Hostname: page-component-669899f699-ggqkh Total loading time: 0 Render date: 2025-04-26T20:39:09.669Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity of Trichobilharzia in New Zealand with a new species and a redescription, and their likely contribution to cercarial dermatitis

Published online by Cambridge University Press:  10 November 2021

Norman E. Davis ,
David Blair Open the ORCID record for David Blair [Opens in a new window]  and
Sara V. Brant Open the ORCID record for Sara V. Brant [Opens in a new window]
Norman E. Davis
Affiliation:
University of Otago, Dunedin, New Zealand
David Blair
Affiliation:
James Cook University, College of Science and Engineering, Townsville, Australia
Sara V. Brant*
Affiliation:
Department of Biology, University of New Mexico Museum of Southwestern Biology Division of Parasites, Albuquerque, New Mexico 87111, USA
*
Author for correspondence: Sara V. Brant, E-mail: sbrant@unm.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

In response to annual outbreaks of human cercarial dermatitis (HCD) in Lake Wanaka, New Zealand, ducks and snails were collected and screened for avian schistosomes. During the survey from 2009 to 2017, four species of Trichobilharzia were recovered. Specimens were examined both morphologically and genetically. Trichobilharzia querquedulae, a species known from four continents, was found in the visceral veins of the duck Spatula rhynchotis but the snail host remains unknown. Cercaria longicauda [i.e. Trichobilharzia longicauda (Macfarlane, 1944) Davis, 2006], considered the major aetiological agent of HCD in Lake Wanaka, was discovered, and redescribed from adults in the visceral veins of the duck Aythya novaeseelandiae and cercariae from the snail Austropeplea tomentosa. Recovered from the nasal mucosa of Ay. novaeseelandiae is a new species of Trichobilharzia that was also found to cycle naturally through Au. tomentosa. Cercariae of a fourth species of Trichobilharzia were found in Au. tomentosa but the species remains unidentified.

Keywords

Austropepleacercarial dermatitisLake Wanakamuseum vouchersNew Zealandschistosomesswimmer's itchTrichobilharzia
Type
Research Article
Information
Parasitology , Volume 149 , Issue 3 , March 2022 , pp. 380 - 395
Check for updates
Copyright
Copyright © The Author(s), 2021. 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.)

