Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-16T15:30:20.401Z Has data issue: false hasContentIssue false

Morphological characterization and molecular phylogeny of zoonotic trematodes in the freshwater snail Asolene platae

Published online by Cambridge University Press:  06 February 2019

Federico A. Dellagnola
Affiliation:
Universidad Nacional de Cuyo, Facultad de Ciencias Médicas, Instituto de Fisiología, 5500 Mendoza, Argentina IHEM, CONICET, Universidad Nacional de Cuyo, 5500 Mendoza, Argentina Universidad Nacional de Cuyo, Facultad de Ciencias Exactas y Naturales, Departamento de Biología, 5500 Mendoza, Argentina
Martín M. Montes
Affiliation:
CEPAVE, CONICET, Universidad Nacional de La Plata, 1900 La Plata, Argentina
Sergio R. Martorelli
Affiliation:
CEPAVE, CONICET, Universidad Nacional de La Plata, 1900 La Plata, Argentina
Israel A. Vega*
Affiliation:
Universidad Nacional de Cuyo, Facultad de Ciencias Médicas, Instituto de Fisiología, 5500 Mendoza, Argentina IHEM, CONICET, Universidad Nacional de Cuyo, 5500 Mendoza, Argentina Universidad Nacional de Cuyo, Facultad de Ciencias Exactas y Naturales, Departamento de Biología, 5500 Mendoza, Argentina
*
Author for correspondence: Israel A. Vega, E-mail: israel.vega7@gmail.com

