Advertisement

Selected Wildlife Trematodes

  • Matthew G. BolekEmail author
  • Jillian T. Detwiler
  • Heather A. Stigge
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)

Abstract

The trematodes are a species-rich group of parasites, with some estimates suggesting that there are more than 24,000 species. However, recent interests on the biology of trematodes of wildlife indicate that the taxonomic status and nomenclature of many of the previous species descriptions of wildlife trematodes throughout the world are confusing and difficult to decipher. In this chapter, we review work on selected trematodes of amphibians, birds, mammals, and their snail intermediate hosts, in the hope of providing a tool kit on how to study trematodes of wildlife. We provide a brief introduction to each group of wildlife trematodes, followed by some examples of the challenges each group of trematodes has relative to the goal of their identification and understanding of their biology and interactions with their wildlife hosts.

Keywords

Trematodes Wildlife Amphibian parasites Bird and mammal parasites Cryptic species Life cycles 

References

  1. Adamson ML, Caira JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S85–S95PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alda P, Lounnas M, Vázquez AA, Ayaqui R, Calvopiña M, Celi-Erazo M, Dillon RT Jr, Jarne P, Loker ES, FCM P, Muzzio-Aroca J, Nárvaez AO, Noya O, Robles LM, Rodríguez-Hidalgo R, Uribe N, David P, Pointier JP, Hurtez-Boussès S (2018) A new multiplex PCR assay to distinguish among three cryptic Galba species, intermediate hosts of Fasciola hepatica. Vet Parasitol 251:101–105PubMedCrossRefPubMedCentralGoogle Scholar
  3. Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Hopcroft RR (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202PubMedCrossRefPubMedCentralGoogle Scholar
  4. Azuma N, Yamazaki T, Chiba S (2011) Mitochondrial and nuclear DNA analysis revealed a cryptic species and genetic introgression in Littorina sitkana (Mollusca, Gastropoda). Genetica 139:1399–1408Google Scholar
  5. Bargues MD, Vigo M, Horak P, Dvorak J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol 1:85–107CrossRefGoogle Scholar
  6. Bargues MD, Artigas P, Khoubbane M, Flores R, Glöer P, Rojas-García R, Ashrafi K, Falkner G, Mas-Coma S (2011) Lymnaea schirazensis, an overlooked snail distorting fascioliasis data: genotype, phenotype, ecology, worldwide spread, susceptibility, applicability. PLoS One 6:e24567PubMedPubMedCentralCrossRefGoogle Scholar
  7. Beaver PC (1937) Experimental studies on Echinostoma revolutum (Froelich), a fluke from birds and mammals. Biol Monogr 15:1–96Google Scholar
  8. Belden LK, Wojdak JM (2011) The combined influence of trematode parasites and predatory salamanders on wood frog (Rana sylvatica) tadpoles. Oecologia 166:1077–1086PubMedCrossRefPubMedCentralGoogle Scholar
  9. Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ (2016) Molecular approaches to trematode systematics: “best practice” and implications for future study. Syst Parasitol 93:295–306PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bolek MG (2006) The role of arthropod second intermediate hosts as avenues for and constraints on the transmission of frog lung flukes (Digenea: Haematoloechidae). PhD thesis, University of Nebraska–Lincoln, LincolnGoogle Scholar
  11. Bolek MG, Coggins JR (2003) Helminth community structure of sympatric eastern American toad, Bufo americanus americanus, northern leopard frog, Rana pipiens, and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin. J Parasitol 89:673–680PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bolek MG, Janovy J Jr (2007a) Small frogs get their worms first: The role of non-odonate arthropods in the recruitment of Haematoloechus coloradensis and Haematoloechus complexus in newly metamorphosed northern leopard frogs, Rana pipiens, and Woodhouse’s toads, Bufo woodhousii. J Parasitol 93:300–312PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bolek MG, Janovy J Jr (2007b) Evolutionary avenues for and constraints on the transmission of frog lung flukes (Haematoloechus spp.) in dragonfly second intermediate hosts. J Parasitol 93:593–607PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bolek MG, Janovy J Jr (2008) Alternative life cycle strategies of Megalodiscus temperatus in tadpoles and metamorphosed anurans. Parasite 15:396–401PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bolek MG, Snyder SD, Janovy J Jr (2009a) Alternative life-cycle strategies and colonization of young anurans by Gorgoderina attenuata in Nebraska. J Parasitol 95:604–615PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bolek MG, Snyder SD, Janovy J Jr (2009b) Redescription of the bladder fluke Gorgoderina attenuata from the northern leopard frog, Rana pipiens. J Parasitol 95:665–668Google Scholar
