The endangered California Condor (Gymnogyps californianus) population is exposed to local haemosporidian parasites

Snyder, N. & Snyder, H. The California Condor: A Saga of Natural History and Conservation (Academic Press, San Diego, 2000).

Google Scholar 

Emslie, S. D. Age and diet of fossil California Condors in Grand Canyon, Arizona. Science 237, 768–770. https://doi.org/10.1126/science.237.4816.768 (1987).

ADS  CAS  Article  PubMed  Google Scholar 

Mee, A. & Snyder, N.F.R. California Condors in the 21st century-Conservation problems and solutions (eds. Mee, A. & Hall, L.S. & Grantham, J.). California Condors in the 21st Century. 243–272 (Series in Ornithology, no. 2. American Ornithologists’ Union and Nuttall Ornithological Club, Washington, DC, 2007).

Parish, C.N., Heinrich, W.R. & Hunt, W.G. Lead exposure, diagnosis, and treatment in California Condors released in Arizona, (eds. Mee, A. & Hall, L.S. & Grantham, J.). California Condors in the 21st Century. 97–108 (Series in Ornithology, no. 2. American Ornithologists’ Union and Nuttall Ornithological Club,Washington, DC, 2007).

Brandt, J. & Astell, M. California Condor Recovery Program 2017 Annual Report (eds. Weprin, N., Cook, D. & Ledig, D.). 1–62. (Hopper Mountain National Wildlife Refuge Complex. US Fish and Wildlife Service, Ventura, CA, 2019).

Parish, C.N., Hunt, W.G., Feltes, E., Sieg, R. & Orr., K. Lead exposure among a reintroduced population of California Condors in northern Arizona and southern Utah (eds. Watson, R.T., Fuller, M., Pokras & M., Hunt, W.G.). Ingestion of lead from spent ammunition: Implications for wildlife and humans. 259–264. (The Peregrine Fund, Boise, Idaho, 2009). DOI https://doi.org/10.4080/ilsa.2009.0217.

Koford, C. B. The California Condor. Nat. Audubon Res. Rep. 4, 1–154 (1953).

Google Scholar 

Wilbur, S.R. The California Condor, 1966–76: a look at its past and future. U. S. Fish & Wildlife Service North American Fauna 72, 1–136 (1978).

D’Elia, J., Haig, S. M., Mullins, T. D. & Miller, M. P. Ancient DNA reveals substantial genetic diversity in the California Condor (Gymnogyps californianus) prior to a population bottleneck. Condor 118, 703–714. https://doi.org/10.1650/CONDOR-16-35.1 (2016).

Article  Google Scholar 

Ralls, K., Ballou, J. D., Rideout, B. A. & Frankham, R. Genetic management of chondrodystrophy in California Condors. Anim. Conserv. 3, 145–153. https://doi.org/10.1111/j.1469-1795.2000.tb00239.x (2000).

Article  Google Scholar 

Ralls, K. & Ballou, J. D. Genetic status and management of California Condors. Condor 106, 215–228 (2004).

Article  Google Scholar 

Aguilar, R. F., Yoshicedo, J. N. & Parish, C. N. Ingluviotomy tube placement for lead-induced crop stasis in the California condor (Gymnogyps californianus). J. Avian Med. Surg. 26, 176–181. https://doi.org/10.1647/2010-029R2.1 (2012).

Article  PubMed  Google Scholar 

Plaza, P. I. & Lambertucci, S. A. What do we know about lead contamination in wild vultures and condors? A review of decades of research. Sci. Total. Environ. 654, 409–417. https://doi.org/10.1016/j.scitotenv.2018.11.099 (2019).

ADS  CAS  Article  PubMed  Google Scholar 

Cade, T.J., Osborn, S.A.H., Hunt & W.G., Woods, C.P. Commentary on released California Condors Gymnogyps californianus in Arizona, (eds. Chancellor, R.D. & Meyburg, B.U.). Raptors worldwide: Proceedings of the VI world conference on birds of prey and owls. 11–25. (World Working Group on Birds of Prey and Owls/MME-Birdlife 11–25, Hungary, 2004).

Hunt, W. G., Parish, C. N., Orr, K. & Aguilar, R. F. Lead poisoning and the reintroduction of the California condor in northern Arizona. J. Avian Med. Surg. 23, 145–150. https://doi.org/10.1647/2007-035.1 (2009).

Article  PubMed  Google Scholar 

Richner, H., Christe, P. & Opplinger, A. Paternal investment affects prevalence of malaria. Proc. Natl. Acad. Sci. USA 92, 1192–1194. https://doi.org/10.1073/pnas.92.4.1192 (1995).

ADS  CAS  Article  PubMed  Google Scholar 

Forrester, D.J. & Spalding, M.G. Parasites and diseases of wild birds in Florida. (University Press of Florida, 2003).

Webb, S. L., Fedynich, A. M., Yeltatzie, S. K., De Vault, T. L. & Rhodes, O. E. Jr. Survey of blood parasites in black vultures and turkey vultures from South Carolina. Southeast Nat. 4, 355–360 (2005).

Article  Google Scholar 

Greiner, E. C., Fedynich, A. M., Webb, S. L., DeVault, T. L. & Rhodes, O. E. Jr. Hematozoa and a new haemoproteid species from Cathartidae (New World Vulture) in South Carolina. J Parasitol. 97, 1137–1139. https://doi.org/10.1645/GE-2332.1 (2011).

