Abstract
Patagifer Dietz, 1909 is a small genus of echinostomatids, with 12 recognized species, mostly parasitising threskiornithid birds, distributed worldwide. In the current research, adult specimens of the type species, Patagifer bilobus (Rudolphi, 1819) Dietz, 1909 from the white faced ibis (Plegadis chihi) and white ibis (Eudocimus albus) were re-described, providing new metrical data for the number of head collar spines. Those specimens were recorded from eight localities in Mexico and compared morphologically with specimens previously identified as Patagifer lamothei. A total of 19 specimens identified as P. bilobus including two hologenophores were sequenced with three molecular markers: domains D1–D3 of the large subunit (LSU), the internal transcribed spacer (ITS1, ITS2) plus 5.8S from the nuclear rDNA, and nicotinamide adenine dinucleotide dehydrogenase subunit 1 (nad1) from mitochondrial DNA. The new sequences were aligned with other sequences of Patagifer spp., downloaded from GenBank. Phylogenetic trees inferred from each data set, placed all the specimens in a clade, confirming that the isolates belonged to the same species. The morphological examination of specimens previously identified as P. lamothei by Ortega-Olivares MP, Hernández-Mena DI, Pérez-Ponce de León G, García-Varela M (2011) Helminths of the white ibis, Eudocimus albus (Aves Therskiornithidae) in Mexico. (Zootaxa 3088, 15–26. 10.11646/zootaxa.3088.1.2) and in combination with molecular data confirms that those specimens should be reassigned to P. bilobus. In addition, this is the first study in P. bilobus using an integrative taxonomy approach.
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References
American Ornithologists’ Union (AOU) (1998) Check-list of North American birds. 7th ed. 829 pp. Washington, DC, AOU.
Boero JJ, Led JE (1968) El parasitismo de la fauna autóctona. III. Los parásitos de las aves argentinas. Revista De La Facultad De Ciencias Veterinarias De La Plata 10:97–129
Bowles J, McManus DP (1993) Rapid discrimination of Echinococcus species and strains using a PCR-based method. Mol Biochem Parasitol 57:231–239. https://doi.org/10.1016/0166-6851(93)90199-8
Brown JW, Payne RB, Mindell DP (2007) Nuclear DNA does not reconcile ‘rocks’ and ‘clocks’ in Neoaves: a comment on Ericson et al. Biol Lett 3:257–259. https://doi.org/10.1098/rsbl.2006.0611
Brown JW, Rest JS, García-Moreno J, Sorenson MD, Mindell DP (2008) Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biol 6:6. https://doi.org/10.1186/1741-7007-6-6
Bush AO, Forrester DJ (1976) Helminths of the white ibis in Florida. Proc Helminthol Soc Wash 43:17–23
Carmona R, Ruíz-Campos G, Castillo-Guerrero JL, Zamora-Orozco M (2002) Current distribution status of the White-faced Ibis, Plegadis chihi, in the Peninsula of Baja California, Mexico, with special reference to the region of La Paz. The Southewestern Naturalis 47:476–482. https://doi.org/10.2307/3672509
Choe S, Lee D, Park H, Oh M, Jeon HK, Lee Y, Na KJ, Kim Y, Lee H, Eom KS (2014) Three echinostome species from wild birds in the Republic of Korea. Korean J Parasitol 52(5):513–520. https://doi.org/10.3347/kjp.2014.52.5.513
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(2):611–620. https://doi.org/10.1016/j.ympev.2010.01.004
Dietz E (1910) Die Echinostomiden der Vo ̈gel. Zoologische Jahrbücher 12:S256–S512
Digiani MC (2000) Digenea and cestodes parasitic in the white-faced ibis Plegadischihi (Aves: Threskiornithidae) from Argentina. Folia Parasitol 47:195–204. https://doi.org/10.14411/fp.2000.037
Dronen NO, Blend CK (2008) Petagifer lamothei n. sp. (Digenea: Echinostomatidae: Nephrostominae) from the white ibis Eudocimus albus (Threskiornithidae) from Texas, USA. Rev Mex De Biodiv 79:23–32
Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I (2004) Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis Aquat Organ 59(1):35–41. https://doi.org/10.3354/dao059035
Faltýnková A, Gibson DI, Kostadinova A (2008) A revision of Patagifer Dietz, 1909 (Digenea: Echinostomatidae) and a key to its species. Syst Parasitol 70:159–183. https://doi.org/10.1007/s11230-008-9136-8
Forrester DJ, Spalding MG (2003) Parasites and diseases of wild birds in Florida. University Press of Florida, Gainesville, Florida, p 1132
Frederick PC, Ogden JC (1997) Philopartry and nomadism: contrasting long-term movement behavior and population dynamics of White Ibises and Wood Storks. Colon Waterbirds 20:316–323
García-Varela M, Nadler SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rRNA gene sequences. J Parasitol 91:1401–1409. https://doi.org/10.1645/GE-523R.1
Georgieva S, Kostadinova A, Skirnisson K (2012) The life-cycle of Petasiger islandicus Kostadinova & Skirnisson, 2007 (Digenea: Echinostomatidae) elucidated with the aid of molecular data. Syst Parasitol 82(3):177–83. https://doi.org/10.1007/s11230-012-9354-y
Georgieva S, Selbach C, Faltýnková 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. Parasites Vectors 6:64. https://doi.org/10.1186/1756-3305-6-64
Georgieva S, Faltýnková A, Brown R, Blasco-Costa I, Soldánová M, Sitko J, Scholz T, Kostadinova A (2014) Echinostoma ‘revolutum’ (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasites Vectors 7:520. https://doi.org/10.1186/s13071-014-0520-8
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(10):3867–3880. https://doi.org/10.1007/s00436-016-5152-9
Gouy M, Guindon S, Gascuel O (2010) SEAVIEW Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Hernández-Cruz E, Hernández-Orts JS, Sereno-Uribe AL, Ponce P, de León G, García-Varela M (2018) Multilocus phylogenetic analysis and morphological data reveal a new species composition of the genus Drepanocephalus Dietz, 1909 (Digenea: Echinostomatidae), parasites of fish-eating birds in the Americas. J Helminthol 92:572–595. https://doi.org/10.1017/S0022149X17000815
Howell SNG, Webb S (1995) A guide to the birds of Mexico and Northern Central America. 851 pp. New York, Oxford University Press.
Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176. https://doi.org/10.1023/A:1022681123340
Kostadinova A (2005) Family Echinostomatidae. pp. 9–64 in Jones A, Bray RA and Gibson DI (Eds) Keys to the Trematoda. Volume 2. Wallingford, CAB International and the Natural History Museum, London.
Kudlai O, Tkach VV, Pulis EE, Kostadinova A (2015) Redescription and phylogenetic relationships of Euparyphium capitaneum Dietz, 1909, the type-species of Euparyphium Dietz, 1909 (Digenea: Echinostomatidae). Syst Parasitol 90:53–65. https://doi.org/10.1007/s11230-014-9533-0
Laidemitt MR, Brant SV, Mutuku MW, Mkoji GM, Loker ES (2019) The diverse echinostomes from East Africa: with a focus on species that use Biomphalaria and Bulinus as intermediate hosts. Acta Trop 193:38–49. https://doi.org/10.1016/j.actatropica.2019.01.025
Lotfy WM, Brant SV, DeJong RJ, Le TH, Demiaszkiewicz A, Rajapakse RP, Perera VB, Laursen JR, Loker ES (2008) Evolutionary origins, diversification, and biogeography of liver flukes (Digenea, Fasciolidae). Am J Trop Med Hyg 79(2):248–255
Lumsden RD (1962) Four echinostome trematodes from Louisiana birds including the description of a new species. Tulane Studies in Zoology 9:301–308
Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.7.5. Available at: http://mesquiteproject.org/.
Matheu E, del Hoyo J (1992) Family Threskiornithidae (Ibises & Spoonbills). In del Hoyo J, Elliott A, Sargatal J (Eds). Handbook of the birds of the world (v 1.0). Barcelona: Lynx Edicions.
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE) 1–8.
