Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-17T10:14:29.648Z Has data issue: false hasContentIssue false

First integrative study of the diversity and specificity of metacercariae of Posthodiplostomum Dubois, 1936 from native and introduced fishes in the Caribbean

Published online by Cambridge University Press:  24 August 2022

Sandra C. Díaz Pernett
Affiliation:
Department of Biology, University of Puerto Rico at Mayagüez, Call Box 9000, Mayagüez, Puerto Rico 00681, USA
Sara V. Brant
Affiliation:
Museum of Southwestern Biology Division of Parasites MSC03 2020, Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA
Sean A. Locke*
Affiliation:
Department of Biology, University of Puerto Rico at Mayagüez, Call Box 9000, Mayagüez, Puerto Rico 00681, USA
*
Author for correspondence: Sean A. Locke, E-mail: [email protected]

Abstract

Metacercariae of the genus Posthodiplostomum are often recorded in freshwater fish hosts. While the diversity and taxonomy of this genus are receiving increasing attention in molecular phylogenetic studies, available data remain geographically biased. Most molecular studies of Posthodiplostomum and morphologically similar (neascus) worms originate in North America and Europe and Asia (more than 60% of DNA sequences are from USA and Canada), with few data currently available from the Neotropics, where high host diversity suggests high and under-sampled parasite diversity. In this study, we report molecular and morphological data from metacercariae of Posthodiplostomum in fish in Puerto Rico, where only a single species has been previously reported. Partial sequences of cytochrome c oxidase subunit 1 from metacercariae from Dajaus monticola (native to Puerto Rico) and the introduced fishes Poecilia reticulata, Parachromis managuensis, Lepomis macrochirus and Micropterus salmoides revealed 7 genetically distinct species-level lineages, of which 4 were novel. We report novel molecular life-cycle linkages in Posthodiplostomum macrocotyle (metacercariae in muscle of the cichlid Pa. managuensis), a species previously known only from adults in birds from South America; and in Posthodiplostomum sp. 23 (metacercariae in poeciliids), which has recently been found in Ardea herodias in Georgia, USA. We also report the first molecular data from Posthodiplostomum sp. 8 in M. salmoides in the Caribbean. Metacercariae of most species were morphologically distinguished and all displayed narrow specificity for fish hosts, with no indication of parasite sharing among introduced and native fishes.

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

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

Achatz, TJ, Pulis, EE, Fecchio, A, Schlosser, IJ and Tkach, VV (2019) Phylogenetic relationships expanded diversity and distribution of Crassiphiala spp. (Digenea, Diplostomidae), agents of black spot disease in fish. Parasitology Research 118, 27812787.CrossRefGoogle ScholarPubMed
Achatz, TJ, Chermak, TP, Martens, JR, Pulis, EE, Fecchio, A, Bell, JA, Greiman, SE, Cromwell, KJ, Brant, SV, Kent, ML and Tkach, VV (2021) Unravelling the diversity of the Crassiphialinae (Digenea: Diplostomidae) with molecular phylogeny and descriptions of five new species. Current Research in Parasitology & Vector-Borne Diseases 1, 100051.CrossRefGoogle ScholarPubMed
Athokpam, VD and Tandon, V (2014) Morphological and molecular characterization of Posthodiplostomum sp. (Digenea: Diplostomidae) metacercaria in the muscles of snakeheads (Channa punctata) from Manipur, India. Helminthologia 51, 141152.CrossRefGoogle Scholar