  17. Bolek MG, Tracy HR, Janovy J Jr (2010) The role of damselflies (Odonata: Zygoptera) as paratenic hosts in the transmission of Halipegus eccentricus (Digenea: Hemiuridae) to anurans. J Parasitol 96:724–735PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bolek MG, Stigge HA, Gustafson KD (2016) The iron wheel of parasite life cycles: then and now. In: Janovy J Jr, Esch GW (eds) A century of parasitology: discoveries, ideas and lessons learned by scientists who published in the Journal of Parasitology, 1914–2014. Wiley, London, pp 131–147CrossRefGoogle Scholar
  19. Bourgat R, Kulo SD (1979) Cycle biologique d’ Haematoloechus johnsoni Bourgat, 1977, (Trèmatode) parasite pulmonaire de Dicroglossus occipitalis (Günther, 1858) (Amphibien, Anoure) au Togo. Rev Suisse Zool 86:467–472CrossRefGoogle Scholar
  20. Brooks DL (1976) Parasites of amphibians of the Great Plains: Part 2. Platyhelminths of amphibians in Nebraska. Bull Univ Nebraska State Mus 10:65–92Google Scholar
  21. Brooks DR, León-Règagnon V, McLennan DA, Zelmer D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87:S76–S85PubMedCrossRefPubMedCentralGoogle Scholar
  22. Burch JB (1968) Erinna newcombi of Hawaii and Limnaea onychia of Japan. Malacol Rev 1:15–30Google Scholar
  23. Chiba S, Davison A (2008) Anatomical and molecular studies reveal several species of the endemic genus Mandarina (Pulmonata: Helicoidea) in the Ogasawara Islands. J Moll Stud 74:373–382CrossRefGoogle Scholar
  24. Chibwana FD, Nkwengulila G, Locke SA, McLaughlin JD, Marcogliese DJ (2015) Completion of the life cycle of Tylodelphys mashonense (Sudarikov, 1971) (Digenea: Diplostomidae) with DNA barcodes and rDNA sequences. Parasitol Res 114:3675–3682PubMedCrossRefPubMedCentralGoogle Scholar
  25. Choudhury A, García-Varela M, Pérez-Ponce de León G (2016) Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far? J Helminthol 91:174–196PubMedCrossRefPubMedCentralGoogle Scholar
  26. Collado GA (2017) Unraveling cryptic invasion of a freshwater snail in Chile based on molecular and morphological data. Biodivers Conserv 26:567–578CrossRefGoogle Scholar
  27. Collado GA, Valladares MA, Mendez MA (2013) Hidden diversity in spring snails from the Andean Altiplano, the second highest plateau on Earth, and the Atacama Desert, the driest place in the world. Zool Stud 52:50CrossRefGoogle Scholar
  28. Collado GA, Valladares MA, Mendez MA (2016) Unravelling cryptic species of freshwater snails (Caenogastropoda, Truncatelloidea) in the Loa River basin, Atacama Desert. Syst Biodivers 14:417–429CrossRefGoogle Scholar
  29. Combes C (1968) Biologie, écologie des cycles et biogeography de digénes et monogénes d’amphibiens dans l’est des Pyrénéés. Ann Mus Natl Hist Nat 51:1–195Google Scholar
  30. Cort WW (1912) North American frog bladder flukes. Trans Am Microsc Soc 31:151–168CrossRefGoogle Scholar
  31. Cort WW (1915) North American frog lung flukes. Trans Am Microsc Soc 34:203–243CrossRefGoogle Scholar
  32. Couceiro L, Lopez L, Sotka EE, Ruiz JM (2012) Molecular data delineate cryptic Nassarius species and characterize spatial genetic structure of N. nitidus. J Mar Biol Assoc U K 92:1175–1182CrossRefGoogle Scholar
  33. Crawford WW (1940) The life history of a gorgoderid trematode, presumably of the genus Phyllodistomum. J Parasitol 26:S38Google Scholar
  34. Criscione F, Kohler F (2015) On the land snail Damochlora Iredale, 1938 and its cryptic sibling Nannochlora n. gen. (Stylommatophora: Camaenidae), each endemic to an island in the Western Australian Kimberley. Molluscan Res 35:275–286CrossRefGoogle Scholar
  35. Cutmore SC, Bennett MB, Cribb TH (2010) Staphylorchis cymatodes (Gorgoderidae Anaporrhutinae) from carcharhiniform, orectolobiform and myliobatiform elasmobranchs of Australasia: low host specificity, wide distribution and morphological plasticity. Parasitol Int 59:579–586PubMedCrossRefPubMedCentralGoogle Scholar
  36. Dale PJ (1967) The life history of Gorgodera australiensis Johnston,1912. Tuatara 15:89–97Google Scholar
  37. De Biasi JB, Tomas ARG, Hilsdorf AWS (2016) Molecular evidence of two cryptic species of Stramonita (Mollusca, Muricidae) in the southeastern Atlantic coast of Brazil. Genet Mol Biol 39:392–397PubMedPubMedCentralCrossRefGoogle Scholar
  38. de Lacerda LEM, Richau CS, Amaral CRL, da Silva DA, Carvalho EF, Barbosa dos Santos S (2015) Ferrissia fragilis (Tryon, 1863): a freshwater snail cryptic invader in Brazil revealed by morphological and molecular data. Aquat Invasions 10:157–168CrossRefGoogle Scholar
  39. Dennis AB, Hellberg ME (2010) Ecological partitioning among parapatric cryptic species. Mol Ecol 19:3206–3225PubMedCrossRefPubMedCentralGoogle Scholar
  40. Depraz A, Hausser J, Pfenninger M (2009) A species delimitation approach in the Trochulus sericeus/hispidus complex reveals two cryptic species within a sharp contact zone. BMC Evol Biol 9:171PubMedPubMedCentralCrossRefGoogle Scholar
  41. Detwiler JT, Bos DH, Minchella DJ (2010) Revealing the secret lives of cryptic species: Examining the phylogenetic relationships of echinostome parasites in North America. Mol Phylogenet Evol 55:611–620PubMedCrossRefPubMedCentralGoogle Scholar
