] 28) long, and 32-55 (43 [+ or -] 7) wide, with spines smaller than body spines, and 10-14 pairs of sensory hairs, without caudal bodies. Furcae 154-230 (204 [+ or -] 26) long and 201-34 (27 [+ or -] 5) wide, with spines smaller than tail stem spines.

At resting position, the cercariae maintained themselves suspended in the water with their bodies directed downward, body and tail stem in a straight line and furcae spread at an angle of approximately 90[degrees] (Fig. 7).

Cercariae emerge from sporocysts. In one snail, metacercariae of normal Tetracotyle form were observed encysted in their own sporocysts; cysts of 180-210 (195 [+ or -] 12) long and 135-165 (139 [+ or -] 10) wide, with thick double wall.

Emergence of cercariae was monitored during two days in two infected snails. At 14.1-27.1[degrees]C cercariae had emergence peaks between 11 am and 3 pm.

Remarks: Furcocercaria V shows the typical characteristics of the cercariae of Cotylurus Szidat, 1928 regarding the presence of four penetration gland-cells, colourless eye-spots, 20 flame cells and transverse commissure anterior to ventral sucker, only differ in the arrangement of penetration gland-cells (anterior to ventral sucker) (Niewiadomska, 2002). Three species of this genus have cercariae with features similar to Furcocercaria V, besides those mentioned above. The cercaria of C. flabelliformis (Faust, 1917) is similar in having 4-5 circles of spines surrounding the opening of its ventral sucker, as well as in size of the suckers, tail stem and furcae, the resting position and the absence of caudal bodies; but differs from Furcocercaria V by having larger body (139-231 vs. 120-195), using snails of genus Lymnaea Lamarck, 1799 and Physa Draparnaud, 1801 as first intermediate hosts, and encysting in snails Lymnaea Lamarck, 1799. Cotylurus flabelliformis may also penetrate snails of Planorbidae and Physidae, but only if they are infected by other species of trematodes, where its encysts within sporocysts and/ or rediae (Cort, Olivier, & Brackett, 1941). The cercaria of C. brevis Dubois & Rausch, 1950 is similar to Furcocercaria V in the number and position of sensory hairs in the body (one pair posterior to ventral sucker); but differs in the number of circles of spines (three) surrounding the opening of ventral sucker, the presence of caudal bodies, a larger body (120-360/30-110 vs. 120-195/46-96) and furcae (240-270 vs. 154-230), and by using snails of genus Lymnaea as first intermediate hosts. The cercaria of Cotylurus (Cotylurus) lutzi Basch, 1969 from Biomphalaria glabrata in Bahia, Brazil is similar to Furcocercaria V in the number of sensory hairs in the tail stem (10-12 pairs) and the hours of emergency (near noon); but differs in having a shorter body (130-174/31-49 vs. 120-195/46-96), tail stem (115-166/29-39 vs. 140-235/32-55) and furcae (143-174/13-16 vs. 154-230/21-34) and more sensory hairs in the body (five pairs). The cercaria of Cotylurus (Cotylurus) lutzi encysts in ovotestis of molluscs or hyperparasitizes the redia or sporocysts of other trematodes, developing encysted metacercariae of the "tetracotyle" form (Yamaguti, 1975).

In Caratinga, Mina Gerais, Brazil Ruiz (1953) described the Cercaria caratinguensis from Australorbis glabratus (= B. glabrata), which is similar to Furcocercaria V in the presence of colourless eye-spots, sensory hairs in the tail stem, resting position in water, and in having a metacercariae of normal Tetracotyle form encysted in some host analized. However, Cercaria caratinguensis differs from Furcocercaria V in the number of flame cells (14 vs. 20), the presence of caudal bodies in tail stem, a shorter body (129-172/61-70 vs. 120-195/4696), oral sucker (25-40 vs. 32-44), tail stem (148-172/37-43 vs. 140-235/32-55) and furcae (166-191 vs. 154-230). The number of penetration gland-cells was not specified by the author.

