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Geography and ecology of invasive Pseudosuccinea columella (Gastropoda: Lymnaeidae) and implications in the transmission of Fasciola species (Digenea: Fasciolidae) – a review

Published online by Cambridge University Press:  07 January 2022

P.I. Ngcamphalala*
Affiliation:
School of Life Science, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville campus, Durban4001, South Africa
M.P. Malatji
Affiliation:
School of Life Science, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville campus, Durban4001, South Africa Foundational Research & Services, South African National Biodiversity Institute, Pretoria0001, South Africa
S. Mukaratirwa
Affiliation:
School of Life Science, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville campus, Durban4001, South Africa One Health Centre for Zoonoses and Tropical Veterinary Medicine, Ross University School of Veterinary Medicine, Basseterre, St Kitts and Nevis
*
Author for correspondence: P.I. Ngcamphalala, E-mail: [email protected]

Abstract

Pseudosuccinea columella is considered invasive and has become an important intermediate host of both Fasciola species in many regions of the world. This systematic review assessed the geographical distribution of P. columella, and its implications in the transmission of Fasciola hepatica and Fasciola gigantica, globally. A literature search was conducted on Google Scholar, JSTOR and PubMed databases using Boolean operators in combination with predetermined search terms for thematic analysis. Results show that P. columella has been documented in 22 countries from Europe (3), Africa (8), Oceania (2), North America (3) and South America (6). Furthermore, this snail species has shown to adapt to and inhabit a vast array of freshwater bodies including thermal lakes and ditches with acidic soils. Studies showed that P. columella transmits F. hepatica, with natural and experimental infections documented in sub-Saharan Africa, Europe, South America and North America. Experimental infection studies in Cuba showed the presence of P. columella populations resistant to F. hepatica infection. Furthermore, some populations of this invasive snail collected from F. hepatica endemic locations in Brazil, Venezuela, Australia, South Africa, Colombia and Argentina were found without Fasciola infection. As a result, the role played by this snail in the transmission of Fasciola spp. in these endemic areas is still uncertain. Therefore, further studies to detect natural infections are needed in regions/countries where the snail is deemed invasive to better understand the veterinary and public health importance of this snail species in Fasciola-endemic areas and determine the global dispersion of resistant populations of P. columella.

Type
Review Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abd El-Wakeil, KF, Obuid-Allah, AH, Mohamed, AH and Abd El-Aziz, FEA (2013) Community structure of molluscans in river Nile and its branches in Assiut governorate, Egypt. Egyptian Journal of Aquatic Research 39, 193198.CrossRefGoogle Scholar
Admassu, B, Shite, A and Kinfe, G (2015) A review on bovine fasciolosis. European Journal of Biological Sciences 7, 139146.Google Scholar
Alba, A, Vázquez, AA, Sánchez, J, Duval, D, Hernández, HM, Sabourin, E, Vittecoq, M, Hurtrez-Boussés, S and Gourbal, B (2018) Fasciola hepaticaPseudosuccinea columella interaction: effect of increasing parasite doses, successive exposures and geographical origin on the infection outcome of susceptible and naturally resistant snails from Cuba. Parasites and Vectors 11, 19.CrossRefGoogle ScholarPubMed
Alba, A, Tetreau, G, Chaparro, C, Sánchez, J, Vazquez, AA and Gourbal, B (2019a) Natural resistance to Fasciola hepatica (Trematoda) in Pseudosuccinea columella snails: a review from literature and insights from comparative “omic” analyses. Developmental & Comparative Immunology 101, 114.CrossRefGoogle Scholar