Article purchase

Temporarily unavailable

References

Aldhoun, J, Podhorský, M, Kolická, M and Horák, P (2012) Bird schistosomes in planorbid snails in the Czech Republic. Parasitology International 61, 250–259.CrossRefGoogle ScholarPubMed
Appleton, CC (1984) Schistosome dermatitis-an unrecognized problem in South Africa. South African Medical Journal 65, 467–469.Google Scholar
Appleton, CC (2003) The avian Schistosomatidae of sub-Saharan Africa with particular reference to Cercariae herini, a cause of dermatitis in people. Proceedings of Workshop on African Freshwater Malacology, 9-12 September, Kampala, Uganda, pp. 213–233.Google Scholar
Ashrafi, K, Nouroosta, A, Sharifdini, M, Mahmoudi, MR, Rahmati, B and Brant, SV (2018) Genetic diversity of an avian nasal schistosome causing cercarial dermatitis in the Black Sea-Mediterranean migratory route. Parasitology Research 117, 3821–3833.CrossRefGoogle ScholarPubMed
Ashrafi, K, Sharifdini, M, Darjani, A and Brant, SV (2021) Migratory routes, domesticated birds and cercarial dermatitis: the distribution of Trichobilharzia franki in Northern Iran. Parasite 28, 4.CrossRefGoogle ScholarPubMed
Basch, PF (1966) The life cycle of Trichobilharzia brevis n. sp., an avian schistosome from Malaya. Zeitschrift für Parasitenkunde 27, 252–259.CrossRefGoogle Scholar
Blair, D and Islam, KS (1983) The life cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Systematic Parasitology 5, 89–117.CrossRefGoogle Scholar
Blair, D and Ottesen, P (1979) Nasal schistosomiasis in Australian anatids. Journal of Parasitology 65, 982–984.CrossRefGoogle Scholar
Boray, JC (1964) Studies on the ecology of Lymnaea tomentosa, the intermediate host of Fasciola hepatica. 1. History, geographical distribution, and environment. Australian Journal of Zoology 12, 217–223.CrossRefGoogle Scholar
Bowles, J and McManus, DP (1993) Rapid discrimination of Echinococcus species and strains using a PCR-based RFLP method. Molecular and Biochemical Parasitology 57, 231–239.CrossRefGoogle Scholar
Bowles, J, Blair, D and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109.CrossRefGoogle ScholarPubMed
Brant, SV and Loker, ES (2009) Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. Journal of Parasitology 95, 941–963.CrossRefGoogle Scholar
Brant, SV and Loker, ES (2013) Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends in Parasitology 29, 449–459.CrossRefGoogle ScholarPubMed
Brant, SV, Morgan, JAT, Mkoji, GM, Snyder, SD, Rajapakse, RPVJ and Loker, ES (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology 92, 77–88.CrossRefGoogle ScholarPubMed
Brant, SV, Bochte, CA and Loker, ES (2011) New intermediate host records for the avian schistosomes Dendritobilharzia pulverulenta, Gigantobilharzia huronensis, and Trichobilharzia querquedulae from North America. Journal of Parasitology 97, 946–949.CrossRefGoogle ScholarPubMed
Brant, SV, Jouet, D, Ferté, H and Loker, ES (2013) Anserobilharzia gen. n. (Digenea, Schistosomatidae) and redescription of A. brantae (Farr & Blankemeyer, 1956) comb. n. (syn. Trichobilharzia brantae), a parasite of geese (Anseriformes). Zootaxa 3670, 139–206.CrossRefGoogle Scholar
Brant, SV, Loker, ES, Casalins, L and Flores, V (2017) Phylogenetic placement of a schistosome from an unusual marine snail host, the false limpet (Siphonaria lessoni) and gulls (Larus dominicanus) from Argentina with a brief review of marine schistosomes from snails. Journal of Parasitology 103, 75–82.CrossRefGoogle ScholarPubMed
Davis, NE (1998) Population dynamics and larval trematode interactions with Lymnaea tomentosa and the potential for biological control fo schistosome dermatitis in Bremner Bay, Lake Wanaka, New Zealand. Journal of Helminthology 72, 319–324.CrossRefGoogle Scholar
Davis, NE (2000) Cercarial Dermatitis and the Possibility of Biological Control in Lake Wanaka, New Zealand (A thesis submitted for the degree of Doctor of Philosophy at the University of Otago). Dunedin, New Zealand.Google Scholar