Furcocercaria XX (Figs. 8-11)

Prevalence: 0.04%

Specimen deposited: accession number CECOAL 12032219

Description: Measurements based on 20 specimens. Body 99-131 (117 [+ or -] 9) long and 39-53 (45 [+ or -] 4) wide. Tegument covered with spines. Three pairs of sensory hairs on lateral margins of body: one pair at level of the anterior organ, one pair anterior to ventral sucker and one pair anterior to excretory vesicle. Anterior organ elongate-oval, 23-37 (30 [+ or -] 3) long and 23-30 (26 [+ or -] 2) wide, first third covered with rows of larger spines. Prepharynx shorter than pharynx, pharynx oval, 9-14 (11 [+ or -] 1) long and 9-11 (10 [+ or -] 1) wide. Oesophagus shorter than pharynx, intestinal bifurcation in posterior third of forebody; caeca terminate fairly close to excretory vesicle. Ventral sucker spherical, post-equatorial, 21-30 (23 [+ or -] 2) long and 18-25 (23 [+ or -] 2) wide, with 2-3 circles of spines surrounding its opening. Colourless eye-spots, 11 long and 9 wide, at half-length between pharynx and ventral sucker. Eight pairs of coarsely granulated penetration gland-cells, lateral and posterior to ventral sucker. Flame cell formula: 2[(1+1)+(1+1+[1])]=10. Excretory vesicle small, V-shaped, with round stem. Incomplete transverse commissure anterior to ventral sucker. Caudal excretory duct passes through tail stem, excretory pores in the first third of furcae. Tail stem 115-126 (120 [+ or -] 3) long and 30-41 (34 [+ or -] 3) wide, with six pairs of sensory hairs and three pairs of caudal bodies. Furcae 126-149 (142 [+ or -] 5) long and 11-18 (14 [+ or -] 2) wide, with spines smaller than body spines.

Cercariae emerge from sporocysts. At resting position, cercarial body and tail stem remain aligned in a straight line and furcae spread at an angle of approximately 90[degrees] (Fig. 11).

Remarks: Furcocercaria sp. XX shows similarities to those of genera Strigea Abildgaard, 1790, Apatemon Szidat, 1928, Pharyngostomum Ciurea, 1922 and Parastrigea Szidat, 1928 due to presence of ten flame cells and non-pigmented eyespots; however, the first three genera have fewer penetration gland-cells (4 or 2 pairs). Only Parastrigea has seven pairs of penetration gland-cells lateral and posterior to ventral sucker and anterior excretory commissure, which may not be closed (Niewiadomska, 2002). The adult stages of this genus use birds and exceptionally mammals as definitive hosts (Yamaguti, 1971).

The cercaria of Parastrigea robusta Szidat, 1928 described by Odening (1965, 1966) parasitizing Planorbis planorbis (Linnaeus, 1758) and Anisus vortex (Linnaeus, 1758) in Germany, is similar to Furcocercaria XX in the arrangement of penetration gland-cells, but differs in having fewer penetration gland-cells (seven pairs P robusta vs. eight pairs Furcocercaria XX), more sensory hairs in the body (four pairs vs. three pairs), fewer sensory hairs in the tail stem (four pairs vs. six pairs), more caudal bodies (five pairs vs. three pairs), longer body (155-224/69-93 vs. 99-131/39-53), tail stem (190-224/38-45 vs. 115-126/30-41) and furcae (190-207/28-35 vs. 126-149/11-18) and lacking an incomplete transverse commissure.

In Corrientes Province, Argentina, Ostrowski de Nunez et al. (1997) described two cercariae similar to Furcocercaria XX in the number of flame cells (10) and the presence of non-pigmented eyespots: Furcocercaria sp. VIII from B. orbignyi and B. peregrina and Furcocercaria sp. XIII from B. tenagophila and B. orbignyi. However, both cercariae differ in having fewer penetration glands (4 pairs) and lacking an incomplete transverse commissure.

DISCUSSION

Cercariae of two species of the family Strigeidae (Furcocercaria V, Furcocercaria XX) and one of the family Diplostomidae (Furcocercaria XIX) were found in a rice field in Corrientes, Argentina. This species are added to the eight cercariae previously reported parasitizing B. straminea in the same environment (Fernandez et al. 2013, 2014), and are new records of cercariae from Argentina.

The furcocercariae identity to genus level cannot be elucidated because the arrangement (Furcocercaria XIX and Furcocercaria V) and the number of penetration gland-cells (Furcocercaria XX) did not match with any species known. However, according to the characteristics of the families to which the cercariae described are tentatively assigned, theirs potential definitive hosts would be mainly aquatic birds. In this sense, the rice fields in Northeastern Argentina harbor numerous species of aquatic birds that use these environments as refuge, food sources and breeding sites (Blanco et al., 2006; Blanco & de la Balze, 2011). Thus, many of these bird species might act as definitive hosts in the life cycles of theses trematodes that are found as larvae parasitizing snails. Furthermore, the positive results of experimental infections of Furcocercaria XIX in fish, suggest that its second intermediate host should be found among these aquatic vertebrates, which are part of the diet of several bird species present in this agricultural environment.