Alba, A, Vázquez, AA, Sánchez, J, Lounnas, M, Pointier, J, Hurtrez-Boussè, S and Gourbal, B (2019b) Patterns of distribution, population genetics and ecological requirements of field-occurring resistant and susceptible Pseudosuccinea columella snails to Fasciola hepatica in Cuba. Nature Research 9, 115.Google Scholar
Alemu, B (2019) Bovine fasciolosis in Ethiopia–a review. Journal of Veterinary and Animal Research 2, 112.Google Scholar
Bardales-Valdivia, JN, Bargues, MD, Hoban-Vergara, C, Bardales-Bardales, C, Goicochea-Portal, C, Bazán-Zurita, H, Del Valle-Mendoza, J, Ortiz, P and Mas-Coma, S (2021) Spread of the fascioliasis endemic area assessed by seasonal follow-up of rDNA ITS-2 sequenced lymnaeid populations in Cajamarca, Peru. One Health 13, 18.CrossRefGoogle ScholarPubMed
Bargues, MD, Artigas, P, Mera y Sierra, RL, Pointier, J-P and Mas-Coma, S (2007) Characterisation of Lymnaea cubensis, L. viatrix and L. neotropica n. sp., the main vectors of Fasciola hepatica in Latin America, by analysis of their ribosomal and mitochondrial DNA. Annals of Tropical Medicine and Parasitology 101, 621641.CrossRefGoogle Scholar
Bargues, MS, González, LC, Artigas, P and Mas-Coma, S (2011) A new baseline for fascioliasis in Venezuela: lymnaeid vectors ascertained by DNA sequencing and analysis of their relationships with human and animal infection. Parasites and Vectors 4, 118.CrossRefGoogle ScholarPubMed
Bargues, MD, Gayo, V, Sanchis, J, Artigas, P, Khoubbane, M, Birriel, S and Mas-Coma, S (2017) DNA multigene characterization of Fasciola hepatica and Lymnaea neotropica and its fascioliasis transmission capacity in Uruguay, with historical correlation, human report review and infection risk analysis. PLoS Neglected Tropical Diseases 11, 133.CrossRefGoogle ScholarPubMed
Beesley, NJ, Caminade, C, Charlier, J, et al. (2018) Fasciola and fasciolosis in ruminants in Europe: identifying research needs. Transboundary and Emerging Diseases 65, 199216.CrossRefGoogle ScholarPubMed
Brown, D (1994) Freshwater snails of Africa and their medical importance. London, Taylor & Francis.CrossRefGoogle Scholar
Calienes, AF, Fraga, J, Pointier, J-P, Yong, M, Sanchez, J, Coustau, C, Gutiérrez, A and Théron, A (2004) Detection and genetic distance of resistant populations of Pseudosuccinea columella (Mollusca: Lymnaeidae) to Fasciola hepatica (Trematoda: Digenea) using RAPD markers. Acta Tropica 92, 8387.CrossRefGoogle ScholarPubMed
Cardoso, PCM, Caldiero, RL, Lovato, MB, Coelho, PMZ, Berne, MEA, Muller, G and Carvalho, O (2006) Genetic variability of Brazilian populations of Lymnaea columella (Gastropoda: Lymnaeidae), an intermediate host of Fasciola hepatica (Trematoda: Digenia). Acta Tropica 97, 339345.CrossRefGoogle Scholar
Carolus, H, Muzarabani, KC, Hammoud, C, Schols, R, Volckaert, FAM, Barson, M and Huyse, T (2019) A cascade of biological invasions and parasite spillback in man-made Lake Kariba. Science of the Total Environment 659, 12831292.CrossRefGoogle ScholarPubMed
Caron, Y, Rondelaud, D and Losson, B (2008) The detection and quantification of a digenean infection in the snail host with special emphasis on Fasciola sp. Parasitology Research 103, 735744.CrossRefGoogle ScholarPubMed
Charlier, J, Soenen, K, De Roeck, E, Hantson, W, Ducheyne, E, Van Coillie, F, De Wulf, R, Hendrickx, G and Vercruysse, J (2014) Longitudinal study on the temporal and micro-spatial distribution of Galba truncatula in four farms in Belgium as a base for small-scale risk mapping of Fasciola hepatica. Parasites & Vectors 7, 18.CrossRefGoogle ScholarPubMed
Chen, J-X, Chen, M-X, Ai, L, et al. (2013) An outbreak of human Fascioliasis gigantica in Southwest China. PLoS One 8, 110.Google ScholarPubMed
