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First morphological and molecular identification of the cercaria of Stomylotrema vicarium from the endemic apple snail Pomacea americanista

Published online by Cambridge University Press:  15 September 2021

Federico A. Dellagnola Open the ORCID record for Federico A. Dellagnola [Opens in a new window] ,
Alejandra D. Campoy-Diaz  and
Israel A. Vega
Federico A. Dellagnola
Affiliation:
IHEM, Universidad Nacional de Cuyo, CONICET, Mendoza City, Mendoza, Argentina Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Cuyo, Mendoza City, Mendoza, Argentina Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Mendoza City, Mendoza, Argentina
Alejandra D. Campoy-Diaz
Affiliation:
IHEM, Universidad Nacional de Cuyo, CONICET, Mendoza City, Mendoza, Argentina Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Cuyo, Mendoza City, Mendoza, Argentina
Israel A. Vega*
Affiliation:
IHEM, Universidad Nacional de Cuyo, CONICET, Mendoza City, Mendoza, Argentina Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Cuyo, Mendoza City, Mendoza, Argentina Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Mendoza City, Mendoza, Argentina
*
Author for correspondence: Israel A. Vega, E-mail: ivega@mendoza-conicet.gob.ar
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Abstract

The adult fluke Stomylotrema vicarium (Stomylotrematidae, Microphalloidea) was described for the first time in Theristicus caerulescens in 1901, but the complete life cycle has remained unknown to date. Here, we found a stomylotrematid trematode in the digestive gland of the endemic apple snail Pomacea americanista. The digestive gland's tubuloacini were compressed by the trematode larvae placed on connective tissues and haemocoel spaces. Non-virgulate, stylet-bearing cercariae showed three pairs of penetration glands with a body, oral sucker and stylet morphometrically similar to those of stylet-bearing, unencysted young metacercariae of S. vicarium found in the aquatic coleopteran Megadytes glaucus, and at a lesser extent with cercariae of S. gratiosus found in the apple snail Pomacea maculata. The larvae molecular phylogeny was inferred using the markers rRNA 28S and ITS1, being these sequences grouped with the sequences of S. vicarium obtained from adult flukes. Together, these findings indicate that the life cycle of S. vicarium begins in P. americanista, thus supporting the hypothesis that the ampullariid snails act as a first intermediate host.

Keywords

Apple snailsdigestive glandITS1microphalloidean trematodesrRNA 28S
Type
Research Article
Information
Parasitology , Volume 149 , Issue 1 , January 2022 , pp. 95 - 104
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Amato, SB and Amato, JF (2006) Belostoma dilatatum (Dufour)(Hemiptera, Belostomatidae) hosting metacercariae of Stomylotrema vicarium Braun (Digenea, Stomylotrematidae) in southern Brazil. Revista Brasileira de Zoologia 23, 307–310.CrossRefGoogle Scholar
Baloch, WA, Memon, UN, Burdi, GH, Soomro, AN, Tunio, GR and Khatian, AA (2012) Invasion of channeled apple snail Pomacea canaliculata, Lamarck (Gastropoda: Ampullariidae) in Haleji Lake, Pakistan. Sindh University Research Journal-SURJ (Science Series) 44, 263–266.Google Scholar
Bartoli, P, Jousson, O and Russell-Pinto, F (2000) The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. Journal of Parasitology 86, 479–489.CrossRefGoogle ScholarPubMed
Bell, JA, González-Acuña, D and Tkach, VV (2018) First record of Gyrabascus (Digenea, Pleurogenidae) from Dromiciops bozinovici D'Elia et al., 2016 (Marsupialia: Microbiotheriidae) in Chile and its phylogenetic relationships. Comparative Parasitology 85, 58–65.CrossRefGoogle Scholar
