Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-18T15:55:01.347Z Has data issue: false hasContentIssue false
  • English
  • Français

Host dispersal and landscape conversion are associated with the composition of haemosporidian parasites of the golden-winged warbler

Published online by Cambridge University Press:  18 September 2019

Chelsea Enslow Open the ORCID record for Chelsea Enslow [Opens in a new window] ,
Rachel Vallender ,
Emily Rondel  and
Nicola Koper
Chelsea Enslow*
Affiliation:
University of Manitoba, 70-220 Dysart Road, Winnipeg, Manitoba, Canada
Rachel Vallender
Affiliation:
Canadian Wildlife Service, Environment and Climate Change Canada, 351 St. Joseph Blvd, Gatineau, QC, Canada
Emily Rondel
Affiliation:
Bird Studies Canada, & Toronto and Region Conservation Authority, 101 Exchange Ave, Concord, ON, Canada
Nicola Koper
Affiliation:
University of Manitoba, 70-220 Dysart Road, Winnipeg, Manitoba, Canada
*
Author for correspondence: Chelsea Enslow, E-mail: 1chelsea.enslow@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Understanding factors that influence the spatial and temporal distributions of blood parasites is important to help predict how host species and their parasites may respond to global change. Factors that may influence parasite distributions are land cover and host dispersal patterns, which may result in exposure of a host to novel parasites, or escape from parasites of their origin. We screened golden-winged warblers from across the United States and Canada for blood parasites, and investigated whether land-use patterns or host dispersal affected the prevalence and composition of haemosporidian assemblages. Parasite prevalence varied strongly with study area, and areas with high agricultural cover had a significantly higher prevalence of Leucocytozoon and Parahaemoproteus parasites. Lineages of Parahaemoproteus and Leucocytozoon were genetically differentiated among study areas, and prevalence and composition of parasite assemblages indicated an increase in parasite prevalence and accumulation of unique parasite lineages from the southeast to the northwest. This matches the historical range expansion and natal dispersal patterns of golden-winged warblers, and suggests that golden-winged warblers may have been sensitive to novel parasites as they dispersed. The high prevalence and diversity of parasite lineages in the north-west extent of their breeding range (Manitoba) indicates that this population may face unique pressures.

Keywords

Anthropogenic disturbancebiogeographyhaemosporidiahost–parasite interactionsVermivora
Type
Research Article
Information
Parasitology , Volume 147 , Issue 1 , January 2020 , pp. 96 - 107
Check for updates
Copyright
Copyright © Cambridge University Press 2019

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

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology, 403–410.CrossRefGoogle ScholarPubMed
Asghar, M, Hasselquist, D and Bensch, S (2011) Are chronic avian haemosporidian infections costly in wild birds? Journal of Avian Biology 42, 530–537.CrossRefGoogle Scholar
Bensch, S, Pérez-Tris, J, Waldenström, J and Olof, H (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 1617–1621.CrossRefGoogle ScholarPubMed
Bensch, S, Waldenström, J, Jonzén, N, Westerdahl, H, Hansson, B, Sejberg, D and Hasselquist, D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112–122.CrossRefGoogle Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) Malavi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.CrossRefGoogle ScholarPubMed
Bernotiene, R and Bartkeviciene, G (2013) The relationship between water temperature and the development cycle beginning and duration in three black fly species. Journal of Insect Science 13, 1–15.CrossRefGoogle ScholarPubMed