  42. Detwiler JT, Zajac AM, Minchella DJ, Belden LK (2012) Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. J Parasitol 98:1148–1155PubMedCrossRefPubMedCentralGoogle Scholar
  43. Dillon TD, Frankis RC (2004) High levels of mitochondrial DNA sequence divergence in isolated populations of freshwater snails of the genus Goniobasis Lea, 1862. Am Malacol Bull 19:69–77Google Scholar
  44. Dollfus R (1961) Station expérimentale de parasitologie de Richelieu (Indre-et-Loire). Contribution à la faune parasitaire régionale. Ann Parasitol Hum Comp 3:169–451Google Scholar
  45. Donald KM, Kennedy M, Poulin R, Spencer HG (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int J Parasitol 34:557–568PubMedCrossRefPubMedCentralGoogle Scholar
  46. Dronen N (1975) The life cycle of Haematoloechus coloradensis Cort, 1915 (Digenea: Plagiorchiidae), with emphasis on host susceptibility to infection. J Parasitol 61:657–660PubMedCrossRefPubMedCentralGoogle Scholar
  47. Dronen NO (2009) Re-evaluation of the species composition of Bashkirovtrema Skrjabin, (1944) (Digenea: Echinostomatidae), with the description of two new species of this genus and the proposal of Kostadinovatrema novaeguiniense n. g., n. sp. Syst Parasitol 74:169–185PubMedCrossRefPubMedCentralGoogle Scholar
  48. Durand P, Pointier JP, Escoubeyrou K, Arenas JA, Yong M, Amarista M, Bargues MD, Mas-Coma S, Renaud F (2002) Occurrence of a sibling species complex within neotropical lymnaeids, snail intermediate hosts of fascioliasis. Acta Trop 83:233–240PubMedCrossRefPubMedCentralGoogle Scholar
  49. El Ayari T, El Menif NT, Saavedra C, Cordero D, Viard F, Bierne N (2017) Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion. Ecol Evol 7:9016–9026PubMedPubMedCentralCrossRefGoogle Scholar
  50. Elejalde MA, Madeira MJ, Muñoz B, Arrébola JR, Gómez-Moliner BJ (2008) Mitochondrial DNA diversity and taxa delineation in the land snails of the Iberus gualtieranus (Pulmonata, Helicidae) complex. Zool J Linn Soc 154:722–737CrossRefGoogle Scholar
  51. Emberton KC (1995) Cryptic, genetically extremely divergent, polytypic, convergent, and polymorphic taxa in Madagascan Tropidophora (Gastropoda, Pomatiasidae). Biol J Linn Soc 55:183–208Google Scholar
  52. Faltynková A, Našincová V, Kablásková L (2007) Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14:39–51PubMedCrossRefPubMedCentralGoogle Scholar
  53. Faltynková A, Našincová V, Kablásková L (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey and key to their identification. Syst Parasitol 69:155–178PubMedCrossRefPubMedCentralGoogle Scholar
  54. Fried B, Pane PL, Reddy A (1997) Experimental infection of Rana pipiens tadpoles with Echinostoma trivolvis cercariae. Parasitol Res 83:666–669PubMedCrossRefPubMedCentralGoogle Scholar
  55. Georgieva S, Selbach C, Faltynková A, Soldánová M, Sures B, Skírnisson K, Kostadinova A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors 6:64PubMedPubMedCentralCrossRefGoogle Scholar
  56. Gibson DI, Bray RA (1994) The evolutionary expansion and host–parasite relationships of the Digenea. Int J Parasitol 24:1213–1226PubMedPubMedCentralCrossRefGoogle Scholar
  57. Gittenberger A, Gittenberger E (2011) Cryptic, adaptive radiation of endoparasitic snails: sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Organ Divers Evol 11:21–41CrossRefGoogle Scholar
  58. Goater TM, Browne CL, Esch GW (1990a) On the life life history and functional morphology of Halipegus occidualis (Trematoda: Hemiuridae), with emphasis on the cystophorous cercaria stage. Int J Parasitol 20:923–934CrossRefGoogle Scholar
  59. Goater TM, Mulvey M, Esch GW (1990b) Electrophoretic differentiation of two Halipegus congeners in a natural amphibian population: comments on genetic diversity in helminth parasites. J Parasitol 76:431–434PubMedCrossRefPubMedCentralGoogle Scholar
  60. Goodchild CG (1943) The life-history of Phyllodistomum solidum Rankin, 1937, with observations on the morphology, development and taxonomy of the Gorgoderinae (Trematoda). Biol Bull 84:59–86CrossRefGoogle Scholar
  61. Goodchild CG (1948) Additional observations on the life history of Gorgodera amplicava Looss, 1899 (Trematoda: Gorgoderidae). J Parasitol 34:407–427PubMedCrossRefPubMedCentralGoogle Scholar
  62. Goodchild CG (1950) Establishment and pathology of gorgoderid infections in anuran kidneys. J Parasitol 36:439–446PubMedCrossRefPubMedCentralGoogle Scholar
  63. Gordy MA, Kish L, Tarrabain M, Hanington PC (2016) A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada. Parasitol Res 115:3867–3880PubMedCrossRefPubMedCentralGoogle Scholar
  64. Grabda-Kazubska B (1960) Life cycle of Haematoloechus similis (Looss, 1899) (Trematoda: Plagiorchiidae). Acta Parasitol 8:357–367Google Scholar
  65. Gustafson KD, Bolek MG (2016) Effects of trematode parasitism on the shell morphology of snails from flow and nonflow environments. J Morphol 277:316–325PubMedCrossRefPubMedCentralGoogle Scholar
  66. Gustafson KD, Kensigner BJ, Bolek MG, Luttbeg B (2014) Distinct snail (Physa) morphotypes from different habitats converge in shell shape and size under common garden conditions. Evol Ecol Res 16:77–89Google Scholar