In general terms, the prevalence of the different furcocercariae was low, and regarding the rice cultivation cycles, it was somewhat higher in the second rice cultivation cycle. Similar results were previously observed in the same rice field (Fernandez et al., 2014), and this could be related to diverse factors, such as the presence of greater numbers of definitive hosts in the environment during the second rice cultivation cycle, or fewer snails in the environment during the same period.

The study of the freshwater species in rice fields is important because it can contribute to the conservation of biodiversity in regions where wetlands have been turned into rice fields (Maltchik et al. 2011). In this sense, given the importance of this agroecosystem type in Northeast Argentina, further research efforts should be encouraged to obtain more knowledge about the larval trematode species that parasitize snails in rice fields (using morphological, molecular and life-cycle data) as well as of their hosts.

ACKNOWLEDGMENTS

We would like to thank the authorities of the Agricultural Experimental Station El Sombrero, Corrientes of Instituto Nacional de Tecnologia Agropecuaria (INTA) for allowing access to the rice field and for providing accommodation during the sampling period. We thank Margarita Ostrowski de Nunez for reviewing a draft version of the manuscript and making useful suggestions and to two anonymous referees, who helped to improve the manuscript. This study was funded by the Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET), Argentina.

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Maria Virginia Fernandez * & Monika Ines Hamann

Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET). Centro de Ecologia Aplicada del Litoral (CECOAL), Ruta 5 Km 2.5, W 3400 AMD, Corrientes, Argentina; mvirginiafernandez@yahoo.com.ar, monika_hamann@yahoo.com

Received 01-VI-2016. Corrected 07-XI-2016. Accepted 06-XII-2016.

Caption: Fig. 1. Prevalence of larval trematode infections in B. straminea from a rice field in Corrientes province during 2 rice cultivation cycles, gray bar: December 2010-May 2011 (n=number of collected snails: 3 494); black bar: December 2011-May 2012 (n= 2 016).

Caption: Figs. 2-11. Line drawings of larval trematodes. 2-4: Furcocercaria XIX (2: cercarial body, 3: cercaria and tail in ventral view, 4: resting position); 5-7: Furcocercaria V (5: cercarial body, 6: cercaria and tail in ventral view; 7: resting position); 8-11: Furcocercaria XX (8: cercarial body in ventral view, showing the penetration gland-cells, 9: cercarial body in ventral view, showing the excretory system, 10: cercaria and tail in ventral view, 11: resting position). Scale bars: 50 [micro]m.

Caption: Figs. 12-13. Light micrographs of Furcocercaria XIX. 12: cercarial body showing tegument covered with large spines distributed in 9-10 transverse rows between anterior organ and ventral sucker; 13: cercarial body showing the penetration gland-cells.

Caption: Figs. 14-18. Scanning electron micrographs of Furcocercaria V 14: dorsal view of cercarial body showing arrangement of sensory button papillae and spines on tegument; 15: ventral view of cercarial body showing arrangement of sensory button papillae and spines on tegument; 16: detail of rows of spines on the anterior organ; 17: ventral sucker with 5 circles of spines surrounding its opening and sensory button papillae above it; 18: detail of spines and sensory button papillae on body.
TABLE 1
Previous records of larval trematodes infecting Biomphalaria
species in different environments of Argentina

Larval Trematodes                  Hosts *               E **

Furcocercaria sp. I                BS                    LW

Furcocercaria sp. III              BO                    SP

Furcocercaria V                    BS                    RF
Furcocercaria sp. VIII             BP, BOR               SP
Furcocercaria sp. X                BOR                   SP
Furcocercaria sp. XIII             BT, BOR               SP
Furcocercaria sp. XIV              BS                    RF
Furcocercaria sp. XV               BS                    RF
Furcocercaria sp. XVI              BS                    RF
Furcocercaria sp. XVII             BS                    RF
Furcocercaria sp. XVIII            BS                    RF
Furcocercaria XIX                  BS                    RF
Furcocercaria XX                   BS                    RF
Furcocercaria I                    BP                    S
Furcocercaria V                    BP                    TW
Furcocercaria VI                   BP                    TW
Cercaria planorbicola n. sp.       BP                    R
Australapatemon magnacetabulum     BT                    TW
Strigea sp.                        BT                    TW
Cercaria Spirorchiidae sp.         BT, BO                SP
Cercaria Clinostomidae sp.         BO                    SP
Clinostomum sp.                    BT                    TW
Cf. Trichobilharzia sp.            BT                    TW
Furcocercaria sp. 6                BT                    TW
Cercaria quequeni n. sp.           BP                    R
Echinocercaria sp. II              BS                    TW
Echinocercaria sp. III             BO                    SP