Abstract

In the context of a broader program dealing with the symbiotic associations of apple snails, we sampled three species that coexist in Lake Regatas (Palermo, Buenos Aires, Argentina). The population of Asolene platae, (but not those of Pomacea canaliculata and Pomacea scalaris) showed trematode larvae (echinocercariae and xiphidiocercariae) in haemocoelic spaces and connective tissue of the digestive gland. The echinocercariae resembled those of the genus Echinochasmus, but lacked sensory hairs on their body and tail; whereas xiphidiocercariae were similar to the xiphidiocercariae armatae belonging to the Opisthoglyphe type. The phylogenetical positions of these trematodes were inferred by the 28S rRNA, ITS1 and mtCOXI gene sequences. The 28S rRNA gene linked the echinocercarial sequences with the polyphyletic genus Echinochasmus (Echinochasmidae), while the xiphidiocercarial sequences were linked with the genus Phaneropsolus (Phaneropsolidae). The molecular markers used were able to distinguish two cryptic molecular entities of the single echinocercarial morphotype. Although ITS1 and mtCOXI did not allow resolving phylogeny beyond the family level because of the scarce number of sequences in the molecular databases, both cercariae (echinocercariae and xiphidiocercariae) could be distinguished by the Internal Transcribed Spacer 1 amplicon size. This is the first correlative morphological and molecular study of zoonotic trematodes in Neotropical ampullariids.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adema, C and Loker, E (2015) Digenean-gastropod host associations inform on aspects of specific immunity in snails. Developmental & Comparative Immunology 48, 275283.Google Scholar
Beaver, P (1941) The life history of Echinochasmus donaldsoni n. sp., a trematode (Echinostomidae) from the pied-billed grebe. The Journal of Parasitology 27, 347355.Google Scholar
Berbery, EH and Barros, BR (2002) The hydrologic cycle of the La Plata Basin in South America. Journal of Hydrometeorology 3, 630645.Google Scholar
Berthold, T (1991) Vergleichende anatomie, phylogenic und historische biogeographie der ampullaridae (Mollusca, Gastropoda). Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg 29, 1256.Google Scholar
Besprozvannykh, V, Rozhkovan, K and Ermolenko, A (2017) Stephanoprora chasanensis n. sp. (Digenea: Echinochasmidae): morphology, life cycle, and molecular data. Parasitology International 66, 863870.Google Scholar
Cable, R (1938) Studies on larval trematodes from Kentucky with a summary of known related species. American Midland Naturalist 19, 440464.Google Scholar
Castro-Vazquez, A, Albrecht, E, Vega, I, Koch, E and Gamarra-Luques, C (2002) Pigmented corpuscles in the midgut gland of Pomacea canaliculata and other neotropical apple-snails (Prosobranchia, Ampullariidae): a possible symbiotic association. Biocell 26, 101109.Google Scholar
Chai, J-Y, Han, E-T, Shin, E-H, Sohn, W-M, Yong, T-S, Eom, K, Min, D-Y, Um, J-Y, Park, M-S and Hoang, E-H (2009) High prevalence of Haplorchis taichui, Phaneropsolus molenkampi, and other helminth infections among people in Khammouane province, Lao PDR. The Korean Journal of Parasitology 47, 243247.Google Scholar
Clausen, J, Madsen, H, Murrell, D, Manh, HN, Viet, KN and Dalsgaard, A (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Neglected Tropical Diseases 6, e1945.Google Scholar
Cowie, R (2002) Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management. In Barker, G (ed.) Molluscs as Crop Pests. Wallingford, UK: CAB-International, pp. 145192.Google Scholar
Cueto, J, Vega, IA and Castro-Vazquez, A (2013) Multicellular spheroid formation and evolutionary conserved behaviors of apple snail hemocytes in culture. Fish & Shellfish Immunology 34, 443453.Google Scholar
Cueto, J, Rodriguez, C, Vega, I and Castro-Vazquez, A (2015) Immune defenses of the invasive apple snail Pomacea canaliculata (Caenogastropoda, Ampullariidae): phagocytic hemocytes in the circulation and the kidney. PloS ONE 10, e0123964.Google Scholar
Damborenea, C, Brusa, F and Paola, A (2006) Variation in worm assemblages associated with Pomacea canaliculata (Caenogastropoda, Ampullariidae) in sites near the Río de la Plata estuary, Argentina. Biocell 30, 457468.Google Scholar