Azevedo, RK, Abdallah, VD and Luque, JL (2006) Ecologia da comunidade de metazoários parasitos do Acará Geophagus brasiliensis (Quoy e Gaimard, 1824) (Preciformes: Cichlidae) do Rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Scientiarum. Biological Sciences 28, 403411.Google Scholar
Azevedo, RK, Abdallah, VD and Luque, JL (2011) Biodiversity of fish parasites from Guandu River, Southeastern Brazil: an ecological approach. Neotropical Helminthology 5, 185199.Google Scholar
Bagley, JC, Alda, F, Breitman, MF, Bermingham, E, van den Berghe, EP and Johnson, JB (2015) Assessing species boundaries using multilocus species delimitation in a morphologically conserved group of Neotropical freshwater fishes, the Poecilia sphenops species complex (Poeciliidae). PLoS ONE 10, e0121139.CrossRefGoogle Scholar
Balian, E, Segers, H, Lévêque, C and Martens, K (2008) The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595, 627637.CrossRefGoogle Scholar
Blair, D (1977) A key to cercariae of British strigeoids (Digenea) for which the life-cycles are known, and notes on the characters used. Journal of Helminthology 51, 155166.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Locke, SA (2017) Life history, systematics and evolution of the Diplostomoidea Poirier, 1886: progress, promises and challenges emerging from molecular studies. Advances in Parasitology 98, 167225.CrossRefGoogle ScholarPubMed
Boone, EC, Laursen, JR, Colombo, RE, Meiners, SJ, Romani, MF and Keeney, DB (2018) Infection patterns and molecular data reveal host and tissue specificity of Posthodiplostomum species in centrarchid hosts. Parasitology 145, 14581468.CrossRefGoogle ScholarPubMed
Brandaõ, M, Luque, LL, Szholz, T and Kostadinova, A (2013) New records and descriptions of digeneans from the Magellanic penguin Spheniscus magellanicus (Forster) (Aves: Sphenisciformes) on the coast of Brazil. Systematic Parasitology 85, 7998.CrossRefGoogle ScholarPubMed
Bunkley-Williams, L and Williams, EH Jr. (1994) Parasites of Puerto Rican Freshwater Sport Fishes. Puerto Rico Department of Natural and Environmental Resources, San Juan, PR and Department of Marine Sciences, University of Puerto Rico, Mayaguez, PR, 168 pp.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis, et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cancel-Villamil, JJ and Locke, SA (2022) Fish assemblage response to removal of a low head dam in the lower reach of a tropical island river. Freshwater Biology 67, 926937.CrossRefGoogle Scholar
Cech, G, Sándor, D, Molnár, K, Paulus, P, Papp, M, Preiszner, B, Vitál, Z, Varga, Á and Székely, C (2020) New record of metacercariae of the North American Posthodiplostomum centrarchi (Digenea, Diplostomidae) in pumpkinseed (Lepomis gibbosus) in Hungary. Acta Veterinaria Hungarica 68, 2029.CrossRefGoogle Scholar
Clarke, K and Gorley, R (2015) PRIMER v7: User Manual/Tutorial. PRIMER-E: Plymouth. UK: PRIMER-E Ltd.Google Scholar
Concheiro Pérez, GA, Říčan, O, Ortí, G, Bermingham, E, Doadrio, I and Zardoya, R (2007) Phylogeny and biogeography of 91 species of heroine cichlids (Teleostei: Cichlidae) based on sequences of the cytochrome b gene. Molecular Phylogenetics and Evolution 43, 91110.CrossRefGoogle Scholar
Conkel, D (1993) Cichlids of North and Central America. New Jersey, USA: TFH Publications Inc.Google Scholar
Cribb, TH, Bray, RA, Justine, JL, Reimer, J, Sasal, P, Shirakashi, S and Cutmore, SC (2022) A world of taxonomic pain: cryptic species, inexplicable host-specificity, and host-induced morphological variation among species of Bivesicula Yamaguti, 1934 (Trematoda: Bivesiculidae) from Indo-Pacific Holocentridae, Muraenidae and Serranidae. Parasitology 149, 831853.CrossRefGoogle Scholar