Bird, CE, Karl, S, Smouse, PE and Toonen, RJ (2011) Detecting and measuring genetic differentiation. In Held, C, Koenemann, S and Schubart, C (eds), Crustacean Issues: Phylogeography and Population Genetics in Crustacea. Boca Raton, USA: CRC Press, pp. 31–73.CrossRefGoogle Scholar
Bishop, AL, Mckenzie, HJ, Barchia, M and Harris, AM (1996) Effect of temperature regimes on the development, survival and emergence of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) in bovine dung. Australian Journal of Entomology 35, 361–368.CrossRefGoogle Scholar
Bonneaud, C, Sepil, I, Milá, B, Buermann, W, Pollinger, J, Sehgal, RNM, Valkiūnas, G, Lezhova, Ta., Saatchi, S and Smith, TB (2009) The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon. Journal of Tropical Ecology 25, 439–447.CrossRefGoogle Scholar
Brearley, G, Rhodes, J, Bradley, A, Baxter, G, Seabrook, L, Lunney, D, Liu, Y and Mcalpine, C (2013) Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88, 427–442.CrossRefGoogle ScholarPubMed
Buehler, D, Roth, A, Vallender, R, Will, T, Confer, JL, Canterbury, RA, Swarthout, SB, Rosenberg, KV and Bulluck, LP (2007) Status and conservation priorities of golden-winged warbler (Vermivora chrysoptera) in North America. The Auk 124, 1439–1445.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference, 2nd Edn. New York City, USA: Springer.Google Scholar
Chasar, A, Loiseau, C, Valkiūnas, G, Iezhova, T, Smith, TB and Sehgal, RNM (2009) Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Molecular Ecology 18, 4121–4133.CrossRefGoogle ScholarPubMed
Confer, JL, Hartman, P and Roth, A (2011) Golden-winged warbler (Vermivora chrysoptera). In Rodewald, PG (ed.), The Birds of North America. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America. Available at https://birdsna.org/Species-Account/bna/species/gowwar.Google Scholar
Córdoba-Lloria, S, Serna-Mompeán, JP, Giménez-Gras, O, Acosta-Aleixandre, R and Bueno-Mari, R (2017) Notes on black flies of the Júcar River and tributaries in Eastern Spain. The Simuliid Bulletin 48, 8–14.Google Scholar
Cozzarolo, C, Christe, P, Jenkins, T, Toews, DPL and Brelsford, A (2018) Prevalence and diversity of haemosporidian parasites in the rumped warbler hybrid zone. Ecology and Evolution 8, 9834–9847.CrossRefGoogle ScholarPubMed
Enslow, C (2017) Human Disturbance, Host Dispersal, and Hybridization Influence Blood Parasite Communities in a Threatened Songbird Species: The Golden-Winged Warbler (Vermivora Chrysoptera) (thesis). University of Manitoba, Winnipeg, Canada.Google Scholar
ESRI (2011) ArcGIS Desktop: Release 10. Redlands, CA: Environmental Systems Research Institute.Google Scholar
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Fecchio, A, Silveira, P, Weckstein, J and Anciaes, M (2019) First record of Leucocytozoon (Haemosporida: Leucocytozoidae) in Amazonia: evidence for rarity in Neotropical lowlands or lack of sampling for this parasite genus? Journal of Parasitology 104, 168–172.CrossRefGoogle Scholar
Figuerola, J, Munoz, E, Gutierrez, R and Ferrer, D (1999) Blood parasites, leucocytes and plumage brightness in the cirl bunting, Emberiza cirlus. Functional Ecology 13, 594–601.CrossRefGoogle Scholar
Fitzpatrick, BM (2009) Power and sample size for nested analysis of molecular variance. Molecular Ecology 18, 3961–3966.CrossRefGoogle ScholarPubMed
Foote, JR, Mennill, DJ, Ratcliffe, LM and Smith, SM (2010) Black-capped chickadee (Poecile atricapillus). In Rodewald, PG (ed.), The Birds of North America. Ithaca: Cornell Lab of Ornithology; Retrieved from the Birds of North America. Available at https://birdsna.org/Species-Account/bna/species/bkcchi.Google Scholar