Article  PubMed  Google Scholar 

Yabsley, M. J. et al. Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida. Malar J. 17, 12. https://doi.org/10.1186/s12936-017-2165-5 (2018).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Wetmore, P. W. Blood parasites of birds of the District of Columbia and Patuxent Research Refuge vicinity. J. Parasitol. 27, 379–393 (1941).

Article  Google Scholar 

Love, G. J., Wilkin, S. A. & Goodwin, M. H. Incidence of blood parasites in birds collected in southwestern Georgia. J. Parasitol. 39, 52–57 (1953).

CAS  Article  Google Scholar 

Halpern, N. & Bennett, G. F. Haemoproteus and Leucocytozoon infections in birds of the Oklahoma City Zoo. J. Wildl. Dis. 19, 330–332 (1983).

CAS  Article  Google Scholar 

Wahl, M. Blood-borne parasites in the Black Vulture Coragyps atratus in northwestern Costa Rica. Vulture News. 64, 21–30 (2013).

Google Scholar 

Chagas, C. R. F. et al. Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar J. 16, 83. https://doi.org/10.1186/s12936-017-1729-8 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Walther, E. L. et al. Description, molecular characterization, and patterns of distribution of a widespread New World avian malaria parasite (Haemosporida: Plasmodiidae), Plasmodium (Novyella) homopolare sp. nov. Parasitol. Res. 113, 3319–3332. https://doi.org/10.1007/s00436-014-3995-5 (2014).

Article  PubMed  Google Scholar 

Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 125, 3389–3402. https://doi.org/10.1093/nar/25.17.3389 (1997).

Article  Google Scholar 

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. https://doi.org/10.1111/j.1755-0998.2009.02692.x (2009).

Article  PubMed  Google Scholar 

Walther, E. L. et al. First molecular study of prevalence and diversity of avian haemosporidia in a Central California songbird community. J. Ornithol. 157, 549–564 (2016).

Article  Google Scholar 

Pacheco, M. A., Escalante, A. A., Garner, M. M., Bradley, G. A. & Aguilar, R. F. Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail. Vet. Parasitol. 182, 113–120. https://doi.org/10.1016/j.vetpar.2011.06.006 (2011).

Article  PubMed  PubMed Central  Google Scholar 

Ishak, H. D. et al. Blood parasites in owls with conservation implications for the Spotted Owl (Strix occidentalis). PLoS ONE 3, e2304. https://doi.org/10.1371/journal.pone.0002304 (2008).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Remple, J. D. Intracellular hematozoa of raptors: a review and update. J. Avian Med. Surg. 18, 75–88 (2004).

Article  Google Scholar 

Valkiunas, G. & Iezhova, T. A. Keys to the avian malaria parasites. Malar. J. 17, 212. https://doi.org/10.1186/s12936-018-2359-5 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Gonzalez-Serrano, P., et al. Climate change and risks for mountain species. Mosquito vectors and circulation of West Nile virus and avian malaria in territories of Bearded vultures (Gypaetus barbatus). First Iberian Congress of Applied Science on Game Resources (CICARC) Ciudad Real, (Spain, 1–4 July 2019).

Garnham, P. C. C. Malaria parasites and other Haemosporidia (Blackwell Scientific Publications, Oxford, 1966).

Google Scholar 

Valkiunas, G. Avian Malaria Parasites and Other Haemosporidia (CRC Press, New York, 2005).

Google Scholar 

Atkinson, C. T. & Samuel, M. D. Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on ‘apapane Himatione sanguinea. J. Avian Biol. 41, 357–366 (2010).

Article  Google Scholar 

Cornet, S., Nicot, A., Rivero, A. & Gandon, S. Evolution of plastic transmission strategies in avian malaria. PLoS Pathog. 10(9), e1004308. https://doi.org/10.1371/journal.ppat.1004308 (2014).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Pacheco, M. A. et al. Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int. J. Parasitol. 48, 657–670. https://doi.org/10.1016/j.ijpara.2018.02.003 (2018).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Smith, K. F., Sax, D. F. & Lafferty, K. D. Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20, 1349–1357. https://doi.org/10.1111/j.1523-1739.2006.00524.x (2006).

Article  PubMed  Google Scholar 

Mace, M.E. California Condor (Gymnogyps californianus) international studbook. (Zoological Society of San Diego, San Diego Wild Animal Park, Escondido, California, 2005).

Pacheco, M. A., García-Amado, M. A., Manzano, J., Matta, N. E. & Escalante, A. A. Blood parasites infecting the Hoatzin (Opisthocomus hoazin), a unique neotropical folivorous bird. PeerJ 7, e6361. https://doi.org/10.7717/peerj.6361 (2019).

Article  PubMed  PubMed Central  Google Scholar 

Gouy, M., Guindon, S. & Gascuel, O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 272, 221–224. https://doi.org/10.1093/molbev/msp259 (2010).

CAS  Article  Google Scholar 

Pacheco, M. A. et al. Mode and rate of evolution of haemosporidian mitochondrial genomes: Timing the radiation of avian parasites. Mol. Biol. Evol. 35, 383–403. https://doi.org/10.1098/rstb.2015.0128 (2018).

CAS  Article  PubMed  Google Scholar 

Benson, D. A. et al. GenBank. Nucl. Acids Res. 41, D36–D42. https://doi.org/10.1093/nar/gks1195 (2012).

CAS  Article  PubMed  Google Scholar 

Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 1912, 1572–1574. https://doi.org/10.1093/bioinformatics/btg180 (2003).

CAS  Article  Google Scholar 

Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874. https://doi.org/10.1093/molbev/msw054 (2016).

CAS  Article  Google Scholar