  67. Haase M, Zielske S (2015) Five new cryptic freshwater gastropod species from New Caledonia (Caenogastropoda, Truncatelloidea, Tateidae). Zookeys 523:63–87CrossRefGoogle Scholar
  68. Harwood P (1932) The helminths parasitic in the Amphibia and Reptilia in Houston, Texas, and vicinity. Proc US Natl Mus 81:1–71CrossRefGoogle Scholar
  69. Holland MP (2010) Echinostome metacercariae cyst elimination in Rana clamitans (Green Frog) tadpoles is age-dependent. J Parasitol 95:281–285CrossRefGoogle Scholar
  70. Holland MP, Skelly DK, Kashgarian M, Bolden SR, Harrison LM, Cappello M (2007) Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. J Zool 271:455–462CrossRefGoogle Scholar
  71. Ingles LG (1932) Four new species of Haematoloechus (Trematoda) from Rana aurora draytoni from California. Univ Calif Publ Zool 37:189–202Google Scholar
  72. Ingles LG (1936) Worm parasites of California Amphibia. Trans Am Microsc Soc 55:73–92CrossRefGoogle Scholar
  73. Irwin MS (1929) A new lung fluke from Rana clamitans Latreille. Trans Am Microsc Soc 48:74–79CrossRefGoogle Scholar
  74. Johnson PTJ, Buller ID (2011) Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. Ecology 92:535–541PubMedCrossRefPubMedCentralGoogle Scholar
  75. Johnson PTJ, McKenzie VJ (2008) Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In: Fried B, Toledo R (eds) The biology of echinostomes, from the molecule to the community. Springer, Berlin, pp 249–280Google Scholar
  76. Johnson SB, Waren A, Tunnicliffe V, Van Dover C, Wheat CG, Schultz TF, Vrijenhoek RC (2015) Molecular taxonomy and naming of five cryptic species of Alviniconcha snails (Gastropoda: Abyssochrysoidea) from hydrothermal vents. Syst Biodivers 13:278–295CrossRefGoogle Scholar
  77. Kanev I, Sorensen R, Sterner M (1998) The identification and characteristics of Echinoparyphium rubrum (Cort, 1914) comb. New (Trematoda, Echinostomatidae) based on experimental evidence of the life cycle. Acta Parasitol 43:181–188Google Scholar
  78. Kanev I, Sorensen R, Radev V (2008) Identification problems with species in the Echinoparyphium recurvatum complex from physid snails in the USA. Parasitol Res 103:963–965PubMedCrossRefPubMedCentralGoogle Scholar
  79. Kanev I, Fried B, Radev B (2009) Collar spine models in the genus Echinostoma (Trematoda: Echinostomatidae). Parasitol Res 105:921–927PubMedCrossRefPubMedCentralGoogle Scholar
  80. Kasl EL, Font WF, Criscione CD (2018) Resolving evolutionary changes in parasite life cycle complexity: molecular phylogeny of the trematode genus Alloglossidium indicates more than one origin of precociousness. Mol Phylogenet Evol 126:371–381PubMedCrossRefPubMedCentralGoogle Scholar
  81. Kennedy MJ (1980a) Host-induced variations in Haematoloechus buttensis (Trematoda: Haematoloechidae). Can J Zool 58:427–442CrossRefGoogle Scholar
  82. Kennedy MJ (1980b) Geographical variation in some representatives of Haematoloechus Looss, 1899 (Trematoda: Haematoloechidae) from Canada and the United States. Parasitol Res 58:1151–1167Google Scholar
  83. Kennedy MJ (1981) A revision of the genus Haematoloechus Looss, 1899 (Trematoda: Haematoloechidae) from Canada and the United States. Parasitol Res 59:1836–1846Google Scholar
  84. Koehler F, Burghardt I (2016) Cryptic diversity in a widespread land snail: revision of the genus Xanthomelon Martens, 1860 from the Australian Monsoon Tropics (Pulmonata, Camaenidae). Zool Scr 45:127–144CrossRefGoogle Scholar
  85. Koehler F, Johnson MS (2012) Species limits in molecular phylogenies: a cautionary tale from Australian land snails (Camaenidae: Amplirhagada Iredale, 1933). Zool J Linn Soc 165:337–362CrossRefGoogle Scholar
  86. Koprivnikar J, Gibson CH, Redfern JC (2002) Infectious personalities: behavioural syndromes and disease risk in larval amphibians. Proc Roy Soc B Biol Sci 279:1544–1550CrossRefGoogle Scholar
  87. Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PTJ (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9:342–360PubMedCrossRefPubMedCentralGoogle Scholar
  88. Kostadinova A (2005) Family Echinostomatidae Looss, 1899. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI Publishing, Wallingford, pp 9–64CrossRefGoogle Scholar
  89. Kraus TJ, Brant SV, Adema CM (2014) Characterization of trematode cercariae from Physella acuta in the Middle Rio Grande. Comp Parasitol 81:105–109CrossRefGoogle Scholar
  90. Krull WH (1930) The life history of two North American frog lung flukes. J Parasitol 16:207–212CrossRefGoogle Scholar
  91. Krull WH (1931) Life history studies on two frog lung flukes, Pneumonoeces medioplexus and Pneumobites parviplexus. Trans Am Microsc Soc 50:215–277CrossRefGoogle Scholar
  92. Krull WH (1932) Studies on the life history of Haematoloechus longiplexus (Stafford). Zool Anz 99:231–239Google Scholar
  93. Krull WH (1933) Studies on the life history of a frog lung fluke, Haematoloechus complexus (Seely, 1906) Krull, n. comb. Z Parasitenkd 6:192–206CrossRefGoogle Scholar