Daszak, P, Cunningham, AA and Hyatt, AD (2000) Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443449.CrossRefGoogle ScholarPubMed
Deacon, AE, Ramnarine, IW and Magurran, AE (2011) How reproductive ecology contributes to the spread of a globally invasive fish. PLoS ONE 6, e24416.CrossRefGoogle Scholar
Domitch, IF and Sarabeev, VL (2000) The trematodes of the far-east-mullet-pelingas (Mugil soiuy) in the Azov Sea aquatories. Vestnik Zoologii 34, 715.Google Scholar
Drago, FB, Lunaschi, LI and Draghi, R (2014) Digenean fauna in raptors from northeastern Argentina, with the description of a new species of Strigea (Digenea: Strigeidae). Zootaxa 3785, 258270.CrossRefGoogle ScholarPubMed
Dubois, G (1936) Nouveaux principes de classification des trématodes du groupe des Strigeida. Note préliminaire. Revue Suisse de Zoologie 43, 507515.CrossRefGoogle Scholar
Dubois, G (1937) Sur quelques Strigéidés (notes préliminaires). Revue Suisse de Zoologie 44, 391396.CrossRefGoogle Scholar
Dubois, G (1938) Monographie des Strigeida (Trematoda). Mémoires de la Société Neuchateloise des Sciences Naturelles 6, 1535.Google Scholar
Dubois, G (1970 a) Les Strigeata (Trematoda) de la collection A. Lutz. Memórias do Instituto Oswaldo Cruz 68, 169196.CrossRefGoogle Scholar
Dubois, G (1970 b) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mémoires de la Société des Sciences Naturelles 2, 259727.Google Scholar
Dubois, G and Macko, J (1972) Contribution à l’étude des Strigeata La Rue, 1926 (Trematoda: Strigeida) de Cuba. Annales de Parasitologie Humaine et Comparée 47, 5175.CrossRefGoogle Scholar
Dyer, WG, Williams, L and Williams, E Jr. (1998) First record in Puerto Rico of Spinitectus agonostomi (Nematoda: Cystidicolidae) from the mountain mullet (Agonostomus monticola). Caribbean Journal of Science 34, 12.Google Scholar
Ebbs, ET, Loker, ES and Brant, SV (2018) Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes. BMC Evolutionary Biology 18, 103.CrossRefGoogle ScholarPubMed
Gibson, DI (1996) Trematoda. In Margolis, L and Kabata, Z (eds), Guide to the Parasites of Fishes of Canada. Part IV. Canadian Special Publication of Fisheries and Aquatic Sciences, vol. 124. Ottawa: NRC Research Press, pp. 1363.Google Scholar
Hendrickson, GL (1986) Observations on the life cycle of Ornithodiplostomum ptychocheilus (Trematoda: Diplostomatidae). Proceedings of the Helminthological Society of Washington 1, 166172.Google Scholar
Hoffman, G (1955) Neascus nolfi n. sp. (Trematoda: Strigeida) from cyprinid minnows with notes on the artificial digest recovery of helminths. American Midland Naturalist 53, 198204.CrossRefGoogle Scholar
Hoffman, G (1958) Studies on the life-cycle of Ornithodiplostomum ptychocheilus (Faust) (Trematoda: Strigeoidea) and the ‘self cure’ of infected fish. Journal of Parasitology 44, 416421.CrossRefGoogle ScholarPubMed
Hoffman, GL (1960) Synopsis of Strigeoidea (Trematoda) of fishes and their life cycles. Fishery Bulletin 175, 439469.Google Scholar
Hoffman, GL (1999) Parasites of North American Freshwater Fishes. Ithaca, NY: Cornell University Press, 539 pp.CrossRefGoogle Scholar
Holmes, BJ, Williams, SM and Power, TN (2020) Evidence of naturalisation of the invasive jaguar cichlid Parachromis managuensis (Günther, 1867), in Queensland, Australia. BioInvasions Records 9, 146157.CrossRefGoogle Scholar