Fredeen, FJH and Shemanchuk, JA (1960) Black flies (Diptera: Simuliidae) of irrigation systems in Saskatchewan and Alberta. Canadian Journal of Zoology 38, 723–735.CrossRefGoogle Scholar
Freeman-Gallant, CR, O'Connor, KD and Breuer, ME (2001) Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis). Oecologia 127, 517–521.CrossRefGoogle Scholar
Freund, D, Wheeler, SS, Townsend, AK, Boyce, WM, Ernest, HB, Cicero, C and Sehgal, RNM (2016) Genetic sequence data reveals widespread sharing of Leucocytozoon lineages in corvids. Parasitology Research, 1–9.Google ScholarPubMed
Galen, SC and Witt, CC (2014) Diverse avian malaria and other haemosporidian parasites in Andean house wrens: Evidence for regional co-diversification by host-switching. Journal of Avian Biology 45, 374–386.CrossRefGoogle Scholar
Gill, FB (1980) Historical aspects of hybridization between blue-winged and golden-winged warblers. The Auk 97, 1–18.Google Scholar
Gill, FB (1997) Local cytonuclear extinction of the golden-winged warbler. Evolution 51, 519–525.CrossRefGoogle ScholarPubMed
González, AD, Lotta, Ia., García, LF, Moncada, LI and Matta, NE (2015) Avian haemosporidians from Neotropical highlands: Evidence from morphological and molecular data. Parasitology International 64, 48–59.CrossRefGoogle ScholarPubMed
Greiner, EC, Bennett, GF, White, EM and Coombs, RF (1975) Distribution of the avian hematozoa of North America. Canadian Journal of Zoology 53, 1762–1787.CrossRefGoogle ScholarPubMed
Guo, SW and Thompson, EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361–372.CrossRefGoogle ScholarPubMed
Hellgren, O, Waldenström, J and Bensch, S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Parahaemoproteus from avian blood. The Journal of Parasitology 90, 797–802.CrossRefGoogle Scholar
Hellgren, O, Wood, M, Hasselquist, D, Ottosson, U, Stervander, M and Bensch, S (2013) Circannual variation in blood parasitism in a sub-Saharan migrant passerine bird, the garden warbler. Journal of Evolutionary Biology 26, 1047–1059.CrossRefGoogle Scholar
Ivanova, NV, DeWaard, JR and Hebert, PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6, 998–1002.CrossRefGoogle Scholar
Jetz, W, Thomas, G, Joy, JB, Hartmann, K and Mooers, A (2012) The global diversity of birds in space and time. Nature 491, 444–448.CrossRefGoogle ScholarPubMed
Kardatzke, JT and Rowley, WA (1971) Comparison of Culicoides larval habitats and populations in central Iowa. Annals of the Entomological Society of America 64, 215–218.CrossRefGoogle Scholar
Keane, RM and Crawley, MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164–170.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kimura, M, Dhondt, AA and Lovette, IJ (2006) Phylogeographic structuring of Plasmodium lineages across the North American range of the house finch (Carpodacus mexicanus). The Journal of Parasitology 92, 1043–1049.CrossRefGoogle Scholar
Kosmidis, I (2013) brglm: Bias reduction in binomial-response generalized linear models. Available at http://www.ucl.ac.uk/~ucakiko/software.html.Google Scholar
Kramer, GR, Streby, HM, Peterson, SM, Lehman, JA, Buehler, DA, Wood, PB, McNeil, DJ, Larkin, JL and Andersen, DE (2017) Nonbreeding isolation and population-specific migration patterns among three populations of golden-winged warblers. The Condor 119, 108–121.CrossRefGoogle Scholar
Kramer, GR, Andersen, DE, Buehler, DA, Wood, PB, Peterson, SM, Lehman, JA, Aldinger, KR, Bulluck, LP, Harding, S, Jones, JA, Loegering, JP and Smalling, C (2018) Population trends in Vermivora warblers are linked to strong migratory connectivity. Proceedings of the National Academy of Sciences of the United States of America 115, 192–200.CrossRefGoogle ScholarPubMed
