Abstract
Blue-winged teal (Anas discors) are abundant, small-bodied dabbling ducks that breed throughout the prairies of the northcentral USA and central Canada and that winter in the southern USA and northern Neotropics. Given the migratory tendencies of this species, it is plausible that blue-winged teal may disperse avian pathogens, such as parasites causing avian malaria, between spatially distant areas. To test the hypothesis that blue-winged teal play a role in the exchange of blood parasites between North America and areas further south, we collected information on migratory tendencies of this species and sampled birds at spatially distant areas during breeding and non-breeding periods to diagnose and genetically characterize parasitic infections. Using a combination of band recovery data, satellite telemetry, molecular diagnostics, and genetic analyses, we found evidence for (1) migratory connectivity of blue-winged teal between our sampling locations in the Canadian prairies and along the US Gulf Coast with areas throughout the northern Neotropics, (2) parasite acquisition at both breeding and non-breeding areas, (3) infection of blue-winged teal sampled in Canada and the USA with Plasmodium parasite lineages associated with the Neotropics, and (4) infection of blue-winged teal with parasites that were genetically related to those previously reported in waterfowl in both North America and South America. Collectively, our results suggest that blue-winged teal likely play a role in the dispersal of blood parasites between the Neotropics and North America, and therefore, the targeting of this species in surveillance programs for the early detection of Neotropical-origin avian pathogens in the USA may be informative.
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References
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Bennett GB, Blandin W, Heusmann HW, Campbell AG (1974) Hematozoa of the Anatidae of the Atlantic flyway. I Massachusetts. J Wildl Dis 10:442–451
Bennett GB, Smith AD, Whitman W (1975) Hematozoa of the Anatidae of the Atlantic flyway. II. The maritime provinces of Canada. J Wildl Dis 11:280–289
Bennett GB, Nieman DJ, Turner B, Kuyt E, Whiteway M, Greiner E (1982) Blood parasites of prairie anatids and their implication in waterfowl management in Alberta and Saskatchewan. J Wildl Dis 18:287–296
Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358
Botero JE, Rusch DH (1988) Recoveries of North American waterfowl in the Neotropics. In: Weller MW (ed) Waterfowl in winter. University of Minnesota Press, Minneapolis, pp 469–482
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer-Verlag, New York
Calisher CH, Maness KSC, Lord RD, Coleman PH (1971) Identification of two South American strains of eastern equine encephalomyelitis virus from migrant birds captured on the Mississippi Delta. Am J Epidemiol 94:172–178
Carney SM (1992) Species, age, and sex identification of ducks using wing plumage. U.S. Department of the Interior, Washington, D.C
Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. Int J Parasitol 44:329–338
Clark NJ, Clegg SM, Klaassen M (2015) Migration strategy and pathogen risk: non‐breeding distribution drives malaria prevalence in migratory waders. Oikos. doi:10.1111/oik.03220
CLS America (2007) Argos user’s manual. Retrieved from: http://www.argos-system.org/manual/
Cohen E, Auckland LD, Marra PP, Hamer SA (2015) Avian migrants facilitate invasions of Neotropical ticks and tick-borne pathogens into the United States. Appl Environ Microbiol. doi:10.1128/AEM.02656-15
Cooch EG, White GC (2014) Program MARK: a gentle introduction, 13th edition. Available at: http://www.phidot.org/software/mark/docs/book/
Cox RR, Afton AD (1994) Portable platforms for setting rocket nets in open-water habitats. J Field Ornithol 65:551–555