Damborenea, C, Brusa, F and Negrete, L (2017) Symbionts and diseases associated with invasive apple snails. In Joshi, R, Cowie, R, Sebastian, L (eds), Biology and Management of Invasive Apple Snails. Muñoz, Philippines: Philippine Rice Research Institute, pp. 7397.Google Scholar
Dellagnola, FA (2015) Estudio comparativo de los corpúsculos pigmentarios de la glándula digestiva de tres especies de ampuláridos. (PhD Thesis). Universidad Nacional de Cuyo, Mendoza, Argentina.Google Scholar
Dellagnola, F, Vega, I and Castro-Vazquez, A (2017) Evidence for a prokaryotic origin of intracellular corpuscles in the digestive gland of the queen conch Lobatus gigas (Linnaeus, 1758) (Gastropoda: Strombidae). Journal of Molluscan Studies 83, 186193.Google Scholar
Diupotex-Chong, M, Cazzaniga, N, Hernández-Santoyo, A and Betancourt-Rule, J (2004) Karyotype description of Pomacea patula catemacensis (Caenogastropoda, Ampullariidae), with an assessment of the taxonomic status of Pomacea patula. Biocell 28, 279285.Google Scholar
Etchegoin, J and Martorelli, S (1998) Nuevas cercarias en Heleobia conexa (Mollusca: Hydrobiidae) de la albufera Mar Chiquita. Neotrópica 44, 4150.Google Scholar
Falconaro, A, Vega, R and Viozzi, G (2017) Helminth communities of two populations of Myotis chiloensis (Chiroptera: Vespertilionidae) from Argentinean Patagonia. International Journal for Parasitology: Parasites and Wildlife 7, 2733.Google Scholar
Fried, B, Graczyk, T and Tamang, L (2004) Food-borne intestinal trematodiases in humans. Parasitology Research 93, 159170.Google Scholar
Galaktionov, K and Skirnisson, K (2007) New data on Microphallus breviatus Deblock & Maillard, 1975 (Microphallidae: Digenea) with emphasis on the evolution of dixenous life cycles of microphallids. Parasitology Research 100, 963971.Google Scholar
Godoy, M, Castro-Vazquez, A and Vega, I (2013) Endosymbiotic and host proteases in the digestive tract of the invasive snail Pomacea canaliculata: diversity, origin and characterization. PloS ONE 8, e66689.Google Scholar
Grabda-Kazubska, B (1971) Main morphological characters in xiphidiocercariae armatae Luhe, 1909 and their taxonomic importance. Parasitologische Schriftenreihe 21, 4955.Google Scholar
Guindon, S, Dufayard, J-F, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.Google Scholar
Hayes, K, Joshi, R, Thiengo, S and Cowie, R (2008) Out of South America: multiple origins of non-native apple snails in Asia. Diversity and Distributions 14, 701712.Google Scholar
Hayes, K, Cowie, R and Thiengo, S (2009) A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biological Journal of the Linnean Society 98, 6176.Google Scholar
Hayes, K, Burks, R, Castro-Vazquez, A, Darby, P, Heras, H, Martin, P, Qiu, J-W, Thiengo, S, Vega, I, Wada, T, Yusa, Y, Burela, S, Cardiemo, P, Cueto, J, Dellagnola, F, Dreon, M, Frassa, V, Giraud-Billoud, M, Godoy, M, Itualte, S, Koch, E, Matsukura, K, Pasquevich, Y, Rodriguez, C, Seveanu, L, Seuffert, M, Strong, E, Sun, J, Tamburi, N, Tiecher, M, Turner, R, Valentine-Darby, P and Cowie, R (2015) Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae). Malacologia 58, 245302.Google Scholar
Heuzé, V and Tran, G (2017) Apple snails as animal feed. In Joshi, R, Cowie, R and Sebastian, L (eds), Biology and Management of Invasive Apple Snails. Muñoz, Philippines: Philippine Rice Research Institute, pp. 369385.Google Scholar
Hotez, P, Fenwick, A, Ray, S, Hay, S and Molyneux, D (2018) “Rapid impact” 10 years after: the first “decade”(2006–2016) of integrated neglected tropical disease control. PLOS Neglected Tropical Diseases 12, e0006137.Google Scholar
James, B (1965) The effects of parasitism by larval Digenea on the digestive gland of the intertidal prosobranch, Littorina saxatilis (Olivi) subsp. tenebrosa (montagu). Parasitology 55, 93115.Google Scholar
Jokela, J and Lively, C (1995) Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum). Oecologia 103, 509517.Google Scholar
Kanarek, G, Zaleśny, G, Sitko, J and Tkach, V (2017) The systematic position and structure of the genus Leyogonimus ginetsinskaya, 1948 (Platyhelminthes: Digenea) with comments on the taxonomy of the superfamily microphalloidea ward, 1901. Acta Parasitologica 62, 617624.Google Scholar
Katoh, K, Rozewicki, J and Yamada, K (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, bbx108, 17. https://academic.oup.com/bib/advance-article/doi/10.1093/bib/bbx108/4106928Google Scholar