Lachish, S, Knowles, SCL, Alves, R, Wood, MJ and Sheldon, BC (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. Journal of Animal Ecology 80, 1196–1206.CrossRefGoogle Scholar
LaPointe, DA, Atkinson, CT and Samuel, MD (2012) Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249, 211–226.CrossRefGoogle ScholarPubMed
Laurance, SGW, Jones, D, Westcott, D, McKeown, A, Harrington, G and Hilbert, DW (2013) Habitat fragmentation and ecological traits influence the prevalence of avian blood parasites in a tropical rainforest landscape. PLoS One 8, e76227.CrossRefGoogle Scholar
Lewicki, KE, Huyvaert, KP, Piaggio, AJ, Diller, LV and Franklin, AB (2015) Effects of barred owl (Strix varia) range expansion on Parahaemoproteus parasite assemblage dynamics and transmission in barred and northern spotted owls (Strix occidentalis caurina). Biological Invasions 17, 1713–1727.CrossRefGoogle Scholar
Loiseau, C, Harrigan, RJ, Cornel, AJ, Guers, SL, Dodge, M, Marzec, T, Carlson, JS, Seppi, B and Sehgal, RNM (2012 a) First evidence and predictions of Plasmodium transmission in Alaskan bird populations. PLoS One 7, e44729.CrossRefGoogle ScholarPubMed
Loiseau, C, Harrigan, RJ, Robert, A, Bowie, RCK, Henri, A, Smith, TB and Sehgal, RNM (2012 b) Host and habitat specialization of avian malaria in Africa. Molecular Ecology 21, 431–441.CrossRefGoogle ScholarPubMed
López-Calderón, C, Van Wilgenburg, SL, Roth, AM, Flaspohler, DJ and Hobson, KA (2019) An evaluation of isotopic (δ 2H) methods to provide estimates of avian breeding and natal dispersal. Ecosphere (Washington, D.C) 10, 1–20.Google Scholar
Manitoba Conservation, Manitoba Land Use Initiative (2005) Land use/Cover maps. Available at http://mli2.gov.mb.ca/landuse/index.html.Google Scholar
Mantilla, JS, Gonzáles, AD, Moncada, L and Matta, NE (2013) Description and molecular characterization of Plasmodium (novyella) unalis sp. nov. from the Great Thrush (Turdus fuscater) in highland of Colombia. Parasitology Research 112, 4193–4204.CrossRefGoogle ScholarPubMed
Marzal, A, de Lope, F, Navarro, C and Møller, AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142, 541–545.CrossRefGoogle Scholar
McCracken, JD (1994) Golden-winged and blue-winged warblers: their history and future in Ontario. In McNicholl, MK and Cranmer-Byng, JL (eds), Ornithology in Ontario. Whitby, Ontario: Hawk Owl Publishing, pp. 279–289.Google Scholar
Meixell, BW, Arnold, TW, Lindberg, MS, Smith, MM, Runstadler, JA and Ramey, AM (2016) Detection, prevalence, and transmission of avian hematozoa in waterfowl at the Arctic/sub-Arctic interface: co-infections, viral interactions, and sources of variation. Parasites & Vectors 9, 1–18.CrossRefGoogle ScholarPubMed
Merino, S, Moreno, J, Vásquez, RA, Martínez, J, Sánchez-monsálvez, I, Estades, CF, Ippi, S, Sabat, P, Rozzi, R and Mcgehee, S (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecology 33, 329–340.CrossRefGoogle Scholar
Møller, AP and Szép, T (2011) The role of parasites in ecology and evolution of migration and migratory connectivity. Journal of Ornithology 152, S141–S150.CrossRefGoogle Scholar
Montagna, CM, Gauna, LE, Angelo, APDD and Anguiano, OL (2012) Evolution of insecticide resistance in non-target black flies (Diptera: Simuliidae) from Argentina. Memórias do Instituto Oswaldo Cruz 107, 458–465.CrossRefGoogle ScholarPubMed
Moulton, L (2017) Golden-Winged Warbler (Vermivora Chrysoptera) Habitat Selection, Mating Behaviour, and Population Viability in a Fragmented Landscape at the Northern Range Limit (PhD thesis). University of Manitoba, Winnipeg, Canada.Google Scholar
Moulton, L and Artuso, C (2017) Golden-winged warbler. In Artuso, C, Couturier, AR, De Smet, KD, Koes, RF, Lepage, D, McCracken, J, Mooi, R and Taylor, P (eds), The Atlas of the Breeding Birds of Manitoba, 2010–2014. Winnipeg, Canada: Bird Studies Canada.Google Scholar