Cianfanelli, S, Lori, E and Bodon, M (2007) Non-indigenous freshwater molluscs and their distribution in Italy. pp. 103–121 in Gherardi, F (Ed.), Biological invaders in inland waters: Profiles, distribution, and threats. Dordrecht, Springer.Google Scholar
Coelho, LHL, Guimaraes, MP and Lima, WS (2008) Influence of shell size of Lymnaea columella on infectivity and development of Fasciola hepatica. Journal of Helminthology 82, 7780.CrossRefGoogle ScholarPubMed
Correa, AC, Escobar, JS, Durand, P, Renaud, F, David, P, Jarne, P, Pointier, J and Hurtrez-Boussès, S (2010) Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of fascioliasis. BMC Evolutionary Biology 10, 112.CrossRefGoogle Scholar
Cowie, RH (1998) Patterns of introduction of non-indigenous non-marine snails and slugs in the Hawaiian Islands. Biodiversity and Conservation 7, 349368.CrossRefGoogle Scholar
Cucher, MA, Carnevale, S, Prepelitchi, L, Labbé, JH and Wisnivesky-Colli, C (2006) PCR diagnosis of Fasciola hepatica in field collected Lymnaea columella and Lymnaea viatrix snails. Veterinary Parasitology 137, 7482.CrossRefGoogle ScholarPubMed
Curtis, BA (1991) Freshwater macro-invertebrates of Namibia. Madoqua 17, 163187.Google Scholar
D'Almeida, SCG, Freitas, DF, Carneiro, MB, Camargo, PF, Azevedo, JC and Martins, IVF (2016) The population density of Lymnaea columella (Say, 1817) (Mollusca, Lymnaeidae) an intermediate host of Fasciola hepatica (Linnaeus, 1758), in the Caparaó microregion, ES, Brazil. Brazilian Journal of Biology 76, 334340.CrossRefGoogle Scholar
Dar, Y, Rondelaud, D, Vignoles, P and Dreyfuss, G (2014) Fasciola hepatica: development of redial generations in experimental infections of Pseudosuccinea columella. Parasitology Research 113, 24672473.CrossRefGoogle ScholarPubMed
Dar, Y, Rondelaud, D, Vignoles, P and Dreyfuss, G (2015a) Fasciola hepatica: the redial generations in juvenile Pseudosuccinea columella. Parasitology Research 114, 28452851.CrossRefGoogle Scholar
Dar, Y, Vignoles, P, Rondelaud, D and Dreyfuss, G (2015b) Role of the lymnaeid snail Pseudosuccinea columella in the transmission of the liver fluke Fasciola hepatica in Egypt. Journal of Helminthology 89, 699706.CrossRefGoogle Scholar
Dar, Y, Amer, S, Eddine, RZ and Dreyfuss, G (2016) Characterisation of Pseudosuccinea columella and Radix natalensis (Gastropoda: Lymnaeidae) in Egypt using shell and molecular data. Molluscan Research 36, 2228.CrossRefGoogle Scholar
Davies, D, Nieva, L, Choke, LA, Issa, FS, Pujadas, J and Prepelitchi, L (2014) First record of Pseudosuccinea columella (Say, 1817) from Salta province, northwest Argentina (Mollusca: Gastropoda: Lymnaeidae). Check List 10, 597599.CrossRefGoogle Scholar
de Kock, KN and Wolmarans, CT (1998) A re-evaluation of the occurrence of freshwater molluscs in the Kruger National Park. Koedoe 41, 18.CrossRefGoogle Scholar
de Kock, KN and Wolmarans, CT (2008) Invasive alien freshwater snail species in the Kruger National Park, South Africa. Koedoe 50, 4953.CrossRefGoogle Scholar
de Kock, K, Joubert, PH and Pretorius, SJ (1989) Geographical distribution and habitat preferences of the invader freshwater snail species Lymnaea columella (Mollusca: Gastropoda) in South Africa. Onderstepoort Journal of Veterinary Research 56, 271275.Google ScholarPubMed
de Kock, KN, Wolmarans, CT and du Preez, LH (2002) Freshwater mollusc diversity in the Kruger National Park: a comparison between a period of prolonged drought and a period of exceptionally high rainfall. Koedoe 45, 111.CrossRefGoogle Scholar
Dreyfuss, G, Vignoles, P and Rondelaud, D (2016) Pseudosuccinea columella: experimental co-infections of juvenile and pre-adult snails with the digeneans Calicophoron daubneyi and Fasciola hepatica. Journal of Helminthology 90, 17.CrossRefGoogle ScholarPubMed