  94. Krull WH (1934) Some additional notes on the life history of a frog lung fluke, Haematoloechus complexus (Seely, 1906) Krull. Trans Am Microsc Soc 53:196CrossRefGoogle Scholar
  95. Krull HW (1935a) Studies on the life history of a frog bladder fluke, Gorgodera amplicava Looss, 1899. Papers of the Michigan Academy of Science, Arts and Letters, vol 20, pp 697–710Google Scholar
  96. Krull HW (1935b) Studies on the life history of Halipegus occiualis Stafford, 1905. Am Midl Nat J 16:129–143CrossRefGoogle Scholar
  97. Krull HW (1952) Studies on the biology of Dicrocoelium dendriticum (Rudolphi, 1819) Looss, 1899 (Trematoda: Dicrocoeliidae), including its relation to the intermediate host, Cionella lubrica (Müller). VII. The second intermediate host of Dicrocoelium dendriticum. Cornell Vet 42:603–604PubMedPubMedCentralGoogle Scholar
  98. Lee T, Kim JJ, Hong HC, Burch JB, Foighil DO (2006) Crossing the Continental Divide: the Columbia drainage species Juga hemphilli (Henderson, 1935) is a cryptic member of the eastern North American genus Elimia (Cerithioidea: Pleuroceridae). J Moll Stud 72:314–317CrossRefGoogle Scholar
  99. León-Règagnon V (2010) Evidence of new species of Haematoloechus (Platyhelminthes: Digenea) using partial cox1 sequences. Mitochon DNA 21:S12–S17CrossRefGoogle Scholar
  100. León-Règagnon V, Brooks DR (2003) Molecular phylogeny of Haematoloechus Looss, 1899 (Digenea: Plagiorchiidae), with emphasis on North American species. J Parasitol 89:1206–1211PubMedCrossRefPubMedCentralGoogle Scholar
  101. León-Règagnon V, Paredes-Calderón EL (2002) Haematoloechus danbrooksi n. sp. (Digenea: Plagiorchioidea) from Rana vaillanti from Los Tuxtlas, Veracruz, Mexico. J Parasitol 88:1215–1221PubMedCrossRefPubMedCentralGoogle Scholar
  102. León-Règagnon V, Romero-Mayén RA (2013) A new species of Halipegus Looss, 1899 (Trematoda: Derogenidae) parasitic of Rana psilonota Webb, 2001 of Atenquique, Jalisco, Mexico. J Parasitol 99:1067–1070PubMedCrossRefPubMedCentralGoogle Scholar
  103. León-Règagnon V, Topan J (2018) Taxonomic revision of species of Haematoloechus Looss, 1899 (Digenea: Plagiorchioidea), with molecular phylogenetic analysis and the description of three new species from Mexico. Zootaxa 4526:251–302PubMedCrossRefPubMedCentralGoogle Scholar
  104. León-Règagnon V, Brooks DR, Pérez-Ponce de León G (1999) Differentiation of Mexican species of Haematoloechus Loss, 1989 (Digenea: Plagiorchiformes): molecular and morphological evidence. J Parasitol 85:935–946PubMedCrossRefPubMedCentralGoogle Scholar
  105. León-Règagnon V, Brooks DR, Zelmer DA (2001) Morphological and molecular description of Haematoloechus meridionalis n. sp. (Digenea: Plagiorchioidea: Haematoloechidae) from Rana vaillanti Brocchi of Guanacaste, Costa Rica. J Parasitol 87:1423–1427PubMedCrossRefPubMedCentralGoogle Scholar
  106. León-Règagnon V, Guillén-Hernández S, Arizmendi-Espinosa MA (2005) Intraspecific variation of Haematoloechus floedae Harwood, 1932 (Digenea: Plagiorchiidae), from Rana spp. in North and Central America. J Parasitol 91:915–921PubMedCrossRefPubMedCentralGoogle Scholar
  107. Leung TLF, Donald KM, Keeney DB, Koehler AV, Peoples RC, Poulin R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles, and DNA barcodes. N Z J Mar Freshw Res 43:857–865CrossRefGoogle Scholar
  108. Locke SA, McLaughlin DJ, 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. Mol Ecol 19:2813–2827PubMedCrossRefPubMedCentralGoogle Scholar
  109. Looss A (1899) Weitere beiträge zur kenntnis der trematodenfauna Aegyptens, zugleich versuch einer natürlichen gliederung des genus Distomum Retzius. Zool Jahr Abteil Syst Oekol Geogr Tiere 12:521–784Google Scholar
  110. Looss A (1902) Ueber neue und bekannte Trematoden aus Seeschildkriten. Zool Jahrb Syst 16:411–891CrossRefGoogle Scholar
  111. Macher JN, Weiss M, Beermann AJ, Leese BJ (2016) Cryptic diversity and population structure at small scales: the freshwater snail Ancylus (Planorbidae, Pulmonata) in the Montseny mountain range. Ann Limnol Int J Limnol 52:387–399CrossRefGoogle Scholar
  112. Macy RW, Cook WA, Demott WR (1960) Studies on the life cycle of Halipegus occidualis Stafford, 1905 (Trematoda: Hemiuridae). Northwest Sci 34:1–17Google Scholar
  113. Madhavi R, Bray R (2018) Digenetic Trematodes of Indian Marine Fishes. Springer, DordrechtCrossRefGoogle Scholar
  114. Manter HW (1938) A collection of trematodes from Florida Amphibia. Trans Am Microsc Soc 57:26–37CrossRefGoogle Scholar
  115. Marzouk Z, Aurelle D, Said K, Chenuil A (2017) Cryptic lineages and high population genetic structure in the exploited marine snail Hexaplex trunculus (Gastropoda: Muricidae). Biol J Linn Soc 122:411–428CrossRefGoogle Scholar
  116. Mata-López R (2006) A new gorgoderid species of the urinary bladder of Rana zweifeli from Michoacán, Mexico. Rev Mex Biodivers 77:191–198Google Scholar
  117. Mata-López R, León-Règagnon V (2005) Gorgoderina festoni n. sp. (Digenea: Gorgoderidae) in anurans (Amphibia) from México. Syst Parasitol 62:185–190PubMedCrossRefPubMedCentralGoogle Scholar