Douglas KO, Lavoie MC, Kim LM, Afonso CL, Suarez DL (2007) Isolation and genetic characterization of avian influenza viruses and a Newcastle disease virus from wild birds in Barbados: 2003–2004. Avian Dis 51:781–787
Douglas DC, Weinzierl R, Davidson SC, Kays R, Wikelski M, Bohrer G (2012) Moderating Argos location errors in animal tracking data. Methods Ecol Evol 3:999–1007
Gilbert M, Xiao X, Domenech J, Lubroth J, Martin V, Slingenbergh J (2006) Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerg Infect Dis 12:1650–1656
González-Reiche AS, Morales-Betoulle ME, Alvarez D, Betoulle J-L, Müller ML, Sosa SM, Perez DR (2012) Influenza A viruses from wild birds in Guatemala belong to the North American lineage. PLoS ONE 7:e32873
Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802
Hupp JW, Yamaguchi N, Flint PL, Pearce JM, Tokita K, Shimada T, Ramey AM, Kharitonov S, Higuchi H (2011) Variation in spring migration routes and breeding distribution of northern pintails Anas acuta that winter in Japan. J Avian Biol 42:289–300
Hupp JW, Kharitonov S, Yamaguchi N, Ozaki K, Flint PL, Pearce JM, Tokita K, Shimada T, Higuchi H (2015) Evidence that dorsally mounted satellite transmitters affect migration chronology of northern pintails. J Ornithol 156:977–989
Karlsson EA, Ciuoderis K, Freiden PJ, Seufzer B, Jones JJ, Johnson J, Parra R, Gongora A, Cardenas D, Barajas D, Osario JE, Schultz-Cherry S (2013) Prevalence and characterization of influenza viruses in diverse species in Los Llanos, Columbia. Emerg Microbiol Infect 2:e20
Kerr KCR, Stoeckle MY, Dove CJ, Weigt LA, Francis CM, Hebert PDN (2007) Comprehensive DNA barcode coverage of North American birds. Mol Ecol 7:535–543
Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118
Lee D-H, Torchetti MK, Winker K, Ip HS, Song C-S, Swayne DE (2015) Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory birds. J Virol 89:6521–6524
Loven JS, Bolen EG, Cain BW (1980) Blood parasitemia in a south Texas wintering waterfowl population. J Wildl Dis 16:25–28
MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press, Burlington
Matta NE, Pacheco MA, Escalante AA, Valkiūnas G, Ayerbe-Quiñones F, Acevedo-Cendales LD (2014) Description and molecular characterization of Haemoproteus macrovacuolatus n. sp. (Haemosporida, Haemoproteidae), a morphologically unique blood parasite of black-bellied whistling duck (Dendrocygna autumnalis) from South America. Parasitol Res 113:2991–3000
Mauser DM, Mensik JG (1992) A portable trap for ducks. Wildl Soc Bull 20:299–302
McClintock BT, Nichols JD, Bailey LL, MacKenzie DI, Kendall WL, Franklin AB (2010) Seeking a second opinion: uncertainty in disease ecology. Ecol Lett 13:659–674
Miller MR, Takekawa JY, Fleskes JP, Orthmeyer DL, Casazza ML, Perry WM (2005) Spring migration of northern pintails from California’s Central Valley wintering area tracked with satellite telemetry: routes, timing, and destinations. Can J Zool 83:1314–1332
Ramey AM, Ely CR, Schmutz JA, Pearce JM, Heard DJ (2012) Molecular detection of hematozoa infections in tundra swans relative to migration patterns and ecological conditions at breeding grounds. PLoS ONE 7:e45789
Ramey AM, Reeves AB, Ogawa H, Ip HS, Imai K, Nghia Bui V, Yamaguchi E, Silko NY, Afonso CL (2013a) Genetic diversity and mutation of avian paramyxovirus serotype 1 (Newcastle disease virus) in wild birds and evidence for intercontinental spread. Arch Virol 158:2495–2503
Ramey AM, Fleskes JP, Schmutz JA, Yabsley MJ (2013b) Evaluation of blood and muscle tissues for molecular detection and characterization of hematozoa infections in northern pintails (Anas acuta) wintering in California. Int J Parasitol Parasites Wildl 2:102–109
Ramey AM, Reed JA, Schmutz JA, Fondell TF, Meixell BW, Hupp JW, Ward DH, Terenzi J, Ely CR (2014) Prevalence, transmission, and genetic diversity of blood parasites infecting tundra-nesting geese in Alaska. Can J Zool 92:699–706
