in

Using a multistate occupancy approach to determine molecular diagnostic accuracy and factors affecting avian haemosporidian infections

  • 1.

    Valkiunas, G. Avian malaria parasites and other Haemosporidia. (CRC Press, 2005).

  • 2.

    Work, T. M. & Rameyer, R. A. Haemoproteus iwa n. sp. in Great Frigatebirds (Fregata minor [Gmelin]) from Hawaii: Parasite morphology and prevalence. J. Parasitol. 82, 489–491 (1996).

  • 3.

    Padilla, L. R. et al. Health Assesment of seabirds on Isla Genovesa, Galapagos Islands. Ornithol. Monogr. 86–97 (2006).

  • 4.

    Levin, I. I. & Parker, P. G. Prevalence of Hemoproteus iwa in Galapagos Great Frigatebirds (Fregata minor) and their obligate fly ectoparasite (Olfersia spinifera). J. Parasitol. 98, 924–929 (2012).

    • PubMed
    • Google Scholar
  • 5.

    Ortego, J., Cordero, P. J., Aparicio, J. M. & Calabuig, G. Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni). J. Ornithol. 149, 337–343 (2008).

    • Google Scholar
  • 6.

    Knowles, S. C. L., Palinauskas, V. & Sheldon, B. C. Chronic malaria infections increase family inequalities and reduce parental fitness: Experimental evidence from a wild bird population. J. Evol. Biol. 23, 557–569 (2010).

  • 7.

    Atkinson, C. T., Woods, K. L., Dusek, R. J., Sileo, L. S. & Iko, W. M. Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111, S59–S69 (1995).

    • PubMed
    • Google Scholar
  • 8.

    Atkinson, C. T., Dusek, R. J., Woods, K. L. & Iko, W. M. Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J. Wildl. Dis. 36, 197–204 (2000).

  • 9.

    Hamilton, W. D. & Zuk, M. Heritable true fitness and bright birds: A role for parasites? Science (80-.). 218, 384–387 (1982).

  • 10.

    Scott, M. E. The impact of infection and disease on animal populations: Implications for conservation biology. Conserv. Biol. 2, 40–56 (1988).

    • Google Scholar
  • 11.

    Spencer, K. A., Buchanan, K. L., Leitner, S., Goldsmith, A. R. & Catchpole, C. K. Parasites affect song complexity and neural development in a songbird. Proc. R. Soc. B Biol. Sci. 272, 2037–2043 (2005).

    • Google Scholar
  • 12.

    Asghar, M. et al. Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds. Science (80-.). 347, 436–438 (2015).

  • 13.

    Lapointe, D. A., Atkinson, C. T. & Samuel, M. D. Ecology and conservation biology of avian malaria. Ann. N. Y. Acad. Sci. 1249, 211–226 (2012).

  • 14.

    Norris, K., Anwar, M. & Read, A. F. Reproductive effort influences the prevalence of Haematozoan parasites in Great Tits. J. Anim. Ecol. 63, 601–610 (1994).

    • Google Scholar
  • 15.

    Calero-Riestra, M. & García, J. T. Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the Tawny pipit, Anthus campestris. Malar. J. 15, 1–11 (2016).

    • Google Scholar
  • 16.

    Carlson, M. L., Proudfoot, G. A., Gentile, K., Dispoto, J. & Weckstein, J. D. Haemosporidian prevalence in northern saw-whet owls Aegolius acadicus is predicted by host age and average annual temperature at breeding grounds. J. Avian Biol. 49, 1–11 (2018).

    • Google Scholar
  • 17.

    Hasselquist, D., Östman, Ö., Waldenström, J. & Bensch, S. Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. J. Ornithol. 148, 401–409 (2007).

    • Google Scholar
  • 18.

    Ricklefs, R. E. et al. Community relationships of avian malaria parasites in southern Missouri. Ecol. Monogr. 75, 543–559 (2005).

    • Google Scholar
  • 19.

    Sol, D., Jovani, R. & Torres, J. Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography (Cop.). 23, 307–314 (2000).

    • Google Scholar
  • 20.

    Shurulinkov, P., Chakarov, N. & Daskalova, G. Blood parasites, body condition, and wing length in two subspecies of Yellow Wagtail (Motacilla flava) during migration. Parasitol. Res. 110, 2043–2051 (2012).

    • PubMed
    • Google Scholar
  • 21.

    Zuk, M. & McKean, K. A. Sex differences in parasite infections: Patterns and processes. Int. J. Parasitol. 26, 1009–1024 (1996).

  • 22.

    Drobney, R. D., Train, C. T. & Fredrickson, L. H. Dynamics of the platyhelminth fauna of wood ducks in relation to food habits and reproductive state. J. Parasitol. 69, 375–380 (1983).

  • 23.

    Tinsley, R. C. The effects of host sex on transmission sucess. Parasitol. Today 5, 190–195 (1989).

  • 24.

    Richner, H., Christe, P. & Oppliger, A. Paternal investment affects prevalence of malaria. Proc. Natl. Acad. Sci. USA 92, 1192–4 (1995).