Hoogendoorn, C, Smit, NJ and Kudlai, O (2019) Molecular and morphological characterization of four diplostomid metacercariae infecting Tilapia sparrmanii (Perciformes: Cichlidae) in the North West Province, South Africa. Parasitology Research 118, 14031416.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Hughes, RC (1927) Studies on the trematode family Strigeidae (Holostomidae) No. VI. A new metacercaria Neascus ambloplitis, sp. nov., representing a new larval group. Transactions of the American Microscopical Society 46, 248267.CrossRefGoogle Scholar
Ivanova, N, Dewaard, JR and Hebert, PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6, 9981002.CrossRefGoogle Scholar
Komatsu, N, Itoh, N and Ogawa, K (2020) Heavy metacercarial infection in the abdominal cavity of hatchery-reared Japanese dace Tribolodon hakonensis. Fish Pathology 55, 5360.CrossRefGoogle Scholar
Krailas, D, Namchote, S, Koonchornboon, T, Dechruksa, W and Boonmekam, D (2014) Trematodes obtained from the thiarid freshwater snail Melanoides tuberculata (Müller, 1774) as vector of human infections in Thailand. Zoosystematics and Evolution 28, 57.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, 15471549.CrossRefGoogle ScholarPubMed
Kvach, Y, Jurajda, P, Bryjová, A, Trichkova, T, Ribeiro, F, Přikrylová, I and Ondračková, M (2017) European distribution for metacercariae of the North American digenean Posthodiplostomum cf. minimum centrarchi (Strigeiformes: Diplostomidae). Parasitology International 66, 635642.CrossRefGoogle ScholarPubMed
Kwak, TJ, Cooney, PB and Brown, CH (2007) Fishery Population and Habitat Assessment in Puerto Rico Streams: Phase 1 Final Report. Federal Aid in Sport Fish Restoration Project F-50 Final Report. Marine Resources Division, San Juan: Puerto Rico Department of Natural and Environmental Resources.Google Scholar
Lafferty, K, Smith, KF, Torchin, ME, Dobson, AP and Kuris, A (2005) The role of infectious diseases in natural communities: what introduced species tell us. In Sax, DF, Stachowicz, JJ and Gaines, SD (eds), Species Invasions: Insights Into Ecology, Evolution and Biogeography. Sunderland, MA, USA: Sinauer Associates, pp. 111134.Google Scholar
Lane, R and Morris, J (2000) Biology, prevention, and effects of common grubs (digenetic trematodes) in freshwater fish. Technical Bulletin Series 115, 16.Google Scholar
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, DJ (2010) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 28132827.CrossRefGoogle Scholar
Locke, SA, Al-Nasiri, FS, Caffara, M, Drago, F, Kalbe, M, Lapierre, AR, McLaughlin, JD, Nie, P, Overstreet, RM, Souza, GT, Takemoto, RM and Marcogliese, DJ (2015) Diversity, specificity, and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal of Parasitology 45, 841855.CrossRefGoogle ScholarPubMed
Locke, SA, Van Dam, A, Caffara, M, Pinto, HA, López-Hernández, D and Blanar, CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal of Parasitology 48, 10431059.CrossRefGoogle ScholarPubMed
López-Hernández, D, Locke, SA, De Melo, AL, Rabelo, EM and Pinto, H (2018) Molecular, morphological, and experimental assessment of the life cycle of Posthodiplostomum nanum Dubois 1937 (Trematoda: Diplostomidae) from Brazil, with phylogenetic evidence of the paraphyly of the genus Posthodiplostomum Dubois, 1936. Infection, Genetics and Evolution 63, 95103.CrossRefGoogle ScholarPubMed
Marcogliese, DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352.CrossRefGoogle Scholar
Mesquita, RLB, Azevedo, RK, Abdallah, VD and Luque, JL (2011) Ectoparasites as numerical dominant species in parasite community of Trachelyopterus striatulus (Siluriformes: Auchenipteridae) from Guandu River, southeastern Brazil. Brazilian Journal of Biology 71, 623627.CrossRefGoogle ScholarPubMed