  118. Mata-López R, León-Règagnon V (2006) Comparative study of the tegumental surface of several species of Gorgoderina Looss, 1902 (Digenea: Gorgoderidae), as revealed by scanning electron microscopy. Comp Parasitol 73:24–34CrossRefGoogle Scholar
  119. Mata-López R, García-Prieto L, León-Régagnon V (2002) Infracomunidades de helmintos parásitos de Ambystoma lermaensis (Caudata: Ambystomatidae) en Lerma, México. Rev Biol Trop 50:303–307PubMedPubMedCentralGoogle Scholar
  120. Mata-López R, León-Règagnon V, Brooks DR (2005) Species of Gorgoderina (Digenea: Gorgoderidae) in Rana vaillanti and Rana cf. forreri (Anura: Ranidae) from Guanacaste, Costa Rica, including a description of a new species. J Parasitol 91:403–410PubMedCrossRefPubMedCentralGoogle Scholar
  121. McAlpine DF (2006) Halipegus occidualis Krull, 1935 and Halipegus eccentricus Thomas, 1939 (Digenea, Hemiuridae): proposed conservation of the specific names. Bull Zool Nomencl 63:12–16Google Scholar
  122. McAlpine DF, Burt MD (1998) Taxonomic status of Halipegus spp. (Digenea: Derogenidae) parasitic in the mouth and eustachian tubes of North American and Mexican amphibians. J Helmithol Soc Washington 65:10–15Google Scholar
  123. Modica MV, Colangelo P, Hallgass A, Barco A, Oliverio M (2016) Cryptic diversity in a chirally variable land snail. Ital J Zool 83:351–363CrossRefGoogle Scholar
  124. Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, 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. Mol Ecol Resour 1:S75–S82CrossRefGoogle Scholar
  125. Nantarat N, Wade CM, Jeratthitikul E, Sutcharit C, Panha S (2014) Molecular evidence for cryptic speciation in the Cyclophorus fulguratus (Pfeiffer, 1854) species complex (Caenogastropoda: Cyclophoridae) with description of new species. PLoS One 9:e109785PubMedPubMedCentralCrossRefGoogle Scholar
  126. Nuñez JJ, Vejar-Pardo A, Guzman BE, Barriga EH, Galindo CS (2012) Phylogenetic and mixed Yule-coalescent analyses reveal cryptic lineages within two South American marine snails of the genus Crepipatella (Gastropoda: Calyptraeidae). Invert Biol 131:301–311CrossRefGoogle Scholar
  127. Odening K (1958) Zur systematik von Haematoloechus (Trematoda, Plagiorchiidae). Mitteil Zool Mus Berlin 34:63–108CrossRefGoogle Scholar
  128. Olson PD, Tkach VV (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Adv Parasitol 60:165–243PubMedPubMedCentralCrossRefGoogle Scholar
  129. Patel S, Schell T, Eifert C, Feldmeyer B, Pfenninger M (2015) Characterizing a hybrid zone between a cryptic species pair of freshwater snails. Mol Ecol 24:643–655PubMedCrossRefPubMedCentralGoogle Scholar
  130. Pérez-Ponce de León G, Nadler SA (2010) What we don’t recognize can hurt us: a plea for awareness about cryptic species. J Parasitol 96:453–464CrossRefGoogle Scholar
  131. Pérez-Ponce de León G, Poulin R (2018) An updated look at the uneven distribution of cryptic diversity among parasitic helminths. J Helminthol 92:197–202PubMedCrossRefPubMedCentralGoogle Scholar
  132. Pérez-Ponce de León G, García-Varela M, Pinacho-Pinacho CD, Sereno-Uribe AL, Poulin R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143:1773–1789PubMedCrossRefPubMedCentralGoogle Scholar
  133. Pienkowska JR, Manganelli G, Giusti F, Hallgass A, Lesicki A (2018) Exploring Monacha cantiana (Montagu, 1803) phylogeography: cryptic lineages and new insights into the origin of the English populations (Eupulmonata, Stylommatophora, Hygromiidae). Zookeys 765:1–41CrossRefGoogle Scholar
  134. Poulin R (2000) The diversity of parasites. Q Rev Biol 75:277–293PubMedCrossRefPubMedCentralGoogle Scholar
  135. Poulin R (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biol Lett 7:241–244PubMedCrossRefPubMedCentralGoogle Scholar
  136. Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18:176–183PubMedCrossRefPubMedCentralGoogle Scholar
  137. Poulin R, Leung TLF (2010) Taxonomic resolution in parasite community studies: are things getting worse? Parasitology 137(13):1967–1973PubMedCrossRefPubMedCentralGoogle Scholar
  138. Prasankok P, Tongkerd P, Sutcharit C, Sutcharitb C, Panhab S (2011) Genetic divergence in the snorkel snail, Rhiostoma housei, a species complex in Thailand (Caenogastropoda: Cyclophoridae). Biochem Syst Ecol 39:834–840CrossRefGoogle Scholar
  139. Pratt HS (1903) Descriptions of four distomes. In: Parker GH (ed) Mark Anniversary Volume to Edward Lawrence Mark. Henry Holt and Company, New York, pp 23–38Google Scholar
  140. Prévot V, Backeljau T, Jordaens K (2015) Morphometric evaluation of DNA-based cryptic taxa in the terrestrial decollate snail genus Rumina. J Moll Stud 81:223–232CrossRefGoogle Scholar
  141. Prokopič J, Křivanec K (1974) Trematodes of the genus Haematoloechus Looss, and their variability. Helminthology 15:779–802Google Scholar
  142. Prudhoe SOBE, Bray RA (1982) Platyhelminth parasites of the amphibia. British Museum (Natural History), OxfordGoogle Scholar