  • 25.

    Hegner, R. E. & Wingfield, J. C. Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male House Sparrows. Auk 104, 462–469 (1987).

    • Google Scholar
  • 26.

    Ardia, D. R. Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J. Anim. Ecol. 74, 517–524 (2005).

    • Google Scholar
  • 27.

    Bensch, S. et al. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc. R. Soc. B 267, 1583–1589 (2000).

  • 28.

    Hellgren, O., Waldenström, J. & Bensch, S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J. Parasitol. 90, 797–802 (2004).

  • 29.

    Waldenström, J., Bensch, S., Hasselquist, D. & Östman, Ö. A new Nested Polymerase Chain Reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J. Parasitol. 90, 191–194 (2004).

    • PubMed
    • Google Scholar
  • 30.

    Bensch, S., Hellgren, O. & Pérez-Tris, J. 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 (2009).

    • PubMed
    • Google Scholar
  • 31.

    Beadell, J. S. et al. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol. Ecol. 13, 3829–3844 (2004).

    • PubMed
    • Google Scholar
  • 32.

    Hellgren, O., Pérez-Triz, J. & Bensch, S. A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849 (2009).

    • PubMed
    • Google Scholar
  • 33.

    Fallon, A. S. M., Ricklefs, R. E., Swanson, B. L. & Bermingham, E. Detecting avian malaria: an improved Polymerase Chain Reaction diagnostic. J. Parasitol. 89, 1044–1047 (2003).

  • 34.

    Fallon, S. M., Fleischer, R. C. & Graves, G. R. Malarial parasites as geographical markers in migratory birds? Biol. Lett. 2, 213–216 (2006).

    • Google Scholar
  • 35.

    Fallon, S. M. & Ricklefs, R. E. Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. J. Avian Biol. 39, 514–522 (2008).

    • Google Scholar
  • 36.

    Svensson-Coelho, M. et al. Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western Amazon assemblage. Ornithol. Monogr. 76, 1–47 (2013).

    • Google Scholar
  • 37.

    Lo, E. et al. Low parasitemia in submicroscopic infections significantly impacts malaria diagnostic sensitivity in the highlands of Western Kenya. 1–15, https://doi.org/10.1371/journal.pone.0121763 (2015).

  • 38.

    Jarvi, S. I., Schultz, J. J. & Atkinson, C. T. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J. Parasitol. 88, 153–158 (2002).

    • PubMed
    • Google Scholar
  • 39.

    Freed, L. A. & Cann, R. L. On Polymerase Chain Reaction tests for estimating prevalence of malaria in birds. J. Exp. Biol. 89, 1261–1264 (2003).

    • CAS
    • Google Scholar
  • 40.

    Freed, L. A. & Cann, R. L. DNA Quality and accuracy of avian malaria PCR diagnostics: A review. Condor 108, 459–473 (2006).

    • Google Scholar
  • 41.

    Cornet, S. & Sorci, G. Avian malaria models of disease. Encycl. Malar. 1–11, https://doi.org/10.1007/978-1-4614-8757-9 (2014).

  • 42.

    Zuk, M. Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol. Today 6, 231–233 (1990).

  • 43.

    Harder, A., Wunderlich, F. & Marinovski, P. Effects of testosterone on Heterakis spumosa infections in mice. Parasitology 105, 335–342 (1992).

  • 44.

    Hughes, V. L. & Randolph, S. E. Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. J. Parasitol. 87, 49–54 (2001).

  • 45.

    Evans, M. R., Goldsmith, A. R. & Norris, S. R. A. The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 47, 156–163 (2000).

    • Google Scholar
  • 46.

    Asghar, M., Hasselquist, D. & Bensch, S. Are chronic avian haemosporidian infections costly in wild birds? J. Avian Biol. 42, 530–537 (2011).

    • Google Scholar
  • 47.

    Bentz, S. et al. Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Parasitology 133, 685–692 (2006).

  • 48.

    Nichols, J. D., Hines, J. E., Mackenzie, D. I., Seamans, M. E. & Gutiérrez, R. J. Occupancy estimation and modeling with multiple states and state uncertainty. Ecol. Soc. Am. 88, 1395–1400 (2007).

    • Google Scholar
  • 49.

    Ayadi, T. et al. Diversity, prevalence and host specificity of avian parasites in southern Tunisian oases. Parasitology 1–8, https://doi.org/10.1017/S0031182017002141 (2017).

  • 50.

    Bennett, G. F., Bishop, M. A. & Peirce, M. A. Checklist of the avian species of Plasmodium Marchiafava & Celli, 1885 (Apicomplexa) and their distribution by avian family and Wallacean life zones. Syst. Parasitol. 26, 171–179 (1993).

    • Google Scholar
  • 51.

    Atkinson, C. T. & Van Riper, C. III in Bird-Parasite Interactions: Ecology, evolution, and behaviour (eds. Loye, J. E. & Zuk, M.) 19–48 (Oxford University Press, 1991).

  • 52.

    Poulin, R. Sexual inequalities in helminth infections: a cost of being a male? Am. Nat. 147, 287–295 (1996).