Mise, FT, Souza, F, Pagotto, JPA and Goulart, E (2015) Intraspecific ecomorphological variations in Poecilia reticulata (Actinopterygii, Cyprinodontiformes): comparing populations of distinct environments. Iheringia, Série Zoologia 105, 217222.CrossRefGoogle Scholar
Mohammed, RS, King, SD, Bentzen, P, Marcogliese, D, van Oosterhout, C and Lighten, J (2020) Parasite diversity and ecology in a model species, the guppy (Poecilia reticulata) in Trinidad. Royal Society Open Science 7, 191112.CrossRefGoogle Scholar
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 7582.CrossRefGoogle ScholarPubMed
Nasir, P, Hamana, SL and Díaz, MT (1969) Studies on freshwater larval trematodes. XXIII. Additional five new species of Venezuelan cercariae. Proceedings of the Helminthological Society of Washington 36, 231239.Google Scholar
Neal, JW, Noble, RL, Olmeda, ML and Lilyestrom, CG (2004) Management of tropical freshwater fisheries with stocking: the past, present, and future of propagated fishes in Puerto Rico. In Nickum, MJ, Mazik, PM, Nickum, JG and MacKinlay, DD (eds), Propagated Fishes in Resource Management. Bethesda, Maryland: American Fisheries Society Symposium, vol. 44, pp. 197206.Google Scholar
Neal, JW, Lilyestrom, CG and Kwak, TJ (2009) Factors influencing tropical island freshwater fishes: species, status, and management implications in Puerto Rico. Fisheries 34, 546554.CrossRefGoogle Scholar
Neves, LR, Pereira, FB, Tavares-Dias, M and Luque, JL (2013) Seasonal influence on the parasite fauna of a wild population of Astronotus ocellatus (Perciformes: Cichlidae) from the Brazilian Amazon. Journal of Parasitology 99, 718721.CrossRefGoogle ScholarPubMed
Nguyen, TC, Li, YC, Makouloutou, P, Jimenez, LA and Sato, H (2012) Posthodiplostomum sp. metacercariae in the trunk muscle of northern snakeheads (Channa argus) from the Fushinogawa River, Yamaguchi, Japan. Journal of Veterinary Medical Science 74, 13671372.CrossRefGoogle ScholarPubMed
Ondračková, M, Dávidová, M, Gelnar, M and Jurajda, P (2006) Susceptibility of Prussian carp infected by metacercariae of Posthodiplostomum cuticola (v. Nordmann, 1832) to fish predation. Ecological Research 21, 526529.CrossRefGoogle Scholar
Ondrejicka, DA, Locke, SA, Morey, K, Borisenko, AV and Hanner, RH (2014) Status and prospects of DNA barcoding in medically important parasites and vectors. Trends in Parasitology 30, 582591.CrossRefGoogle ScholarPubMed
Osorio-Sarabia, D, Pérez-Ponce de León, G and García-Marquez, LJ (1986) Helmintos de peces en Pátzcuaro, Michoacán II: Estudio histopatológico de la lesión causada por metacercarias de Posthodiplostomum minimum (Trematoda: Diplostomatidae) en el hígado de Chirostoma estor. Anales del Instituto de Biología Universidad Nacional Autónoma de México Serie Zoología 57, 247260.Google Scholar
Ostrowski de Núñez, M (1973) Sobre el ciclo biologico experimental de Posthodiplostomum nanum Dubois, 1937 (Trematoda, Diplostomidae). Physis 32, 121132.Google Scholar
Özer, A and Yilmaz Kirca, D (2015) Parasite fauna of the grey mullet Mugil cephalus L. 1758, and its relationship with some ecological factors in Lower Kızılırmak Delta located by the Black Sea, Turkey. Journal of Natural History 49, 933956.CrossRefGoogle Scholar
Palmieri, JR (1975) Host–parasite relationships and intraspecific variations in Posthodiplostomum minimum (Trematoda: Diplostomatidae). The Great Basin Naturalist 36, 334346.Google Scholar
Palmieri, JR (1977 a) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplostomatidae). II. Body measurements and tegument modifications. The Great Basin Naturalist 37, 129137.Google Scholar