Duffy, T, Kleiman, F, Pietrokovsky, S, Issia, L, Schijman, AG and Wisnivesky-Colli, C (2009) Real-time PCR strategy for rapid discrimination among main lymnaeid species from Argentina. Acta Tropica 109, 14.CrossRefGoogle ScholarPubMed
Dung, BT, Doanh, PN, The, DT, Loan, HT, Losson, B and Caron, Y (2013) Morphological and molecular characterization of lymnaeid snails and their potential role in transmission of Fasciola spp. in Vietnam. Korean Journal of Parasitology 51, 657662.CrossRefGoogle ScholarPubMed
El-Kady, GA, Shoukry, A, Reda, LA and El-Badri, YS (2000) Survey and population dynamics of freshwater snails in newly settled areas of the Sinai Peninsula. Egyptian Journal of Biology 2, 4248.Google Scholar
Gasnier, N, Rondelaud, D, Abrous, M, Carreras, F, Boulard, C, Diez-Baños, P and Cabaret, J (2000) Allopatric combination of Fasciola hepatica and Lymnaea truncatula is more efficient than sympatric ones. International Journal for Parasitology 30, 573578.CrossRefGoogle ScholarPubMed
Glöer, P and Sîrbu, I (2005) New freshwater molluscs species found in the Romanian fauna. Heldia 6, 229238.Google Scholar
Grabner, DS, Mohamed, FAMM, Nachev, M, Meabed, EMH, Sabry, AHA and Sures, B (2014) Invasion biology meets parasitology: a case study of parasite spill-back with Egyptian Fasciola gigantica in the invasive snail Pseudosuccinea columella. PLoS One 9, 17.CrossRefGoogle ScholarPubMed
Gutiérrez, A, Perera, G, Yong, M and Wong, L (2001) The effect of isolation on the life-history traits of Pseudosuccinea columella (Pulmonata: Lymnaeidae). Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 96, 577581.CrossRefGoogle Scholar
Gutiérrez, A, Yong, M, Perera, G, Sánchez, J and Théron, A (2002) Fasciola hepatica (Trematoda: Digenea): its effect on the life history traits of Pseudosuccinea columella (Gasteropoda: Lymnaeidae), an uncommon interaction. Parasitology Research 88, 535539.CrossRefGoogle Scholar
Gutierrez, A, Pointier, J-P, Yong, M, Sánchez, J and Théron, A (2003) Evidence of phenotypic differences between resistant and susceptible isolates of Pseudosuccinea columella (Gastropoda: Lymnaeidae) to Fasciola hepatica (Trematoda: Digenea) in Cuba. Parasitology Research 90, 129134.CrossRefGoogle Scholar
Gutiérrez, A, Hernandez, DF and Sánchez, J (2005) Variation of snail's abundance in two water bodies harboring strains of Pseudosuccinea columella resistant and susceptible to Fasciola hepatica miracidial infection, in Pinar del Río Province, Cuba. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 100, 725727.CrossRefGoogle Scholar
Gutierrez, A, Vázquez, AA, Hevia, Y, Sánchez, J, Correa, AC, Hurtrez-Boussès, S, Pointier, J-P and Théron, A (2011) First report of larval stages of Fasciola hepatica in a wild population of Pseudosuccinea columella from Cuba and the Caribbean. Journal of Helminthology 85, 109111.CrossRefGoogle Scholar
Hubendick, B (1951) Recent Lymnaeidae, their variation, morphology, taxonomy, nomenclature, and distribution. Kungliga Svenska Vetenskapsakademiens Handlingar 3, 1223.Google Scholar
Kemp, M, de Kock, KN, Zaayman, JL and Wolmarans, CT (2016) A comparison of mollusc diversity between the relatively pristine Marico River and the impacted Crocodile River, two major tributaries of the Limpopo River, South Africa. Water SA 42, 253260.CrossRefGoogle Scholar
Kleiman, F, Pietrokovsky, S, Prepelitchi, L, Carbajo, AE and Wisnivesky-Colli, C (2007) Dynamics of Fasciola hepatica transmission in the Andean Patagonian valleys, Argentina. Veterinary Parasitology 145, 274286.CrossRefGoogle ScholarPubMed
Leka, FL (2019) The prevalence of bovine fasciolosis and hydatidosis at Wolita Soddo municipal abattoir, Southern Ethiopia. International Journal of Research Studies in Biosciences 7, 2744.Google Scholar