Davis, NE (2006a) Identification of an avian schistosome recovered from Aythya novaeseelandiae and infectivity of its miracidia to Lymnaea tomentosa snails. Journal of Helminthology 80, 225–253.Google Scholar
Davis, NE (2006b) A survey of waterfowl for echinostomes and schistosomes from Lake Wanaka and the Waitaki River watershed, New Zealand. Journal of Helminthology 80, 33–40.CrossRefGoogle Scholar
Devkota, R, Brant, SV, Thapa, S and Loker, ES (2014) Two avian schistosome cercariae from Nepal, including a Macrobilharzia-like species from Indoplanorbis exustus. Parasitology International 63, 374–380.CrossRefGoogle ScholarPubMed
Dyer, J and Williams, M (2010) An introduction most determined: Mallard (Anas platyrhynchos) to New Zealand. Notornis 57, 178–195.Google Scholar
Ebbs, ET, Loker, ES, Davis, NE, Flores, V, Veleizan, A and Brant, SV (2016) Schistosomes with wings: how host phylogeny and ecology shape the global distribution of Trichobilharzia querquedulae (Schistosomatidae). International Journal for Parasitology 46, 669–677.CrossRefGoogle 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
Fain, A (1955) Recherches sur les schistosomes d’oiseaux au Ruanda-Urundi (Congo belge). Revue de Zoologie et de Botanique Africaines 51, 373–387.Google Scholar
Fain, A (1956) Les schistosomes d'oiseaux du genre Trichobilharzia Skrjabin et Zakharov, 1920 au Ruanda Urundi. Revue de Zoologie et de Botanique Africaines 54, 147–178.Google Scholar
Fain, A (1959) Un nouveau schistosome du genre Trichobilharzia dans les fosses nasales du canard nain. Revue de Zoologie et de Botanique Africaines 60, 227–232.Google Scholar
Fakhar, M, Ghobaditara, M, Brant, SV, Karamian, M, Gohardehi, S and Bastani, R (2016) Phylogenetic analysis of nasal avian schistosomes (Trichobilharzia) from aquatic birds in Mazandaran Province, northern Iran. Parasitology International 65, 151–158.CrossRefGoogle ScholarPubMed
Featherston, DW and McDonald, TG (1988) Schistosome dermatitis in Lake Wanaka: survey of the snail population, 1976–77. New Zealand Journal of Zoology 15, 439–442.CrossRefGoogle Scholar
Featherston, DW, Weeks, PJ and Featherston, N (1988) Schistosome dermatitis in Lake Wanaka: Cercaria longicauda prevalence in Lymnaea tomentosa, 1978–1983. New Zealand Journal of Zoology 15, 381–386.CrossRefGoogle Scholar
Fraser, SJ, Allan, SJR, Roworth, M, Smith, HV and Holme, SA (2009) Cercarial dermatitis in the UK. Clinical and Experimental Dermatology 34, 344–346.CrossRefGoogle ScholarPubMed
Guay, PJ, Williams, M and Robinson, RW (2015) Lingering genetic evidence of North American mallards (Anas platyrhynchos) introduced to New Zealand. New Zealand Journal of Ecology 39, 103–109.Google Scholar
Horák, P, Kolárová, L and Dvořák, J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae) a new nasal schistosome from Europe. Parasite 5, 349–357.CrossRefGoogle Scholar
Horák, P, Kolárová, L and Adema, CM (2002) Biology of the schistosome genus Trichobilharzia. Advances in Parasitology 52, 155–233.CrossRefGoogle ScholarPubMed
Horák, P, Schets, FM, Kolárová, L and Brant, SV (2012) Chapter 42. Trichobilharzia. In Lui, D (ed.), Molecular Detection of Human Parasitic Pathogens. New South Wales, Australia: RCPA Biosecurity QAP. CRC Press, pp. 455–465.Google Scholar
Horák, P, Mikeš, L, Lichtenbergová, L, Skála, V, Soldánová, M and Brant, SV (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clinical Microbiology Reviews 28, 165–190.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.CrossRefGoogle ScholarPubMed
Islam, KS (1986) The morphology and life-cycle of Trichobilharzia arcuata n. sp. (Schistosomatidae: Bilharziellinae) a nasal schistosome of water whistle ducks (Dendrocygna arcuata) in Australia. Systematic Parasitology 8, 117–128.CrossRefGoogle Scholar
Islam, KS and Copeman, DB (1986) The morphology and life-cycle of Trichobilharzia parocellata (Johnston & Simpson, 1939) Islam & Copeman, 1980 from the visceral blood vessels of Australian anatids. Systematic Parasitology 8, 39–49.CrossRefGoogle Scholar
Jouet, D, Ferté, H, Depaquit, J, Rudolfová, J, Latour, P, Zanella, D, Kaltenback, ML and Léger, N (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitology Research 103, 51–58.CrossRefGoogle ScholarPubMed