    • Google Scholar
  • 53.

    Deerenberg, C., Arpanius, V., Daan, S. & Bos, N. Reproductive effort decreases antibody responsiveness. Proc. R. Soc. London B 264, 1021–1029 (1997).

    • ADS
    • Google Scholar
  • 54.

    Fischer, J., Jung, N., Robinson, N. & Lehmann, C. Sex differences in immune responses to infectious diseases. Infection 43, 399–403 (2015).

  • 55.

    Valkiūnas, G. et al. Nested cytochrome b Polymerase Chain Reaction diagnostics underestimate mixed infections of avian blood Haemosporidian parasites: microscopy is still essential. J. Parasitol 92, 418–422 (2006).

    • PubMed
    • Google Scholar
  • 56.

    Martínez, J. et al. A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitolo 136, 713–722 (2009).

    • Google Scholar
  • 57.

    Valkiūnas, G. et al. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J. Parasitol. 94, 1395–1401 (2008).

    • PubMed
    • Google Scholar
  • 58.

    Garamszegi, L. Z. The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds. J. pa 96, 1197–1203 (2010).

    • Google Scholar
  • 59.

    Bell, J. A., Weckstein, J. D., Fecchio, A. & Tkach, V. V. A new real-time PCR protocol for detection of avian haemosporidians. Parasit. Vectors 8, 1–9 (2015).

    • CAS
    • Google Scholar
  • 60.

    Rooyen, J. V., Lalubin, F., Glaizot, O. & Christe, P. Avian haemosporidian persistence and co-infection in great tits at the individual level. Malar. J. 12, 1–8 (2013).

    • Google Scholar
  • 61.

    Knowles, S. C. L. et al. Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol. Ecol. 20, 1062–1076 (2011).

    • PubMed
    • Google Scholar
  • 62.

    Biedrzycka, A., Migalska, M. & Bielanski, W. A quantitative PCR protocol for detecting specific Haemoproteus lineages: molecular characterization of blood parasites in a Sedge Warbler population from southern Poland. J. Ornithol. 156, 201–208 (2015).

    • Google Scholar
  • 63.

    Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C. & Qvarnström, A. Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos. Trans. R. Soc. B Biol. Sci. 346, 323–331 (1994).

  • 64.

    Patz, J. A., Graczyk, T. K., Geller, N. & Vittor, A. Y. Effects of environmental change on emerging parasitic diseases. Int. J. Parasitol. 30, 1395–1405 (2000).

  • 65.

    Beier, J. C. Malaria Parasite Development in Mosquitoes. Annu. Rev. Entomol. 43, 519–543 (1998).

  • 66.

    Schrader, M. S., Walters, E. L., James, F. C. & Greiner, E. C. Seasonal prevalence of a haematozoan parasite of Red-Bellied Woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival. Auk 120, 130–137 (2003).

    • Google Scholar
  • 67.

    Cosgrove, C. L., Wood, M. J., Day, K. P. & Sheldon, B. C. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J. Anim. Ecol. 77, 540–548 (2008).

    • PubMed
    • Google Scholar
  • 68.

    Fecchio, A. et al. Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae). Parasitology 144, 984–993 (2017).

  • 69.

    Sigrist, T. Guia de campo Avis Brasilis – Avifauna brasileira. (Avis Brasilis, 2014).

  • 70.

    del Hoyo, J., Elliott, A. & Christie, D. A. Handbook of the birds of the world alive. Volume 16 -Tanagers to new world blackbirds (Lynx Edicions, 2011).

  • 71.

    Macario, P. et al. Apparent survival and cost of reproduction for White-lined Tanager (Tachyphonus rufus, Thraupidae) in the northern Atlantic Rainforest, Brazil. PLoS One 12, 1–13 (2017).

    • Google Scholar
  • 72.

    Alvares, C. A. et al. Köppen’s climate classification map for Brazil. Meteorol. Zeitschrift 22, 711–728 (2014).

    • ADS
    • Google Scholar
  • 73.

    Sambrook, J. & Russell, D. W. Molecular cloning: a laboratory manual. (Cold Spring Harbor Laboratory Press, 2001).

  • 74.

    Bensch, S., Pérez-Tris, J., Waldenström, J. & Hellgren, O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution (N. Y). 58, 1617–1621 (2004).

    • CAS
    • Google Scholar
  • 75.

    Outlaw, D. C. & Ricklefs, R. E. Species limits in avian malaria parasites (Haemosporida): How to move forward in the molecular era. Parasitology 141, 1223–1232 (2014).

    • PubMed
    • Google Scholar
  • 76.

    White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46 (Supple, S120-139 (1999).

  • 77.

    Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: A practical information-theoretical approach. 172, (Springer, 2002).

  • 78.

    Lebreton, J.-D., Burnham, K. P., Clobert, J. & David, R. A. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol. Monogr. 62, 67–118 (1992).

    • Google Scholar

  • Source: Ecology - nature.com

    Towable sensor free-falls to measure vertical slices of ocean conditions

    The quest for practical fusion energy sources