Lofty, WM and Lofty, LM (2015) Synopsis of the Egyptian freshwater snail fauna. Folia Malacologica 23, 1940.Google Scholar
Lounnas, M, Correa, AC, Vazquez, AA, et al. (2017) Self-fertilization, long-distance flash invasion and biogeography shape the population structure of Pseudosuccinea columella at the worldwide scale. Molecular Ecology 26, 887903.CrossRefGoogle Scholar
Magalhães, KG, Passos, LKJ and dos Santos Carvalho, O (2004) Detection of Lymnaea columella infection by Fasciola hepatica through Multiplex-PCR. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 99, 421424.CrossRefGoogle ScholarPubMed
Malatji, MP and Mukaratirwa, S (2019) Molecular detection of natural infection of Lymnaea (Pseudosuccinea) columella (Gastropoda: Lymnaeidae) with Fasciola gigantica (Digenea: Fasciolidae) from two provinces of South Africa. Journal of Helminthology 94, 16.Google Scholar
Malatji, MP, Lamb, J and Mukaratirwa, S (2019) Molecular characterization of liver fluke intermediate host lymnaeids (Gastropoda: Pulmonata) snails from selected regions of the Okavango Delta of Botswana, KwaZulu-Natal, and Mpumalanga provinces of South Africa. Veterinary Parasitology: Reginal Studies and Reports 17, 16.Google Scholar
Martin, PR, Ovando, XNC and Seuffert, ME (2016) First record of the freshwater snail Pseudosuccinea columella (Gastropoda: Lymnaeidae) in southern Pampas (Argentina) and assessment of future spread. Molluscan Research 36, 213221.CrossRefGoogle Scholar
Mas-Coma, S (2004) Human fascioliasis: epidemiological patterns in human endemic areas of South America, Africa and Asia. The Southeast Asian Journal of Tropical Medicine and Public Health 35, 111.Google Scholar
Mas-Coma, S (2005) Epidemiology of fascioliasis in human endemic areas. Journal of Helminthology 79, 207216.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Bargues, MD and Valero, MA (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 12551278.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Valero, MA and Bargues, MD (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41146.CrossRefGoogle ScholarPubMed
McKown, RD and Ridley, RK (1995) Distribution of fasciolosis in Kansas, with results of experimental snail susceptibility. Veterinary Parasitology 56, 281291.CrossRefGoogle ScholarPubMed
Mendes, EA, Lima, WS and de Melo, AL (2008) Development of Fasciola hepatica in Lymnaea columella infected with miracidia derived from cattle and marmoset infections. Journal of Helminthology 82, 8184.CrossRefGoogle ScholarPubMed
Mochankana, ME and Robertson, ID (2018) Cross-sectional prevalence of Fasciola gigantica infections in beef cattle in Botswana. Tropical Animal Health and Production 50, 13551363.CrossRefGoogle ScholarPubMed
Molloy, JB and Anderson, GR (2006) The distribution of Fasciola hepatica in Queensland, Australia, and the potential impact of introduced snail intermediate hosts. Veterinary Parasitology 137, 6266.CrossRefGoogle ScholarPubMed
Pereira, AE, Uribe, N and Pointier, J-P (2020) Lymnaeidae from Santander and bordering departments of Colombia: morphological characterization, molecular identification and natural infection with Fasciola hepatica. Veterinary Parasitology: Regional Studies and Reports 20, 19.Google ScholarPubMed
Pereira de Souza, CP, Magalhães, KG, Passos, LKJ, Pereira dos Santos, GC, Ribeiro, F and Naftale, K (2002) Aspects of the maintenance of the life cycle of Fasciola hepatica in Lymnaea columella in Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 97, 407410.CrossRefGoogle Scholar
Perissinotto, R, Miranda, NAF, Raw, JL and Peer, N (2014) Biodiversity census of lake St Lucia, iSimangaliso Wetland Park (South Africa): gastropod molluscs. ZooKeys 440, 143.CrossRefGoogle Scholar