Berthold, T (1991) Vergleichende anatomie, phylogenic und historische biogeographie der ampullaridae (Mollusca, Gastropoda). Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg 29, 1–256.Google Scholar
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295–306.10.1007/s11230-016-9631-2CrossRefGoogle ScholarPubMed
Braun, MG (1901) Zur Kenntnis der Trematoden der Säugetiere. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere 14, 311–348.Google Scholar
Bush, AO and Forrester, DJ (1976) Helminths of the white ibis in Florida. Proceedings of the Helminthological Society of Washington 43, 17–23.Google Scholar
Castro-Vazquez, A, Albrecht, E, Vega, IA, 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, 101–109.Google ScholarPubMed
Cueto, J, Rodriguez, C, Vega, IA 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.CrossRefGoogle ScholarPubMed
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, 457–468.CrossRefGoogle Scholar
Dellagnola, FA, Vega, IA 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, 186–193.CrossRefGoogle Scholar
Dellagnola, FA, Montes, MM, Martorelli, SR and Vega, IA (2019 a) Morphological characterization and molecular phylogeny of zoonotic trematodes in the freshwater snail Asolene platae. Parasitology 146, 839–848.10.1017/S0031182019000027CrossRefGoogle ScholarPubMed
Dellagnola, FA, Rodriguez, C, Castro-Vazquez, A and Vega, IA (2019 b) A multiple comparative study of putative endosymbionts in three coexisting apple snail species. PeerJ 7, e8125.CrossRefGoogle ScholarPubMed
Forrester, DJ, Bush, AO and Williams, LE Jr (1975) Parasites of Florida sandhill cranes, Grus canadensis pratensis. The Journal of Parasitology 61, 547–548.CrossRefGoogle Scholar
Gibson, ID, Jones, A and Bray, RA (2002) Keys to the Trematoda Vol. 1. London, UK: CABI Publishing and The Natural History Museum.CrossRefGoogle Scholar
Giraud-Billoud, M, Koch, E., Vega, IA, Gamarra-Luques, C and Castro-Vazquez, A (2008) Urate cells and tissues in the South American apple snail Pomacea canaliculata. Journal of Molluscan Studies 74, 259–266.10.1093/mollus/eyn017CrossRefGoogle 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, 307–321.CrossRefGoogle ScholarPubMed
Gurovich, FM, Burela, S and Martín, PR (2017) Life cycle of Pomacea americanista, a poorly known apple snail endemic to the Iguazú and Alto Paraná Rivers, southern South America. Journal of Molluscan Studies 84, 62–68.10.1093/mollus/eyx046CrossRefGoogle 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, 61–76.CrossRefGoogle Scholar
Hayes, K, Burks, R, Castro-Vazquez, A, Darby, P, Heras, H, Martin, P, Qiu, J-W, Thiengo, S, Vega, IA, Wada, T, Yusa, Y, Burela, S, Cardiemo, P, Cueto, J, Dellagnola, FA, 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, 245–302.10.4002/040.058.0209CrossRefGoogle Scholar
Heneberg, P, Faltýnková, A, Bizos, J, Malá, M, Žiak, J and Literák, I (2015) Intermediate hosts of the trematode Collyriclum faba (Plagiochiida: Collyriclidae) identified by an integrated morphological and genetic approach. Parasites & Vectors 8, 85.CrossRefGoogle ScholarPubMed
Hon, LT, Forrester, DJ and Williams, LE Jr (1978) Helminth acquisition by wild turkeys (Meleagris gallopavo osceola) in Florida. Proceedings of the Helminthological Society of Washington, 45, 211–218.Google Scholar
Hylton Scott, MIH (1957) Estudio morfológico y taxonómico de los ampulláridos de la República Argentina. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” e Instituto Nacional de Investigacion de las Ciencias Naturales. Ciencias Zoológicas 3, 233–333.Google Scholar
Joshi, RC, Cowie, RH and Sebastian, LS (2017) Biology and Management of Invasive Apple Snails. Muñoz, Philippines: Philippine Rice Research Institute.Google Scholar