Molnar K, Gibson DI, Cech G, Papp M, Deak-Paulus P, Juhasz L, Toth N, Szekely C (2015) The occurrence of metacercariae of Petasiger (Digenea: Echinostomatidae) in an unusual site, within the lateral line scales of cyprinid fishes. Folia Parasitol, 1, 62. https://doi.org/10.14411/fp.2015.017
Morgan JAT, Blair D (1998) Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. Int J Parasitol 28:493–502. https://doi.org/10.1016/s0020-7519(97)00204-x
Nadler SA, D´Amelio S, Fagerholm HP, Berland B, Paggi L (2000) Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris
Ortega-Olivares MP, Hernández-Mena DI, Pérez-Ponce de León G, García-Varela M (2011) Helminths of the white ibis, Eudocimus albus (Aves Therskiornithidae) in Mexico. Zootaxa 3088, 15–26. https://doi.org/10.11646/zootaxa.3088.1.2
Padilla-Aguilar P, Romero-Callejas E, Osorio-Sarabia D, Pérez-Ponce de León G, Alcalá-Canto Y (2020) New records of helminth parasites of nine species of waterfowl in Mexico, and a checklist of the helminth fauna of Anatidae occurring in Mexican wetlands. J Helminthol 94:E176. https://doi.org/10.1017/S0022149X20000577
Patten MA, Lasley GW (2000) Range expansion of the Glossy Ibis in North America. North America Birds 54:241–247
Pinto HA, Griffin MJ, Quiniou SM, Ware C, Melo AL (2016) Biomphalaria straminea (Mollusca: Planorbidae) as an intermediate host of Drepanocephalus spp. (Trematoda: Echinostomatidae) in Brazil: a morphological and molecular study. Parasitol Res 115:51–62. https://doi.org/10.1007/s00436-015-4469-0
Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371. https://doi.org/10.1016/j.ympev.2008.03.024
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083
Rambaut A (2012) FigTree v1.4.0. Institute of Evolutionary Biology. University of Edinburgh, UK.
Ramirez JL, Miyaqui CY, Del Lama SN (2013) Molecular phylogeny of Threskionithidae (Aves: Pelecaniformes) based on nuclear and mitochondrial DNA. Genet Mol Res 12:2740–2750. https://doi.org/10.4238/2013.July.30.11
Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard M, Huelsenbeck JP (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Ryder RA, Manry DE (1994). White-faced Ibis (Plegadis chihi). The Birds of North America (P.G. Rodewald Ed.). Ithaca: Cornell Lab of Ornithology. https://www.allaboutbirds.org/guide/White-faced_Ibis/overview
Schmidt GD, Bush AO (1972) Parvitaenia ibisae sp. n. (Cestoidea: Dilepididae), from birds in Florida. J Parasitol 58:1095–1097
Sereno-Uribe AL, Pinacho-Pinacho CD, Sanchéz Cordero V, García-Varela M (2015) Morphological and molecular analyses of larval and adult stages of Echinoparyphium recurvatum von Linstow 1873 (Digenea: Echinostomatidae) from central Mexico. J Helminthol 89:458–464. https://doi.org/10.1017/S0022149X14000297
Shuford WD, Hickey CM, Safran RJ, Page GW (1996) A review of the status of the White-faced Ibis in winter in California. Western Birds 27:169–196
Silvestro D, Michalak I (2011) RaxmlGUI: a graphical front end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tkach V, Pawlowski J, Mariaux J (2000) Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 30(1):83–93. https://doi.org/10.1016/S0020-7519(99)00163-0
Tkach V, Kudlai O, Kostadinova A (2016) Molecular phylogeny and systematic of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). Int J Parasitol 46:171–185. https://doi.org/10.1016/j.ijpara.2015.11.001
Viana L (1924) Tentativa de catalogaçao das espécies brasileiras de trematódeos. Mem Inst Oswaldo Cruz 17:95–227
Acknowledgements
We are grateful to Laura Márquez and Nelly López Ortiz, LaNaBio for their help during the sequencing of the DNA fragments. We are grateful to Berenit Garfias for her help in laboratory. We are also grateful to Luis García for loan material from CNHE. MTGG and ALJ thank the support of the Programa de Posgrado en Ciencias Biológicas, UNAM, and CONACYT (CVU 956064; CVU 706119) respectively for granting a scholarship to complete their Master and PhD programme.
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This research was supported by grants from the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM) IN201122.
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Sereno-Uribe, A.L., González-García, M.T., Ortega-Olivares, M.P. et al. First record of Patagifer bilobus (Rudolphi, 1819) Dietz, 1909 (Digenea: Echinostomatidae), with a morphological and molecular characterization from two threskiornithid species in Mexico. Parasitol Res 121, 1921–1935 (2022). https://doi.org/10.1007/s00436-022-07526-3
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DOI: https://doi.org/10.1007/s00436-022-07526-3