Echinocercaria sp. IV              BO, BT, BS, BP, BOR   SP

Echinocercaria sp. V               BOR                   SP
Echinocercaria sp. VII             BO                    SP
Cercaria Ribeiroia sp.             BO                    SP

Ribeiroia sp.                      BOR, BT               D
Cercaria Echinostoma No. 3         BT                    S

Cercaria Monostoma No. 1           BT                    R
Cercaria Macrogranulosa            BS, BP, BOR           LW,R
Echinocercaria sp. XIII            BS                    RF
Echinocercaria sp. XIV             BS, BO                RF, SP
Echinocercaria sp. XVI             BS                    RF
Echinocercaria sp. 1               BO, BT                SP
Echinocercaria sp. 2               BO                    SP
Echinocercaria sp. 3               BT, BO                SP
Echinocercaria I                   BP                    D, SP
Episthmium suspensum               BP                    S
Petasiger sp.                      BT, BOR               D
Echinocercaria sp. 1               BT                    D
Echinocercaria sp. 3               BT                    LW
Zygocotyle lunata                  BP, BT                P

Magnivitellinum simplex            BOR, BT               TW
Notocotylus biomphalariae n. sp.   BP                    P
Hippocrepis fuelleborni            BP                    TW
Xiphidiocercaria sp. I             BS, BP, BOR           R, TW
Xiphidiocercaria sp. II            BS                    TW
Xiphidiocercaria sp. V             BO                    SP
Xiphidiocercaria A                 BP                    S
Xiphidiocercaria B                 BP                    S
Xiphidiocercaria sp. 1             BP                    TW
Xiphidiocercaria sp. 2             BT                    TW

Larval Trematodes                  Locality

Furcocercaria sp. I                Corrientes

Furcocercaria sp. III              Corrientes

Furcocercaria V                    Corrientes
Furcocercaria sp. VIII             Corrientes
Furcocercaria sp. X                Corrientes
Furcocercaria sp. XIII             Corrientes
Furcocercaria sp. XIV              Corrientes
Furcocercaria sp. XV               Corrientes
Furcocercaria sp. XVI              Corrientes
Furcocercaria sp. XVII             Corrientes
Furcocercaria sp. XVIII            Corrientes
Furcocercaria XIX                  Corrientes
Furcocercaria XX                   Corrientes
Furcocercaria I                    Buenos Aires
Furcocercaria V                    Buenos Aires
Furcocercaria VI                   Buenos Aires
Cercaria planorbicola n. sp.       Buenos Aires
Australapatemon magnacetabulum     Salta
Strigea sp.                        Salta
Cercaria Spirorchiidae sp.         Corrientes
Cercaria Clinostomidae sp.         Corrientes
Clinostomum sp.                    Salta
Cf. Trichobilharzia sp.            Salta
Furcocercaria sp. 6                Salta
Cercaria quequeni n. sp.           Buenos Aires
Echinocercaria sp. II              Corrientes
Echinocercaria sp. III             Corrientes

Echinocercaria sp. IV              Corrientes

Echinocercaria sp. V               Corrientes
Echinocercaria sp. VII             Corrientes
Cercaria Ribeiroia sp.             Corrientes

Ribeiroia sp.                      Salta
Cercaria Echinostoma No. 3         Corrientes

Cercaria Monostoma No. 1           Corrientes
Cercaria Macrogranulosa            Corrientes
Echinocercaria sp. XIII            Corrientes
Echinocercaria sp. XIV             Corrientes
Echinocercaria sp. XVI             Corrientes
Echinocercaria sp. 1               Corrientes
Echinocercaria sp. 2               Corrientes
Echinocercaria sp. 3               Corrientes
Echinocercaria I                   Cordoba, Buenos Aires
Episthmium suspensum               Buenos Aires
Petasiger sp.                      Salta
Echinocercaria sp. 1               Salta
Echinocercaria sp. 3               Salta
Zygocotyle lunata                  Buenos Aires, Salta

Magnivitellinum simplex            Salta
Notocotylus biomphalariae n. sp.   Rio Negro
Hippocrepis fuelleborni            Buenos Aires
Xiphidiocercaria sp. I             Corrientes
Xiphidiocercaria sp. II            Corrientes
Xiphidiocercaria sp. V             Corrientes
Xiphidiocercaria A                 Buenos Aires
Xiphidiocercaria B                 Buenos Aires
Xiphidiocercaria sp. 1             Buenos Aires
Xiphidiocercaria sp. 2             Salta