Keawjam, R, Poonswad, P, Upatham, E and Banpavichit, S (1993) Natural parasitic infection of the golden apple snail, Pomacea canaliculata. The Southeast Asian Journal of Tropical Medicine and Public Health 24, 170177.Google Scholar
Kostadinova, A, Jones, A, Jones, A, Bray, RA and Gibson, DI (2005) Superfamily echinostomatoidea looss, 1899. In Jones, A, Bray, R and Gibson, D (eds), Keys to the Trematoda, vol. 2. Wallingford and London, UK: CABI Publishing and The Natural History Museum, pp. 964.Google Scholar
Kudlai, O, Stunžėnas, V and Tkach, V (2015) The taxonomic identity and phylogenetic relationships of Cercaria pugnax and C. helvetica XII (Digenea: Lecithodendriidae) based on morphological and molecular data. Folia Parasitologica 62, 003.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Labriola, J and Suriano, D (1998) Digeneans of bird (Ardeidae) from the Monte Lake, Buenos Aires, Argentina. Physis (rio De Janeiro, Brazil) 56, 17.Google Scholar
Le, TH, Nguyen, NTB, Nguyen, KT, Doan, HTT and Blair, D (2016) A complete mitochondrial genome from Echinochasmus japonicus supports the elevation of Echinochasminae Odhner, 1910 to family rank (Trematoda: Platyhelminthes). Infection, Genetics and Evolution 45, 369377.Google Scholar
Leedom, W and Short, R (1981) Cercaria pomaceae sp. n., a dermatitis-producing schistosome cercaria from Pomacea paludosa, the Florida apple snail. The Journal of Parasitology 67, 257261.Google Scholar
Lefort, V, Longueville, J-E and Gascuel, O (2017) SMS: smart model selection in PhyML. Molecular Biology and Evolution 34, 24222424.Google Scholar
Leung, T, Keeney, D and Poulin, R (2009) Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 136, 241252.Google Scholar
López-Soriano, J, Salgado, S and Tarruella, A (2009) Presencia masiva de Pomacea cf. canaliculata (lamarck, 1822) (Gastropoda: Ampullariidae) en el Delta del Ebro (Cataluña, España). Spira 3, 117121.Google Scholar
Lv, S, Zhang, Y, Liu, H-X, Hu, L, Yang, K, Steinmann, P, Chen, Z, Wang, L-Y, Utzinger, J and Zhou, X-N (2009) Invasive snails and an emerging infectious disease: results from the first national survey on Angiostrongylus cantonensis in China. PLoS Neglected Tropical Diseases 3, e368.Google Scholar
Malek, E (2018) Snail Transmitted Parasitic Diseases. Boca Ratón, Florida: CRC Press.Google Scholar
Manning, G and Lertprasert, P (1973) Studies on the life cycle of Phaneropsolus bonnei and Prosthodendrium molenkampi in Thailand. Annals of Tropical Medicine & Parasitology 67, 361365.Google Scholar
Marcó del Pont, A (1926) Contribución al estudio de los zooparásitos de los animales salvajes. Semana Médica 33, 1622.Google Scholar
Martorelli, S (1985) Estudios parasitológicos en biotopos lénticos de la República Argentina I: el ciclo biológico de Echinochasmus talaensis sp. nov. (Digenea) parásito de Pitangus sulphuratus bolivianus (Aves, Tyrannidae). Neotropica 31, 187200.Google Scholar
Martorelli, S (1987) Estudios parasitológicos en biotopos lénticos de la República Argentina. IV. El ciclo biológico de Echinostoma parcespinosum Lutz, 1924 (Digenea) parásito de Rallus maculatus maculatus y Rallus sanguinolentus sanguinolentus (Aves: Rallidae). Revista del Museo de La Plata, Nueva Serie, Zoología 14, 4756.Google Scholar
Martorelli, S, Fredensborg, B, Leung, T and Poulin, R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology 35, 7384.Google Scholar
Milano, A (2016) Helmintofauna de murciélagos (Chiroptera) del Nordeste argentino (PhD Thesis). Universidad Nacional de La Plata, La Plata, Argentina.Google Scholar
Miura, O, Kuris, A, Torchin, M, Hechinger, R, Dunham, E and Chiba, S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793801.Google Scholar
Nasir, P and Diaz, L (1968) Studies on freshwater larval trematodes XVII. The life cycle of Echinochasmus zubedakhaname sp. n. Zeitschrift fur Parasitenkunde 30, 126133.Google Scholar
Nasir, P, Tulio Díaz, M and Hamana, L (1969) Studies on freshwater larval trematodes XXV. Two new species of Echinostome cercariae. Proceedings of the Helminthological Society of Washington 36, 175177.Google Scholar
Olson, P, Cribb, T, Tkach, V, Bray, R and Littlewood, D (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.Google Scholar
Oscoz, J, Tomds, P and Duron, C (2010) Review and new records of non-indigenous freshwater invertebrates in the Ebro River basin (Northeast Spain). Aquatic Invasions 5, 263284.Google Scholar