  143. Puillandre N, Cruaud C, Kantor YI (2010) Cryptic species in Gemmuloborsonia (Gastropoda: Conoidea). J Moll Stud 76:11–23CrossRefGoogle Scholar
  144. Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91:1900–1907PubMedCrossRefPubMedCentralGoogle Scholar
  145. Rama Rao S, Liew TS, Yow YY, Ratnayeke S (2018) Cryptic diversity: two morphologically similar species of invasive apple snail in Peninsular Malaysia. PLoS One 13:e0196582PubMedPubMedCentralCrossRefGoogle Scholar
  146. Rankin JS (1939) The life cycle of the frog bladder fluke, Gorgoderina attenuata Stafford, 1902 (Trematoda: Gorgoderidae). Am Midl Nat 21:476–488CrossRefGoogle Scholar
  147. Rankin JS (1944) A review of the trematode genus Halipegus Loss, 1899, with an account of the life history of H. amherstensis n. s. Trans Am Microsc Soc 63:149–164CrossRefGoogle Scholar
  148. Razkin O, Sonet G, Breugelmans K, Madeira MJ, Gómez-Moliner BJ, Backeljau T (2016) Species limits, interspecific hybridization and phylogeny in the cryptic land snail complex Pyramidula: the power of RADseq data. Mol Phylogenet Evol 101:267–278PubMedCrossRefPubMedCentralGoogle Scholar
  149. Razkin O, Gomez-Moliner BJ, Vardinoyannis K, Martínez-Ortí A, Madeira MJ (2017) Species delimitation for cryptic species complexes: case study of Pyramidula (Gastropoda, Pulmonata). Zool Scr 46:55–72CrossRefGoogle Scholar
  150. Rhoden HR, Bolek MG (2012) Helminth and leech community structure in tadpoles and caudatan larvae of two amphibian species from western Nebraska. J Parasitol 98:236–244PubMedCrossRefPubMedCentralGoogle Scholar
  151. Rosenberg G (2014) A new critical estimate of named species-level diversity of the recent Mollusca. Am Malacol Bull 32:308–322CrossRefGoogle Scholar
  152. Routtu J, Grunberg D, Izhar R, Dagan Y, Guttel Y, Ucko M, Ben-Ami F (2014) Selective and universal primers for trematode barcoding in freshwater snails. Parasitol Res 113:2535–2540PubMedCrossRefGoogle Scholar
  153. Rudolphi CA (1819) Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini, BerlinCrossRefGoogle Scholar
  154. Rundell RJ (2008) Cryptic diversity, molecular phylogeny and biogeography of the rock- and leaf litter-dwelling land snails of Belau (Republic of Palau, Oceania). Philos Trans R Soc B 363:3401–3412CrossRefGoogle Scholar
  155. Schell SC (1965) The life history of Haematoloechus breviplexus Stafford, 1902, (Trematoda: Haplometridae McMullen, 1937), with emphasis on the development of the sporocysts. J Parasitol 51:587–593PubMedCrossRefPubMedCentralGoogle Scholar
  156. Schell SC (1985) Trematodes of North America. University of Idaho Press, MoscowGoogle Scholar
  157. Schmidt-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, OxfordGoogle Scholar
  158. Scholz T, Besprozvannykh VV, Boutorina TE, Choudhury A, Cribb TH, Ermolenko AV, Faltýnková A, Shedko MB, Shimazu T, Smit NJ (2016) Trematode diversity in freshwater fishes of the Globe I: ‘Old World’. Syst Parasitol 93:257–269PubMedCrossRefGoogle Scholar
  159. Schotthoefer AM, Cole RA, Beasley VR (2003) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. J Parasitol 89:475–482PubMedCrossRefPubMedCentralGoogle Scholar
  160. Seely LA (1906) Two distomes. Biol Bull 10:249–254CrossRefGoogle Scholar
  161. Shields JD (1987) Pathology and mortality of the lung fluke Haematoloechus longiplexus (Trematoda) in Rana catesbeiana. J Parasitol 75:1005–1013CrossRefGoogle Scholar
  162. Skrjabin KI, Antipin DN (1962) The superfamily Plagiorchioidea Dollfus, 1930. In: Skrjabin KI (ed) Trematodes of animals and man, vol. 20. Akademy Nauk, CCCR, Moscow, pp 47–163 (in Russian)Google Scholar
  163. Snyder SD (1996) Host specificity among species of Haematoloechus (Digenea: Haematoloechidae). PhD thesis, University of Nebraska–Lincoln, LincolnGoogle Scholar
  164. Snyder SD, Janovy J Jr (1994) Second intermediate host-specificity of Haematoloechus complexus and Haematoloechus medioplexus (Digenea: Haematoloechidae). J Parasitol 80:1052–1055PubMedCrossRefPubMedCentralGoogle Scholar
  165. Snyder SD, Janovy J Jr (1996) Behavioral basis of second intermediate host specificity among four species of Haematoloechus (Digenea: Haematoloechidae). J Parasitol 82:94–99PubMedCrossRefPubMedCentralGoogle Scholar
  166. Snyder SD, Tkach VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). J Parasitol 87:1433–1440PubMedCrossRefPubMedCentralGoogle Scholar
  167. Sorensen RE, Minchella DJ (1998) Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia 115:188–195PubMedCrossRefPubMedCentralGoogle Scholar
  168. Stafford J (1902) The American representatives of Distomum cygnoides. Zool Jahr Abt Syst Geogr Biol Tiere 17:411–424Google Scholar
  169. Stafford J (1905) Trematodes from Canadian vertebrates. Zool Anz 28:681–694Google Scholar
  170. Standley CJ, Prepelitchi L, Pietrokovsky SM, Issia L, Stothard JR, Wisnivesky-Colli C (2013) Molecular characterization of cryptic and sympatric lymnaeid species from the Galba/Fossaria group in Mendoza Province, Northern Patagonia, Argentia. Parasit Vectors 6:304PubMedPubMedCentralCrossRefGoogle Scholar