Moulton, LL, Vallender, R, Artuso, C and Koper, N (2018) The final frontier: early-stage genetic introgression and hybrid habitat use in the final frontier: early-stage genetic introgression and hybrid habitat use in the northwestern extent of the golden-winged Warbler breeding range. Conservation Genetics 18, 1481–1487.CrossRefGoogle Scholar
Murdock, CC, Adler, PH, Frank, J and Perkins, SL (2015) Molecular analyses on host-seeking black flies (Diptera: Simuliidae) reveal a diverse assemblage of Leucocytozoon (Apicomplexa: Haemospororida) parasites in an alpine ecosystem. Parasites & Vectors 8, 343.CrossRefGoogle Scholar
Oakgrove, KS, Harrigan, RJ, Loiseau, C, Guers, S, Seppi, B and Sehgal, RNM (2014) Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. International Journal for Parasitology 44, 717–727.CrossRefGoogle ScholarPubMed
Okanga, S, Cumming, GS, Hockey, PAR and Peters, JL (2013) Landscape structure influences avian malaria ecology in the Western Cape, South Africa. Landscape Ecology 28, 2019–2028.CrossRefGoogle Scholar
Olsson-Pons, S, Clark, NJ, Ishtiaq, F and Clegg, SM (2015) Differences in host species relationships and biogeographical influences produce contrasting patterns of prevalence, community composition and genetic structure in two genera of avian malaria parasites in southern Melanesia. Journal of Animal Ecology 84, 985–998.CrossRefGoogle Scholar
Ontario Ministry of Natural Resources (2008) Southern Ontario Land Resource Information System 1.2. Available at: https://www.javacoeapp.lrc.gov.on.ca/geonetwork/srv/en/main.home?uuid=c42f0216-df61-405f-8b99-0e613e1cfc85.Google Scholar
Ontario Natural Resources and Forestry (2011) Southern Ontario land resource information system 2.0. Available at https://www.ontario.ca/data/southern-ontario-land-resource-information-system-solris-20.Google Scholar
Pagenkopp, KM, Klicka, J, Durrant, KL, Garvin, JC and Fleischer, RC (2008) Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conservation Genetics 9, 1577–1588.CrossRefGoogle Scholar
Palinauskas, V, Valkiūnas, G, Bolshakov, CV and Bensch, S (2011) Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology 127, 527–533.CrossRefGoogle ScholarPubMed
Patz, JA, Olson, SH, Uejio, CK and Gibbs, HK (2008) Disease emergence from global climate and land use change. The Medical Clinics of North America 92, 1473–1491.CrossRefGoogle ScholarPubMed
Pérez-Rodríguez, A, Fernández-González, S, de la Hera, I and Pérez-Tris, J (2013) Finding the appropriate variables to model the distribution of vector-borne parasites with different environmental preferences: climate is not enough. Global Change Biology 19, 3245–3253.Google ScholarPubMed
Pulgarín, PC, Fitzgerald, AM, Gómez, C, Bayly, NJ, Bensch, S, Starkloff, N, Kirchman, JJ, González-prieto, AM, Hobson, KA, Ungvari-martin, J, Skeen, H, Isabel, M, Carlos, C and Cadena, D (2019) Migratory birds as vehicles for parasite dispersal? Infection by avian haemosporidians over the year and throughout the range of a long – distance migrant. Journal of Biogeography 46, 83–96.CrossRefGoogle Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Ricklefs, RE and Fallon, SM (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society B: Biological Sciences 269, 885–892.CrossRefGoogle ScholarPubMed
Ricklefs, RE, Outlaw, DC, Svensson-Coelho, M, Medeiros, MCI, Ellis, VA and Latta, S (2014) Species formation by host shifting in avian malaria parasites. Proceedings of the National Academy of Sciences of the United States of America 111, 14816–14821.CrossRefGoogle ScholarPubMed
Ricklefs, RE, Medeiros, M, Ellis, VA, Svensson-coelho, M, Blake, JG, Loiselle, BA, Soares, L, Fecchio, A, Outlaw, D, Marra, PP, Latta, SC, Bar, R and Jeremoabo, D (2016) Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography, 1277–1286.CrossRefGoogle Scholar
