Introduced vector-borne diseases, particularly avian malaria (Plasmodium relictum) and avian pox virus (Avipoxvirus spp.), continue to play significant roles in the decline and extinction of native forest birds in the Hawaiian Islands. Hawaiian honeycreepers are particularly susceptible to avian malaria and have survived into this century largely because of persistence of high elevation refugia on Kaua‘i, Maui, and Hawai‘i Islands, where transmission is limited by cool temperatures. The long term stability of these refugia is increasingly threatened by warming trends associated with global climate change. Since cost effective and practical methods of vector control in many of these remote, rugged areas are lacking, adaptation through processes of natural selection may be the best long-term hope for recovery of many of these species. We document emergence of tolerance rather than resistance to avian malaria in a recent, rapidly expanding low elevation population of Hawai‘i ‘Amakihi (Hemignathus virens) on the island of Hawai‘i. Experimentally infected low elevation birds had lower mortality, lower reticulocyte counts during recovery from acute infection, lower weight loss, and no declines in food consumption relative to experimentally infected high elevation Hawai‘i ‘Amakihi in spite of similar intensities of infection. Emergence of this population provides an exceptional opportunity for determining physiological mechanisms and genetic markers associated with malaria tolerance that can be used to evaluate whether other, more threatened species have the capacity to adapt to this disease.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Atkinson CT, Dusek RJ, Lease JK (2001) Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 37:20–27
Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases 36:197–204
Atkinson CT, Lease JK, Dusek RJ, Samuel MD (2005) Prevalence of pox-like lesions and malaria in forest bird communities on leeward Mauna Loa Volcano, Hawaii. Condor 107:537–546
Atkinson CT, Paxton EH (2013) Immunological markers for tolerance to avian malaria in Hawai‘i ‘Amakihi: new tools for restoring native Hawaiian forest birds? Hawai‘i Cooperative Studies Unit, University of Hawai‘i at Hilo, Hawaii Cooperative Studies Unit Technical Report HCSU-042. http://hilo.hawaii.edu/hcsu/documents/TR042_Atkinson_Immunologicalmarkers.pdf. Accessed 13 Jan 2014
Atkinson CT, Woods KL, Dusek RJ, Sileo LS, Iko WM (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111:S59–S69
Ayres JS, Freitag N, Schneider DS (2008) Identification of Drosophila mutants altering defense of and endurance to Listeria monocytogenes infection. Genetics 178:1807–1815
Ayres JS, Schneider DS (2008) A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biology 6:2764–2773
Ayres JS, Schneider DS (2009) The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biology 7:e1000150. doi:10.1371/journal.pbio.1000150
Banko WE, Banko PC (2009) Historic decline and extinction. In: Conservation Biology of Hawaiian Forest Birds: Implications for Island Avifauna, Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (editors), New Haven: Yale University Press, pp 25–58
Benning TL, LaPointe DA, Atkinson CT, Vitousek PM (2002) Interactions of climate change with land use and biological invasions in the Hawaiian Islands: modeling the fate of endemic birds using GIS. Proceedings of the National Academy of Sciences 99:14246–14249
Bichet C, Cornet S, Larcombe S, Sorci G (2012) Experimental inhibition of nitric oxide increases Plasmodium relictum (lineage SGS1) parasitaemia. Experimental Parasitology 132:417–423
Bonneaud C, Perez-Tris J, Federici P, Chastel O, Sorci G (2006) Mhc alleles confer local resistance to malaria in a wild passerine. Evolution 60:383–389.