Pointier, J-P, Coustau, C, Rondelaud, D and Théron, A (2007) Pseudosuccinea columella (Say 1817) (Gastropoda, Lymnaeidae), snail host of Fasciola hepatica: first record for France in the wild. Parasitology Research 101, 13891392.CrossRefGoogle ScholarPubMed
Pointier, J-P, Noya, O, Alarcón de Noya, B and Théron, A (2009) Distribution of Lymnaeidae (Mollusca: Pulmonata), intermediate snail hosts of Fasciola hepatica in Venezuela. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 104, 790796.CrossRefGoogle Scholar
Prepelitchi, L, Kleiman, F, Pietrokovsky, SM, Moriena, RA, Racioppi, O, Alvarez, J and Wisnivesky-Colli, C (2003) First report of Lymnaea columella Say, 1817 (Pulmonata: Lymnaeidae) naturally infected with Fasciola hepatica (Linnaeus, 1758) (Trematoda: Digenea) in Argentina. Memórias do Instituto Oswaldo Cruz 98, 889891.CrossRefGoogle Scholar
Prepelitchi, L, Pietrokovsky, S, Kleiman, F, Rubel, D, Issia, L, Moriena, R, Racioppi, O, Álvarez, J and Wisnivesky-Colli, C (2011) Population structure and dynamics of Lymnaea columella (Say, 1817) (Gastropoda: Lymnaeidae) in wetlands of northeastern Argentina. Zoological Studies 50, 164176.Google Scholar
Sabourin, E, Alda, P, Vázquez, A, Hurtrez-Boussès, S and Vittecoq, M (2018) Impact of human activities on fasciolosis transmission. Trends in Parasitology 34, 891903.CrossRefGoogle ScholarPubMed
Salazar, L, Estrada, VE and Velásquez, LE (2006) Effect of the exposure to Fasciola hepatica (Trematoda: Digenea) on life history traits of Lymnaea cousini and Lymnaea columella (Gastropoda: Lymnaeidae). Experimental Parasitology 114, 7783.CrossRefGoogle Scholar
Sanabria, R, Mouzet, R, Courtioux, B, Vignoles, P, Rondelaud, D, Dreyfuss, G, Cabaret, J and Romero, J (2012) Intermediate snail hosts of French Fasciola hepatica: Lymnaea neotropica and Lymnaea viatrix are better hosts than local Galba truncatula. Parasitology Research 111, 20112016.CrossRefGoogle ScholarPubMed
Tchakonté, S, Ajeagah, GA, Diomandé, D, Camara, AI and Ngassam, P (2014) Diversity, dynamic and ecology of freshwater snails related to environmental factors in urban and suburban streams in Douala-Cameroon (Central Africa). Aquatic Ecology 48, 379395.CrossRefGoogle Scholar
Valero, MA, Darce, NA, Panova, M and Mas-Coma, S (2001) Relationships between species and morphometric patterns in Fasciola hepatica adults and eggs from the Northern Bolivian Altiplano hyperendemic region. Veterinary Parasitology 102, 85100.CrossRefGoogle Scholar
Vázquez, AA, Sánchez, J, Pointier, J-P, Théron, A and Hurtrez-Boussès, S (2014) Fasciola hepatica in Cuba: compatibility of different isolates with two intermediate snail hosts, Galba cubensis and Pseudosuccinea columella. Journal of Helminthology 88, 434440.CrossRefGoogle ScholarPubMed
Vázquez, AA, Sabourin, E, Alda, P, et al. (2020) Genetic diversity and relationships of the liver fluke Fasciola hepatica (Trematoda) with native and introduced definitive and intermediate hosts. Transboundary and Emerging Diseases 68, 113.Google ScholarPubMed
Vignoles, P, Dreyfuss, G and Rondelaud, D (2015) Fasciola hepatica: comparative metacercarial productions in experimentally infected Galba truncatula and Pseudosuccinea columella. Parasite 22, 18.CrossRefGoogle ScholarPubMed
Vignoles, P, Dreyfuss, G and Rondelaud, D (2018) Consequences of invasion by Pseudosuccinea columella on the dynamics of native lymnaeids living on the acid soils of central France. Molluscan Research 38, 287295.CrossRefGoogle Scholar
Vorster, JH and Mapham, PH (2008) Fasciolosis in livestock. Jaargang 10, 612.Google Scholar
Wolmarans, CT and de Kock, KN (2006) The current status of freshwater molluscs in the Kruger National Park. Koedoe 49, 3944.CrossRefGoogle Scholar
Zarco, A, Fantozzi, MC and Cuervo, PF (2011) Gastropoda, Pulmonata, Lymnaeidae, Pseudosuccinea columella (Say, 1817): first record in Córdoba province, central Argentina. Check List 7, 391393.CrossRefGoogle Scholar