Kanarek, G, Zalesny, G, Sitko, J and Tkach, VV (2014) Phylogenetic relationships and systematic position of the families Cortrematidae and Phaneropsolidae (Platyhelminthes: Digenea). Folia Parasitologica 61, 523.CrossRefGoogle ScholarPubMed
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, 617–624.CrossRefGoogle ScholarPubMed
Katoh, K, Rozewicki, J and Yamada, K (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 1160–1166.CrossRefGoogle Scholar
Kinsella, JM, Foster, GW and Forrester, DJ (2001) Parasitic helminths of five species of owls from Florida, USA. Comparative Parasitology 68, 130–133.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.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lefort, V, Longueville, J-E and Gascuel, O (2017) SMS: smart model selection in PhyML. Molecular Biology and Evolution 34, 2422–2424.10.1093/molbev/msx149CrossRefGoogle ScholarPubMed
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, 117–121.Google Scholar
Lotz, JM and Font, WF (2008) Family Lecithodendriidae Lühe, 1901. In Bray, RA, Gibson, DI and Jones, A (eds), Keys to the Trematoda, vol. 3. Wallingford, UK and the Natural History Museum, London: CABI Publishing, pp. 527–536.Google Scholar
Lumsden, RD and Zischke, JA (1963) Studies on the trematodes of Louisiana birds. Zeitschrift fur Parasitenkunde 22, 316–366.10.1007/BF00260192CrossRefGoogle ScholarPubMed
Lunaschi, L, Cremonte, F and Drago, FB (2007) Checklist of digenean parasites of birds from Argentina. Zootaxa 1403, 1–36.CrossRefGoogle Scholar
Macko, JK, Spakulová, M and Casanova, JC (1999) Morphology and taxonomy of Stomylotrema (Digenea: Stomylotrematidae) representatives from ciconiiform and podicipediform birds in Cuba. Folia Parasitologica 46, 185–190.Google Scholar
Martín, PR, Burela, S and Gurovich, FM (2015) Ongoing research into the natural history and ecology of an endemic and little known apple snail from the Alto Paraná and Iguazú rivers (Argentina). Tentacle 23, 3–6.Google Scholar
Meenakshi, VR (1955) The excretory spherioles in the digestive gland of Pila virens. Journal Animal Morphology and Physiology (Bombay) 3, 75–78.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, 793–801.CrossRefGoogle ScholarPubMed
Nasir, P and Acuña, C (1966) Studies on freshwater larval trematodes. Part VIII. Two new species of non-virgulate Xiphidiocercariae from Venezuela. Zoologischer Anzeiger 176, 291–296.Google Scholar
Nasir, P and Díaz, MT (1968) Studies on freshwater larval trematodes. Part XVI. Five new species of cercariae from Venezuela. Proceedings of the Helminthological Society of Washington 35, 67–74.Google Scholar
Nolan, MJ and Cribb, TH (2004) The life cycle of Paracardicoloides yamagutii Martin, 1974 (Digenea: Sanguinicolidae). Folia Parasitologica 51, 320–326.CrossRefGoogle ScholarPubMed
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, 733–755.10.1016/S0020-7519(03)00049-3CrossRefGoogle ScholarPubMed
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, 263–284.CrossRefGoogle Scholar
Ostrowski de Núñez, M (1978) Zum Entwicklungszyklus von Stomylotrema vicarium. Angewandte Parasitologie 19, 208–213.Google ScholarPubMed
Pinto, HA, Cantanhede, SPD, Thiengo, SC, de Melo, AL and Fernandez, MA (2015) The apple snail Pomacea maculata (Caenogastropoda: Ampullariidae) as the intermediate host of Stomylotrema gratiosus (Trematoda: Stomylotrematidae) in Brazil: the first report of a mollusc host of a stomylotrematid trematode. Journal of Parasitology 101, 134–139.CrossRefGoogle ScholarPubMed
Porebski, S, Bailey, LG and Baum, BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Molecular Biology Reporter 15, 8–15.CrossRefGoogle Scholar