Palmieri, JR (1977 b) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplotomatidae). III. Organs of attachment. The Great Basin Naturalist 37, 375382.Google Scholar
Palmieri, JR (1977 c) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplostomatidae). IV. Organs of reproduction (ovary and testes), vitelline gland and egg. The Great Basin Naturalist 37, 481488.Google Scholar
Pattengale, ND, Alipour, M, Bininda-Emonds, OR, Moret, BM and Stamatakis, A (2010) How many bootstrap replicates are necessary? Journal of Computational Biology 17, 337354.CrossRefGoogle ScholarPubMed
Perales Macedo, DMB, Díaz Pernett, SC, Díaz González, MG, Torres Nieves, GM, Santos Flores, CJ, Díaz Lameiro, AM and Locke, SA (2022) Autochthonous transmission of the Indomalayan parasite, Transversotrema patialense, in the Caribbean: molecular, morphological, and experimental evidence. Experimental Parasitology 242, 108368.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G, Sereno-Uribe, A, Pinacho-Pinacho, C and García-Varela, M (2022) Assessing the genetic diversity of the metacercariae of Posthodiplostomum minimum (Trematoda: Diplostomidae) in middle American freshwater fishes: one species or more? Parasitology 149, 239252.CrossRefGoogle ScholarPubMed
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369371.CrossRefGoogle Scholar
Radabaugh, DC (1980) Encystment site selection in the brain-inhabiting metacercariae of Ornithodiplostomum ptychocheilus (Trematoda: Strigeoidea). Journal of Parasitology 66, 183184.CrossRefGoogle Scholar
Rahel, FJ (2010) Homogenization, differentiation, and the widespread alteration of fish faunas. In Gido, KE and Jackson, DA (eds), Community Ecology of Stream Fishes: Concepts, Approaches, and Techniques. Vol. 73. Bethesda (Maryland): American Fisheries Society, pp. 311326.Google Scholar
Ratnasingham, S and Hebert, PDN (2007) BOLD: the barcode of life data system. Molecular Ecology Notes 7, 355364.CrossRefGoogle ScholarPubMed
Ratnasingham, S and Hebert, PDN (2013) A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8, e66213.CrossRefGoogle ScholarPubMed
Ritossa, L, Flores, V and Viozzi, G (2013) Life-cycle stages of a Posthodiplostomum species (Digenea: Diplostomidae) from Patagonia, Argentina. Journal of Parasitology 99, 777780.CrossRefGoogle ScholarPubMed
Rodríguez-Barreras, R, Zapata-Arroyo, C, Falcón, WL and Olmeda, ML (2020) An island invaded by exotics: a review of freshwater fish in Puerto Rico. Neotropical Biodiversity 6, 4259.CrossRefGoogle Scholar
Salgado-Maldonado, G, Mercado-Silva, N, Cabañas-Carranza, G, Caspeta-Mandujano, J, Aguilar-Aguilar, R and Iñiguez, RL (2004) Helminth parasites of freshwater fishes of the Ayuquila River, Sierra de Manantlán Biosphere Reserve, West Central Mexico. Comparative Parasitology 71, 6772.CrossRefGoogle Scholar
Salgado-Maldonado, G, Caspeta-Mandujano, JM, Martínez-Ramírez, E, Montoya-Mendoza, J and Mendoza-Franco, EF (2020) Diversity of helminth parasites of freshwater fish in the headwaters of the Coatzacoalcos River, in Oaxaca, Mexico. International Journal for Parasitology: Parasites and Wildlife 12, 142149.Google ScholarPubMed
Sandlund, OT, Daverdin, RH, Choudhury, A, Brooks, DR and Diserud, OH (2010) A survey of freshwater fishes and their macroparasites in the Guanacaste Conservation Area (ACG), Costa Rica. NINA Report 635, 45.Google Scholar
Sankurathri, CS and Holmes, JC (1976) Effects of thermal effluents on parasites and commensals of Physa gyrina Say (Mollusca: Gastropoda) and their interactions at Lake Wabamun, Alberta. Canadian Journal of Zoology 54, 17421753.CrossRefGoogle Scholar