Rosenberg, KV, Will, T, Buehler, DA, Swarthout, SB, Thogmartin, WE, Bennett, RE and Chandler, RB (2016) Dynamic distributions and population declines of Golden-winged Warblers. In Streby, HM, Andersen, DE and Buehler, DA (eds), Golden-winged Warbler Ecology, Conservation, and Habitat Management. Boca Raton, FL: CRC Press, pp. 3–28.Google Scholar
Samuel, MD, Hobbelen, PHF, DeCastro, F, Ahumada, JA, LaPointe, DA, Atkinson, CT, Woodworth, BL, Hart, PJ and Duffy, DC (2011) The dynamics, transmission, and population impacts of avian malaria in native Hawaiian birds: a modeling approach. Ecological Applications 21, 2960–2973.CrossRefGoogle Scholar
Sarquis-Adamson, Y and MacDougall-Shackleton, EA (2016) Song sparrows Melospiza melodia have a home-field advantage in defending against sympatric malarial parasites. Royal Society Open Science 3, 160216.CrossRefGoogle ScholarPubMed
Sauer, JR, Hines, JE, Fallon, JE, Pardieck, KL, Ziolkowski, DJ Jr and Link, WA (2011) The North American Breeding Bird Survey, Results and Analysis 1966–2010, version 12.07. 2011 USGS Patuxent Wildlife Research Center, Laurel, MD. doi: 10.1128/JB.01736-06.CrossRefGoogle Scholar
Sehgal, RNM (2010) Deforestation and avian infectious diseases. The Journal of Experimental Biology 213, 955–960.CrossRefGoogle ScholarPubMed
Smith, JD, Gill, SA, Baker, KM and Vonhof, MJ (2017) Prevalence and diversity of avian Haemosporida infecting songbirds in southwest Michigan. Parasitology Research 117, 471–489.CrossRefGoogle ScholarPubMed
Sol, D, Jovani, R and Torres, J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Species At Risk Act (2002) s. 27. c. 29. Vol 141. No. 26 (2007).Google Scholar
Szymanski, MM and Lovette, IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. The Journal of Parasitology 91, 768–774.CrossRefGoogle Scholar
Takaoka, H, Yunus, M, Hadi, UK, Sigit, SH and Miyagi, I (2000) Preliminary report of faunistic surveys on black flies (Diptera: Simuliidae) in Sumatra, Indonesia. 28, 157–166.CrossRefGoogle Scholar
US Geological Survey, Multi-Resolution Land Characteristics (MRLC) Consortium (2011) National land cover database 2011. Available at https://www.mrlc.gov/nlcd2011.php.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Ratón, USA: CRC Press.Google Scholar
Vallender, R, Robertson, RJ, Friesen, VL and Lovette, IJ (2007) Complex hybridization dynamics between golden-winged and blue-winged warblers (Vermivora chrysoptera and Vermivora pinus) revealed by AFLP, microsatellite, intron and mtDNA markers. Molecular Ecology 16, 2017–2029.CrossRefGoogle ScholarPubMed
Vallender, R, Bull, RD, Moulton, LL and Robertson, RJ (2012) Blood parasite infection and heterozygosity in pure and genetic-hybrid golden-winged warblers (Vermivora chrysoptera) across Canada. The Auk 129, 716–724.CrossRefGoogle Scholar
Walther, EL, Carlson, JS, Cornel, A, Morris, BK and Sehgal, RNM (2016) First molecular study of prevalence and diversity of avian haemosporidia in a Central California songbird community. Journal of Ornithology 157, 549–564.CrossRefGoogle Scholar
White, P and Densmore, LD (1992) Molecular genetic analysis of populations. In Hoelzel, AR (ed.), A Practical Approach. Oxford, UK: Oxford University Press, pp. 29–58.Google Scholar
Zylberberg, M, Derryberry, EP, Breuner, C, Macdougall-shackleton, E and Cornelius, JM (2015) Haemoproteus infected birds have increased lifetime reproductive success. Parasitology 142, 1033–1043.CrossRefGoogle ScholarPubMed
Supplementary material: File

Enslow et al. supplementary material

Enslow et al. supplementary material

Download Enslow et al. supplementary material(File)
File 67.9 KB