Ramírez-Cañas, SA, George-Nascimento, M, García-Prieto, L and Mata-López, R (2019) Helminth community structure of the gray four-eyed opossum Philander opossum (Mammalia: Didelphidae) in the Neotropical portion of Mexico. Journal of Parasitology 105, 624–629.10.1645/18-195CrossRefGoogle ScholarPubMed
Rasband, WS (2012) ImageJ. Bethesda, MD: U. S. National Institutes of Health. https://imagej.nih.gov/ij/docs/faqs.html.Google Scholar
Rawlings, TA, Hayes, KA, Cowie, RH and Collins, TM (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology 7, 97.CrossRefGoogle ScholarPubMed
Razo-Mendivil, U, Vázquez-Domínguez, E, Rosas-Valdez, R, de León, GP-P and Nadler, SA (2010) Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. International Journal for Parasitology 40, 471–486.10.1016/j.ijpara.2009.10.004CrossRefGoogle ScholarPubMed
Rodriguez, C, Prieto, GI, Vega, IA and Castro-Vazquez, A (2021) Morphological grounds for the obligate aerial respiration of an aquatic snail: functional and evolutionary perspectives. PeerJ 9, e10763.CrossRefGoogle ScholarPubMed
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, 2–12.10.1007/PL00006441CrossRefGoogle Scholar
Seuffert, ME and Martín, PR (2009) Influence of temperature, size and sex on aerial respiration of Pomacea canaliculata (Gastropoda: Ampullariidae) from southern Pampas, Argentina. Malacologia 51, 191–200.CrossRefGoogle Scholar
Seuffert, ME and Martín, PR (2010) Dependence on aerial respiration and its influence on microdistribution in the invasive freshwater snail Pomacea canaliculata (Caenogastropoda. Ampullariidae). Biological Invasions 12, 1695–1708.CrossRefGoogle Scholar
Shchenkov, SV, Denisova, SA, Kremnev, GA and Dobrovolskij, AA (2020) Five new morphological types of virgulate and microcotylous xiphidiocercariae based on morphological and molecular phylogenetic analyses. Journal of Helminthology 94, E94.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Szidat, L (1964) Vergleichende Helminthologische untersuchungen an den argentinischen grossmöwen Larus marinus dominicanus Lichtenstein und Larus ridibundus maculipennis Lichtenstein nebst neuen beobachtungen über die artbildung bei parasiten. Zeitschrift fur Parasitenkunde 24, 351–414.10.1007/BF00260454CrossRefGoogle Scholar
Takebayashi, TE (2013) What are the C and K corpuscles of apple snails? The Malacologist 61, 3–6.Google Scholar
Tkach, V, Pawlowski, J and Mariaux, J (2000) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial 1srDNA sequences. International Journal for Parasitology 30, 83–93.CrossRefGoogle ScholarPubMed
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, 1–15.10.1023/A:1025546001611CrossRefGoogle ScholarPubMed
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, 945–952.CrossRefGoogle ScholarPubMed
Vega, IA, 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, 37–45.Google Scholar
Vega, IA, Giraud-Billoud, M, Koch, E, Gamarra-Luques, C and Castro-Vazquez, A (2007) Uric acid accumulation within intracellular crystalloid corpuscles of the midgut gland in Pomacea canaliculata (Caenogastropoda, Ampullariidae). Veliger 48, 276–283.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, 839–846.10.1017/S0031182005008437CrossRefGoogle ScholarPubMed
Yanygina, LV, Kirillov, VV and Zarubina, EY (2010) Invasive species in the biocenosis of the cooling reservoir of Belovskaya power plant (Southwest Siberia). Russian Journal of Biological Invasions 1, 50–54.CrossRefGoogle Scholar
Zhang, Z, Schwartz, S, Wagner, L and Miller, W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203–214.CrossRefGoogle ScholarPubMed
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