Ramey AM, Reeves AB, Sonsthagen SA, TeSlaa JL, Nashold S, Donnelly T, Casler B, Hall JS (2015a) Dispersal of H9N2 influenza A viruses between East Asia and North America by wild birds. Virology 482:79–83
Ramey AM, Schmutz JA, Reed JA, Fujita G, Scotton BD, Casler B, Fleskes JP, Konishi K, Uchida K, Yabsley MJ (2015b) Evidence for intercontinental parasite exchange through molecular detection and characterization of hematozoa in northern pintails (Anas acuta) sampled throughout the North Pacific Basin. Int J Parasitol Parasites Wildl 4:11–21
Ramey AM, Walther P, Link P, Poulson RL, Wilcox BR, Newsome GM, Spackman E, Brown JD, Stallknecht DE (2016) Optimizing surveillance for South American origin influenza A viruses along the United States Gulf Coast through genomic characterization of isolates from blue-winged teal. Transbound Emerg Dis 63:194–202
Reeves AB, Smith MM, Meixell BW, Fleskes JP, Ramey AM (2015) Genetic diversity and host specificity varies across three genera of blood parasites in ducks of the Pacific Americas flyway. PLoS ONE 10:e0116661
Rohwer FC, Johnson WP, Loos ER (2002) Blue-winged teal (Anas discors), the birds of North America online (A. Poole, Ed.). Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/625 doi:10.2173/bna.625.
Smith MM, Ramey AM (2015) Prevalence and genetic diversity of hematozoa in South American waterfowl and evidence for intercontinental redistribution of parasites by migratory birds. Int J Parasitol Parasites Wildl 4:22–28
Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774
Tallman EJ, Corkum KC, Tallman DA (1985) The trematode fauna of two intercontinental migrants: Tringa solitaria and Calidris melanotos (Aves: Charadriiformes). Am Midl Nat 113:374–383
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
Verhagen JH, van der Jeugd HP, Nolet BA, Slaterus R, Kharitonov SP, de Vries PP, Vuong O, Majoor F, Kuiken T, Fouchier RA (2015) Wild bird surveillance around outbreaks of highly pathogenic avian influenza A (H5N8) virus in the Netherlands, 2014, within the context of global flyways. Euro Surveill 20:
White EM, Greiner EC, Bennett GF, Herman CM (1978) Distribution of the hematozoa of Neotropical birds. Rev Biol Trop 26(Suppl 1):43–102
Acknowledgments
This work was funded by the US Geological Survey through the Wildlife Program of the Ecosystem Mission Area and the Contaminants Biology Program of the Environmental Health Mission Area. Canadian field work was funded by Environment Canada, Alberta Conservation Association, Institute for Wetland and Waterfowl Research–Ducks Unlimited Canada, and the University of Saskatchewan. Waterfowl captures in Canada were conducted in collaboration with the US Fish and Wildlife Service and Canadian Wildlife Service personnel. Sample collection and/or deployment of PTTs were conducted with the help of Amy Wilson, Sofia Mlala, Gillian Treen, Jamille McLeod, Kailee Price, Emilie Bouchard, Karen Gesy, Ben Wilcox, George Newsome, Phillip Pauling, Paul Oesterle, Wade Broussard, Alinde Fojtik, Deborah Carter, Jeremiah Slagter, Nick Davis-Fields, Jim LaCour, Jacob Gray, and Kristen DeMarco. We thank Craig Ely for providing advice regarding obtaining and analyzing band recovery data. We appreciate critical reviews provided by John Pearce, Brandt Meixell, Michael Yabsley, and an anonymous reviewer. None of the authors have any financial interests or conflict of interest with this article. Any use of trade names is for descriptive purposes only and does not imply endorsement by the US Government.
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Ramey, A.M., Reed, J.A., Walther, P. et al. Evidence for the exchange of blood parasites between North America and the Neotropics in blue-winged teal (Anas discors). Parasitol Res 115, 3923–3939 (2016). https://doi.org/10.1007/s00436-016-5159-2
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DOI: https://doi.org/10.1007/s00436-016-5159-2