  171. Stigge HA, Bolek MG (2015) The alteration of life history traits and increased success of Halipegus eccentricus through the use of a paratenic host: a comparative study. J Parasitol 101:658–665PubMedCrossRefPubMedCentralGoogle Scholar
  172. Stigge HA, Bolek MG (2016a) Anuran host species influence site fidelity of Halipegus occidualis. J Parasitol 102:47–53PubMedCrossRefPubMedCentralGoogle Scholar
  173. Stigge HA, Bolek MG (2016b) Evaluating the biological and ecological factors influencing transmission of larval digenetic trematodes: a test of second intermediate host specificity of two North American Halipegus species. J Parasitol 102:613–621PubMedCrossRefPubMedCentralGoogle Scholar
  174. Sudarikov VE (1950) The trematodes of vertebrates in the Middle Volga area. Trudy Gelmintol Lab Akad Nauk SSSR 3:131–141Google Scholar
  175. Szuroczki D, Richardson JML (2009) The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players. Oecologia 161:371–385PubMedCrossRefPubMedCentralGoogle Scholar
  176. Taylor DW (2003) Introduction to Physidae (Gastropoda: Hygrophila); biogeography, classification, morphology. Rev Biol Trop 51:S1–S287Google Scholar
  177. Thomas LJ (1939) Life cycle of a fluke Halipegus eccentricus n. sp. found in the ears of frogs. J Parasitol 25:207–221CrossRefGoogle Scholar
  178. Tkach VV, Lotz J, Swideerski Z, Esteban JG (2002) On the systematic position of Ophiosacculus Macy, 1935 (Digenea: Lecithodendriidae), with the erection of the Ophiosacculinae n. subfam. Syst Parasitol 53:159–167PubMedCrossRefPubMedCentralGoogle Scholar
  179. Toledo R, Carpena I, Espert A, Sotillo J, Munoz-Antoli C, Esteban JG (2006) A quantitative approach to the experimental transmission success of Echinostoma friedi (Trematoda: Echinostomatidae) in rats. J Parasitol 92:16–20PubMedCrossRefPubMedCentralGoogle Scholar
  180. Toledo R, Muñoz-Antoli C, Fried B (2007) The use of echinostomes to study host–parasite relationships between larval trematodes and invertebrate and cold-blooded vertebrate hosts. Parasitol Res 100:1177–1185PubMedCrossRefPubMedCentralGoogle Scholar
  181. Ubelaker JE, Olsen OW (1972) Life cycle of Phyllodistomum bufonis (Digenea: Gorgoderidae) from the boreal toad, Bufo boreas. Proc Helminthol Soc Wash 39:94–100Google Scholar
  182. van Theil PH (1930) Die Entwicklung von Agamodistomum anophelis zum Pneumonoecues variegates Rud. Zentralbl Bakteriol B 117:103–112Google Scholar
  183. Walther AC, Burch JB, Foighil DO (2010) Molecular phylogenetic revisions of the freshwater limpet genus Ferrissia (Planorbidae: Ancylinae) in North America yields two species: Ferrissia (Ferrissia) rivularis and Ferrissia (Kincaidilla) fragilis. Malacologia 53:25–45Google Scholar
  184. Ward HB (1917) On structure and classification of North American parasitic worms. J Parasitol 4:1–11CrossRefGoogle Scholar
  185. Weiss M, Weigand H, Weigand AM, Leese F (2018) Genome-wide single-nucleotide polymorphism data reveal cryptic species within cryptic freshwater snail species—the case of the Ancylus fluviatilis species complex. Ecol Evol 8:1063–1072PubMedCrossRefPubMedCentralGoogle Scholar
  186. Wetzel EJ, Esch GW (1996) Seasonal population dynamics of Halipegus occidualis and Halipegus eccentricus (Digenea: Hemiuridae) in their amphibian host, Rana clamitans. J Parasitol 82:414–422PubMedCrossRefPubMedCentralGoogle Scholar
  187. Wilke T, Pfenninger M (2002) Separating historic events from recurrent processes in cryptic species: phylogeography of mud snails (Hydrobia spp.). Mol Ecol 11:1439–1451PubMedCrossRefPubMedCentralGoogle Scholar
  188. Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku Publishing, TokyoGoogle Scholar
  189. Zamparo D, Ferrao A, Brooks DR, Bettaso J, Mata-Lopez R (2011) New species of Haematoloechus (Digenea: Plagiorchidae) in the lung of the foothill yellow-legged frog Rana boylii (Anura), from Humboldt County, California, USA. Rev Mexicana Biodivers 82:445–451Google Scholar
  190. Zelmer DA, Brooks DR (2000) Halipegus eschi n. sp. (Digenea: Hemiuridae) in Rana vaillanti from Guanacaste province, Costa Rica. J Parasitol 86:1114–1117PubMedCrossRefPubMedCentralGoogle Scholar
  191. Zelmer DA, Esch GW (1998a) Bridging the gap: the odonate naiad as a paratenic host for Halipegus occidualis. J Parasitol 84:94–96Google Scholar
  192. Zelmer DA, Esch GW (1998b) Interactions between Halipegus occidualis and its ostracod second intermediate host: evidence for castration. J Parasitol 84:778–782PubMedCrossRefPubMedCentralGoogle Scholar
  193. Zelmer DA, Esch GW (1999) Reevaluation of the taxonomic status of Halipegus occidualis Stafford, 1905 (Digenea: Hemiuridae). J Parasitol 85:157–160PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Matthew G. Bolek
    • 1
    Email author
  • Jillian T. Detwiler
    • 2
  • Heather A. Stigge
    • 3
  1. 1.Department of Integrative BiologyOklahoma State UniversityStillwaterUSA
  2. 2.Department of Biological SciencesUniversity of ManitobaWinnipegCanada
  3. 3.Department of BiologyCollege of Saint MaryOmahaUSA

Personalised recommendations