Ostrowski de Núñez, M (1974) Sobre el ciclo biológico de Episthmium suspensum (Braun 1901) Travassos 1922. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Parasitología 1, 153164.Google Scholar
Ostrowski de Nuñez, M (1979) Ungewöhnliche xiphidiocercarie aus Ampullaria canaliculata nebst Bemerkungen über Travtrema stenocotyle. Angewandte Parasitologie 20, 4652.Google Scholar
Ostrowsky de Núñez, M (1975) Fauna de agua dulce de la República Argentina IV. Cercarias (Trematoda) de Littoridina piscium. Physis (rio De Janeiro, Brazil) 34, 6368.Google Scholar
Rodriguez, C, Prieto, GI, Vega, IA and Castro-Vazquez, A (2018) Assessment of the kidney and lung as immune barriers and hematopoietic sites in the invasive apple snail Pomacea canaliculata. PeerJ 6, e5789.Google Scholar
Schell, S (1970) How to Know the trematodes. Dubuque, Iowa: Brown Company.Google Scholar
Schneider, C, Rasband, W and Eliceiri, K (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671675.Google Scholar
Schulenburg, J-H, Englisch, U and Wägele, J-W (1999) Evolution of ITS1 rDNA in the Digenea (Platyhelminthes: Trematoda): 3’ end sequence conservation and its phylogenetic utility. Journal of Molecular Evolution 48, 212.Google Scholar
Seo, B, Lee, S, Chai, J and Hong, S (1985) Studies on intestinal trematodes in Korea XX. Four cases of natural human infection by Echinochasmus japonicus. The Korean Journal of Parasitology 23, 214220.Google Scholar
Sievers, F, Wilm, A, Dineen, D, Gibson, T, Karplus, K, Li, W, Lopez, R, McWilliam, H, Remmert, M and Söding, J (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7, 539.Google Scholar
Tesana, S, Srisawangwonk, T, Kaewkes, S, Sithithaworn, P, Kanla, P and Arunyanart, C (1991) Eggshell morphology of the small eggs of human trematodes in Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 22, 631636.Google Scholar
Tesana, S, Srisawangwong, T, Sithithaworn, P and Laha, T (2008) Angiostrongylus cantonensis: experimental study on the susceptibility of apple snails, Pomacea canaliculata compared to Pila polita. Experimental Parasitology 118, 531535.Google Scholar
Tiecher, M, Burela, S and Martín, P (2014) Mating behavior, egg laying, and embryonic development in the South American apple snail Asolene pulchella (Ampullariidae, Caenogastropoda). Invertebrate Reproduction & Development 58, 1322.Google Scholar
Tkach, V, Littlewood, T, Olson, P, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 115.Google Scholar
Tkach, V, Kudlai, O and Kostadinova, A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171185.Google Scholar
Toledo, R and Esteban, J (2016) An update on human echinostomiasis. Transactions of The Royal Society of Tropical Medicine and Hygiene 110, 3745.Google Scholar
Valente, R, Robles, MDR, Navone, G and Diaz, J (2018) Angiostrongylus spp. in the Americas: geographical and chronological distribution of definitive hosts versus disease reports. Memórias do Instituto Oswaldo Cruz 113, 143152.Google Scholar
Van Steenkiste, N, Locke, S, Castelin, M, Marcogliese, D and Abbott, C (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources 15, 945952.Google Scholar
Vega, I, Gamarra-Luques, C, Koch, E, Bussmann, L and Castro-Vazquez, A (2005) A study of corpuscular DNA and midgut gland occupancy by putative symbiotic elements in Pomacea canaliculata (Caenogastropoda, Ampullariidae). Symbiosis 39, 3745.Google Scholar
Vega, I, Damborenea, M, Gamarra-Luques, C, Koch, E, Cueto, J and Castro-Vazquez, A (2006) Workshop: biology of Ampullariidae. Facultative and obligate symbiotic associations of Pomacea canaliculata (Caenogastropoda, Ampullariidae). Biocell 30, 367375.Google Scholar
Vilas, R, Criscione, C and Blouin, M (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 839846.Google Scholar
Zhang, Z, Schwartz, S, Wagner, L and Miller, W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203214.Google Scholar
Supplementary material: File

Dellagnola et al. supplementary material

Dellagnola et al. supplementary material 1

Download Dellagnola et al. supplementary material(File)
File 24.8 KB
Supplementary material: File

Dellagnola et al. supplementary material

Dellagnola et al. supplementary material 2

Download Dellagnola et al. supplementary material(File)
File 20 KB
Supplementary material: File

Dellagnola et al. supplementary material

Dellagnola et al. supplementary material 3

Download Dellagnola et al. supplementary material(File)
File 267.5 KB