Larval Trematodes                  References

Furcocercaria sp. I                Ostrowski de Nunez, Hamann, &
                                     Rumi, 1990
Furcocercaria sp. III              Ostrowski de Nunez, Hamann, & Rumi,
                                     1997, Fernandez, Hamann, &
                                     Ostrowski de Nunez, 2016
Furcocercaria V                    Present study
Furcocercaria sp. VIII             Ostrowski de Nunez et al., 1997
Furcocercaria sp. X                Ostrowski de Nunez et al., 1997
Furcocercaria sp. XIII             Ostrowski de Nunez et al., 1997
Furcocercaria sp. XIV              Fernandez et al., 2013
Furcocercaria sp. XV               Fernandez et al., 2013
Furcocercaria sp. XVI              Fernandez et al., 2013
Furcocercaria sp. XVII             Fernandez et al., 2013
Furcocercaria sp. XVIII            Fernandez et al., 2013
Furcocercaria XIX                  Present study
Furcocercaria XX                   Present study
Furcocercaria I                    Ostrowski de Nunez, 1972
Furcocercaria V                    Ostrowski de Nunez, 1977
Furcocercaria VI                   Ostrowski de Nunez, 1977
Cercaria planorbicola n. sp.       Szidat & de Szidat, 1960
Australapatemon magnacetabulum     Davies & Ostrowski de Nunez, 2012
Strigea sp.                        Davies, 2014
Cercaria Spirorchiidae sp.         Fernandez et al., 2016
Cercaria Clinostomidae sp.         Fernandez et al., 2016
Clinostomum sp.                    Davies, 2014
Cf. Trichobilharzia sp.            Davies, 2014
Furcocercaria sp. 6                Davies, 2014
Cercaria quequeni n. sp.           Szidat, 1951
Echinocercaria sp. II              Ostrowski de Nunez et al., 1990
Echinocercaria sp. III             Ostrowski de Nunez, Hamann, & Rumi,
                                   1991
Echinocercaria sp. IV              Ostrowski de Nunez et al., 1997,
                                     Fernandez et al., 2016
Echinocercaria sp. V               Ostrowski de Nunez et al., 1997
Echinocercaria sp. VII             Ostrowski de Nunez et al., 1991
Cercaria Ribeiroia sp.             Ostrowski de Nunez et al., 1991,
                                     Fernandez et al., 2016
Ribeiroia sp.                      Davies, 2014
Cercaria Echinostoma No. 3         Martorelli, Alda, Marcotegui,
                                     La Sala, & Montes, 2013
Cercaria Monostoma No. 1           Martorelli et al., 2013
Cercaria Macrogranulosa            Ostrowski de Nunez et al., 1990
Echinocercaria sp. XIII            Fernandez et al., 2014
Echinocercaria sp. XIV             Fernandez et al., 2014, 2016
Echinocercaria sp. XVI             Fernandez et al., 2014
Echinocercaria sp. 1               Fernandez et al., 2016
Echinocercaria sp. 2               Fernandez et al., 2016
Echinocercaria sp. 3               Fernandez et al., 2016
Echinocercaria I                   Ostrowski de Nunez, 1981
Episthmium suspensum               Ostrowski de Nunez, 1974a
Petasiger sp.                      Davies, 2014
Echinocercaria sp. 1               Davies, 2014
Echinocercaria sp. 3               Davies, 2014
Zygocotyle lunata                  Ostrowski de Nunez, Davies, &
                                     Spatz, 2011
Magnivitellinum simplex            Davies, 2014
Notocotylus biomphalariae n. sp.   Flores & Brugni, 2005.
Hippocrepis fuelleborni            Ostrowski de Nunez, 1976
Xiphidiocercaria sp. I             Ostrowski de Nunez et al., 1990
Xiphidiocercaria sp. II            Ostrowski de Nunez et al., 1990
Xiphidiocercaria sp. V             Ostrowski de Nunez et al., 1991
Xiphidiocercaria A                 Morris, 1976
Xiphidiocercaria B                 Morris, 1976
Xiphidiocercaria sp. 1             Ostrowski de Nunez, 1974b.
Xiphidiocercaria sp. 2             Davies, 2014

* Hosts: BT, B. tenagophila; BO, B. occidentalis; BOR, B. orbignyi
BP, B. peregrina BS, B. straminea. ** Environments (E): RF, rice
field; SP, semipermanent ponds; P, pond; LW, lotic waterbodies; TW,
temporary waterbody; D, dam; R, river; S, stream.
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