Jouet, D, Skírnisson, K, Kolárová, L and Ferté, H (2010a) Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infection, Genetics and Evolution 10, 1218–1227.CrossRefGoogle Scholar
Jouet, D, Skírnisson, K, Kolárová, L and Ferté, H (2010b) Final hosts and variability of Trichobilharzia regenti under natural conditions. Parasitology Research 107, 923–930.CrossRefGoogle Scholar
Jouet, D, Kolárová, L, Patrelle, C, Ferté, H and Skírnisson, K (2015) Trichobilharzia anseri n. sp. (Schistosomatidae: Digenea), a new visceral species of avian schistosomes isolated from graylag good (Anser anser L.) in Iceland and France. Infection Genetics and Evolution 34, 298–306.CrossRefGoogle Scholar
Kolárová, L, Skírnisson, K, Ferté, H and Jouet, D (2013) Trichobilharzia mergi sp nov (Trematoda: Digenea: Schistosomatidae), a visceral schistosome of Mergus serrator (L.) (Aves: Anatidae). Parasitology International 62, 300–308.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lawton, SP, Lim, RM, Dukes, JP, Cook, RT, Walker, AJ and Kirk, RS (2014) Identification of a major causative agent of human cercarial dermatitis, Trichobilharzia franki (Müller and Kimmig 1994), in southern England and its evolutionary relationships with other European populations. Parasite Vectors 7, 277.CrossRefGoogle Scholar
Lockyer, AE, Olsen, PD, Ostergaard, P, Rollinson, D, Johnston, DA, Attwood, S W, Southgate, VR, Horák, P, Snyder, SD, Le, TH, Agatsuma, T, Mcmanus, DP, Carmichael, AC, Name, S and Littlewood, DTJ (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224.CrossRefGoogle ScholarPubMed
Lui, Z and Bai, G (1976) On bird schistosomes from Jilin Province: Jilinobilharzia crecci gen. nov., sp. nov. (Schistosomatidae: Bilharziellinae) with a discussion on the taxonomy of the subfamily Bilharziellinae. Acta Zoologica Sinica 22, 385–392.Google Scholar
Macfarlane, WV (1944) Schistosome dermatitis in the southern lakes: an investigation of swimmer's itch. New Zealand Medical Journal 43, 136–140.Google Scholar
Macfarlane, WV (1949) Schistosome dermatitis in New Zealand: part 1. The parasite. American Journal of Hygiene 50, 143–151.Google Scholar
Macfarlane, WV (1952) Schistosome dermatitis in Australia. The Medical Journal of Australia 20, 669–672.CrossRefGoogle Scholar
Maleki, SH, Athari, A, Haghighi, A, Taghipour, N, Gohardehi, SH and Tabaei, SS (2012) Species identification of bird nasal Trichobilharzia in Sari, north of Iran. Iran Journal of Parasitology 7, 82–85.Google Scholar
Manzoli, DE, Saravia-Pietropaolo, MJ, Arce, SI, Percara, A and Beldomenico, PM (2021) Specialist by preference, generalist by need: availability of quality hosts drives parasite choice in a natural multihost–parasite system. International Journal of Parasitology 51, 527–534.CrossRefGoogle Scholar
Mcleod, JA (1937) Two new schistosomid trematodes from water birds. Journal of Parasitology 23, 456–466.CrossRefGoogle Scholar
Mcmullen, DB and Beaver, PC (1945) Studies of schistosome dermatitis. IX. The life cycles of three dermatitis-producing schistosomes from birds and a discussion of the subfamily Bilharziellinae (Trematoda: Schistosomatidae). American Journal of Hygiene 42, 128–154.Google Scholar
Moema, EB, King, PH and Baker, C (2008) Cercariae developing in Lymnaea natalensis Krauss, 1848 collected in the vicinity of Pretoria, Gauteng Province, South Africa. Onderstepoort Journal of Veterinary Research 75, 215–233.CrossRefGoogle ScholarPubMed
Moema, EB, King, PH and Rakgole, JN (2019) Phylogenetic studies of larval digenean trematodes from freshwater snails and fish species in the proximity of Tshwane metropolitan, South Africa. Onderstepoort Journal of Veterinary Research 86, a1726.CrossRefGoogle ScholarPubMed
Morley, N (2009) Cercarial dermatitis in the UK: a long established history. Clinical and Experimental Dermatology 34, E443.CrossRefGoogle ScholarPubMed
Müller, V and Kimmig, P (1994) Trichobilharzia franki n. sp.-the cause of swimmer’s dermatitis in southwest German dredged lakes. Applied Parasitology 35, 12–31.Google Scholar