Santos, GG, Oliveira, M, Neves, LR and Tavares-Dias, M (2018) Parasites community of Astronotus crassipinnis (Cichlidae), a fish from the Brazilian Amazon. Annals of Parasitology 64, 121128.Google Scholar
Sarabeev, V, Balbuena, JA and Morand, S (2017) The effects of host introduction on the relationships between species richness and aggregation in helminth communities of two species of grey mullets (Teleostei: Mugilidae). Vie et Milieu – Life and Environment 67, 121130.Google Scholar
Schories, S, Meyer, MK and Schartl, M (2009) Description of Poecilia (Acanthophacelus) obscura n. sp., (Teleostei: Poeciliidae), a new guppy species from western Trinidad, with remarks on P. wingei and the status of the Endler's guppy. Zootaxa 2266, 3550.CrossRefGoogle Scholar
Sowersby, WG (2017) Behavioural and Morphological Variation in Neotropical Cichlid Fishes (Thesis). Monash University, Melbourne, Australia.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313.CrossRefGoogle ScholarPubMed
Sterba, G (1967) Freshwater Fishes of the World, 3rd Edn. London: Pet Library Ltd.Google Scholar
Stoyanov, B, Georgieva, S, Pankov, P, Kudlai, O, Kostadinova, A and Georgiev, BB (2017) Morphology and molecules reveal the alien Posthodiplostomum centrarchi Hoffman, 1958 as the third species of Posthodiplostomum Dubois, 1936 (Digenea: Diplostomidae) in Europe. Systematic Parasitology 94, 120.CrossRefGoogle ScholarPubMed
Stoyanov, B, Mutafchiev, Y, Pankov, P and Georgiev, BB (2018) Helminth parasites in the alien Lepomis gibbosus (L.) (Centrarchidae) from the Lake Atanasovsko Wetlands, Bulgaria: survey of species and structure of helminth communities. Acta Zoologica Bulgarica 69, 555574.Google Scholar
Tavares-Dias, M and Oliveira, MSB (2017) Structure of parasites community in Chaetobranchopsis orbicularis (Cichlidae), a host from the Amazon River system in northern Brazil. Parasitology Research 116, 23132319.CrossRefGoogle ScholarPubMed
Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ and Kuris, AM (2003) Introduced species and their missing parasites. Nature 421, 628630.CrossRefGoogle ScholarPubMed
Travassos, L, Teixeira de Freitas, JF and Koh, A (1969) Trematodeos do Brasil. Memorias do Instituto Oswaldo Cruz 67, 8187.Google Scholar
Van Steenkiste, N, Locke, SA, Castelin, M, Marcogliese, DJ and Abbott, CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources 15, 945952.CrossRefGoogle ScholarPubMed
Veeravechsukij, N, Namchote, S, Neiber, MT, Glaubrecht, M and Krailas, D (2018) Exploring the evolutionary potential of parasites: larval stages of pathogen digenic trematodes in their thiarid snail host Tarebia granifera in Thailand. Zoosystematics and Evolution 94, 425.CrossRefGoogle Scholar
Velázquez-Urrieta, Y and Pérez-Ponce de León, G (2021) Morphological and molecular assessment of the diversity of trematode communities in freshwater gastropods and bivalves in Los Tuxtlas tropical rainforest. Journal of Helminthology 95, 116.CrossRefGoogle Scholar
Vilas, R, Criscione, CD and Blouin, MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 839846.CrossRefGoogle ScholarPubMed
Ward, RD, Zemlak, TS, Innes, BH, Last, PR and Hebert, PD (2005) DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 18471857.CrossRefGoogle ScholarPubMed
Wheeler, DL, Church, DM, Federhen, S, Lash, AE, Madden, TL, Pontius, JU, Schuler, GD, Schriml, LM, Sequeira, E, Tatusova, EA and Wagner, L (2003) Database resources of the National Center for Biotechnology. Nucleic Acids Research 31, 2833.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Díaz Pernett et al. supplementary material

Tables S1-S3

Download Díaz Pernett et al. supplementary material(PDF)
PDF 504 KB