Palumbi, S, Martin, A, Romano, S, Wo, MM, Stice, L and Grabowski, G (1991) The Simple Fool's Guide to PCR. Honolulu, Hawaii. https://searchworks.stanford.edu/view/9267895.Google Scholar
Pinto, HA, Brant, SV and de Melo, AL (2014) Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Tropica 138, 38–43.CrossRefGoogle Scholar
Pinto, HA, Pulido-Murillo, EA, de Melo, AL and Brant, SV (2017) Putative new genera and species of avian schistosomes potentially involved in human cercarial dermatitis in the Americas, Europe and Africa. Acta Tropica 176, 415–420.CrossRefGoogle ScholarPubMed
Podhorský, M, Hůzová, Z, Mikeš, L and Horák, P (2009) Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitologica 54, 28–36.CrossRefGoogle Scholar
Porter, A (1938) The larval Trematoda found in certain South African Mollusca with special reference to schistosomiasis (bilharziasis). Publications of the South African Institute for Medical Research 62, 1–492.Google Scholar
Posada, D and Crandall, KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Pullan, NB, Climo, FM and Mansfield, CB (1972) Studies on the distribution and ecology of the family Lymnaeidae (Mollusca: Gastropoda) in New Zealand. Journal of the Royal Society of New Zealand 2, 393–405.CrossRefGoogle Scholar
Puslednik, L, Ponder, WF, Dowton, M and Davis, AR (2009) Examining the phylogeny of the Australasian Lymnaeidae (Heterobranchia: Pulmonata: Gastropoda) using mitochondrial, nuclear and morphological markers. Molecular Phylogenetics and Evolution 52, 643–659.CrossRefGoogle ScholarPubMed
Rind, S (1974) Some helminth parasites of freshwater birds from the South Island, New Zealand, with particular reference to trematodes of ducks. Mauri ora 2, 139–146.Google Scholar
Rind, S (1991) Three ocellate schistosome cercariae (Trematoda: Schistosomatidae) in Gyraulus corinna, with reference to Cercaria longicauda Macfarlane, 1944 in Lymnaea tomentosa. New Zealand Journal of Zoology 18, 53–62.CrossRefGoogle Scholar
Rudolfová, J, Sitko, J and Horák, P (2002) Nasal schistosomes of wildfowl in the Czech Republic. Parasitology Research 88, 1093–1095.CrossRefGoogle ScholarPubMed
Rudolfová, J, Hampl, V, Bayssade-Dufour, C, Lockyer, AE, Littlewood, DTJ and Horák, P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitology Research 95, 79–89.CrossRefGoogle ScholarPubMed
Skírnisson, K, Kolárová, L, Horák, P, Ferté, H and Jouet, D (2012) Morphological features of the nasal blood fluke Trichobilharzia regenti (Schistosomatidae, Digenea) from naturally infected hosts. Parasitology Research 110, 1881–1892.CrossRefGoogle ScholarPubMed
Soldanová, M, Selbach, C, Kalbe, M, Kostadinova, A and Sures, B (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends in Parasitology 29, 65–74.CrossRefGoogle ScholarPubMed
Spurr, EB, Coleman, JD and Whenua, M (2005) Review of Canada Goose Population Trends, Damage and Control in New Zealand. Lincoln, NZ: Manaaki Whenua Press, Landcare Research.Google Scholar
Stecher, G, Tamura, K and Kumar, S (2020) Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution. https://doi.org/10.1093/molbev/msz312.CrossRefGoogle ScholarPubMed
Suzuki, N and Kawanaka, M (1980) Trichobilharzia brevis Basch, 1966, as a cause of an outbreak of cercarial dermatitis in Japan. Japanese Journal of Parasitology 29, 1–11.Google Scholar
Thompson, CW, Phelps, KL, Allard, MW, Cook, JA, Dunnum, JL, Ferguson, AW, Gelang, M, Khan, FAA, Paul, DL, Reeder, DM, Simmons, NB, Vanhove, MPM, Webala, PW, Weksler, M and Kilpatrick, CW (2021) Preserve a voucher specimen! The critical need for integrating natural history collections in infectious disease studies. mBio 12, e02698–20.CrossRefGoogle ScholarPubMed
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, 839–846.CrossRefGoogle ScholarPubMed
Vinarski, MV, Aksenova, OV and Bolotov, IN (2020) Taxonomic assessment of genetically-delineated species of radicine snails (Mollusca, Gastropoda, Lymnaeidae). Zoosystematics and Evolution 96, 577–608.CrossRefGoogle Scholar