Cann RL, Douglas LJ (1999) Parasites and conservation of Hawaiian birds. In: Genetics and the Extinction of Species, Landweber LF, Dobson AP (editors), Princeton, NJ: Princeton University Press, pp 121–136
Christe P, Glaizot O, Strepparava N, Devevey G, Fumagalli L (2012) Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitemia and to a decrease in resistance to oxidative stress. Proceedings of the Royal Society B 279:1142–1149
Eggert LS, Terwilliger LA, Woodworth BL, Hart PJ, Palmer D, Fleischer RC (2008) Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria. BMC Evolutionary Biology 8:315
Foster JT, Woodworth BL, Eggert LE, Hart PJ, Palmer D, Duffy DC, Fleischer RC (2007) Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Molecular Ecology 16:4738–4746
Gering E, Atkinson CT (2004) A rapid method for counting nucleated erythrocytes on stained blood smears by digital image analysis. Journal of Parasitology 90:879–881
Gorresen PM, Camp RJ, Reynolds MH, Woodworth BL, Pratt TK (2009) Status and trends of native Hawaiian songbirds. In: Conservation Biology of Hawaiian Forest Birds: Implications for Island Avifauna, Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (editors), New Haven: Yale University Press, pp 108–136
Graczyk TK, Cranfield MR, Shiff CJ (1993) ELISA method for detecting anti-Plasmodium relictum and anti-Plasmodium elongatum antibody in infected duckling sera using Plasmodium falciparum antigens. Journal of Parasitology 79:879–885
Graham AL, Allen JE, Read AF (2005) Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution and Systematics 36:373–397
Grueber CE, Wallis GP, King TM, Jamieson IG (2012) Variation at innate immunity Toll-like receptor genes in a bottlenecked population of a New Zealand Robin. PLoS ONE 7:e45011. doi:10.1371/journal.pone.0045011
Hellgren O, Sheldon BC (2011) Locus-specific protocol for nine different innate immune genes (antimicrobioal peptides: β-defensins) across passerine bird species reveals within-species coding variation and a case of trans-species polymorphisms. Molecular Ecology Resources 11:686–692
Jarvi SI, Atkinson CT, Fleischer RC (2001) Immunogenetics and resistance to avian malaria (Plasmodium relictum) in Hawaiian Honeycreepers (Drepanidinae). Studies in Avian Biology 22:254–263
Jarvi SI, Tarr CL, McIntosh CE, Atkinson CT, Fleishcer RC (2004) Natural selection of the major histocompatibility complex (Mhc) in Hawaiian honeycreepers (Drepanidinae). Molecular Ecology 13:2157–2168
Kilpatrick AM (2006) Facilitating the evolution of resistance to avian malaria in Hawaiian birds. Biological Conservation 128:475–485
Kilpatrick AM, LaPointe DA, Atkinson CA, Woodworth BL, Lease JK, Reiter ME, Gross K (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). The Auk 123:764–774
Klein A, Hart P, Stumpf K, Tweed E, Henneman C, Spiegel C, LeBrun J, McClure K, Woodworth B (2004) Nests of Amakihi near sea-level on Hawai‘i Island. Elepaio 63:67–68
Krend KL (2011) Avian malaria on Oahu: Disease ecology, population genetics, and the evolution of resistance in Oahu Amakihi. PhD Dissertation, University of Hawaii, Manoa
LaPointe DA, Goff ML, Atkinson CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawaii. Journal of Parasitology 96:318–324
Lerner HRL, Meyer M, James HF, Hofreiter M, and Fleischer RC (2011) Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Current Biology 21:1–7
Lindsey GD, Vander Werf EA, Baker H, and Baker PE (1998) Hawaii Amakihi (Hemignathus virens), The Birds of North America Online, Poole A (editor), Ithaca: Cornell Lab of Ornithology. http://bna.birds.cornell.edu/bna/species/360adoi:10.2173/bna.360
Nielsen BMB (2000) Nesting ecology of Apapane (Himationesanguinea). PhD Dissertation, University of Idaho, Moscow, ID
Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, Chora A, Rodrigues CD, Gregoire IP, Cunha-Rodrigues M, Portugal S, Soares MP, Mota MM (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nature Medicine 13:703–710
Peck RW, Banko PC, Schwarzfeld M, Euaparadorn M, Brinck KW (2008) Alien dominance of the parasitoid wasp community along an elevation gradient on Hawai’i Island. Biological Invasions 10:1441–1455
Pratt TK (2009) Origins and evolution. In: Conservation Biology of Hawaiian Forest Birds: Implications for Island Avifauna, Pratt TK, Atkinson CT, Banko PC, Jacobi JD, Woodworth BL (editors), New Haven: Yale University Press, pp 3–23
Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B 364:37–49
Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812–814
Read AF, Graham AL, Råberg L (2008) Animal defenses against infectious agents: is damage control more important than pathogen control? PLoS Biology 6:2638–2641.
Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63.
Samuel MD, Hobbelen PHF, DeCastro F, Ahumada JA, LaPointe DA, Atkinson CT, Woodworth BL, Hart PJ, Duffy DC (2011) The dynamics, transmission, and population impacts of avian malaria in native Hawaiian birds—an epidemiological modeling approach. Ecological Applications 21:2960–2973
Scott JM, van Riper III C (2001) Limiting factors affecting Hawaiian native birds. Studies in Avian Biology 22:221–233
Seixas E, Gozzelinoa R, Chora A, Ferreira A, Silva G, Larsen R, Rebelo S, Penido C, Smith N, Coutinho A, Soares MP (2009) Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proceedings of the National Academy of Science USA 106:15837–15842
Sepil I, Lachish S, Hinks AE, Sheldon BC (2013) Mhc supertypes confer both qualitative and quantitative resistance to avian malaria infection in a wild bird population. Proceedings of the Royal Society B 280:20130134
Shehata CL, Freed LA, Cann RL (2001) Changes in native and introduced bird populations on O‘ahu: infectious diseases and species replacement. Studies in Avian Biology 22:264–273
Spiegel CS, Hart PJ, Woodworth BL, Tweed EJ, LeBrun JJ (2006) Distribution and abundance of native forest birds in low-elevation areas on Hawai‘i Island: Evidence of range expansion. Bird Conservation International 16:175–185
Sorci G (2013) Immunity, resistance and tolerance in bird–parasite interactions. Parasite Immunology 35:350–361
Sorci G, Faivre B (2009) Inflammation and oxidative stress in vertebrate host–parasite systems. Philosophical Transactions of the Royal Society B 364:71–83
Steinberg MK, Sugishita J, Kinney KM (2010) Land-use changes and conservation of Hawai‘i ‘Amakihi. Geographical Review 100:204–215
Systat Software, Inc. (2004) Systat 11 Statistics. Systat Software, Inc., Richmond, CA.
Totino PRR, Magalhaes AS, Silva LA, Banic DM, Daniel-Ribeiro CT, Ferreira-da-Cruz MF (2010) Apoptosis of non-parasitized red blood cells in malaria: a putative mechanism involved in the pathogenesis of anaemia. Malaria Journal 9:350
U.S. Fish and Wildlife Service (2006) Revised Recovery Plan for Hawaiian Forest Birds. Portland, OR: U.S. Fish and Wildlife Service, Region 1
U.S. Fish and Wildlife Service (2010) 50 CFR Part 17, Endangered and Threatened Wildlife and Plants; Determination of Endangered Status for 48 Species on Kauai and Designation of Critical Habitat; Final Rule. Federal Register 75:18960–19165
Vander Werf EA, Burt MD, Rohrer JL, Mosher SM (2006) Distribution and prevalence of mosquito-borne diseases in O‘ahu‘Elepaio. The Condor 108:770–777
Vander Werf EA, Rohrer JL (1996) Discovery of an ‘I‘iwi population in the Ko‘olau Mountains of O‘ahu. Elepaio 56:25–28
van Riper C III, Atkinson CT, Seed TM (1994) Plasmodia of Birds. In: Parasitic Protozoa, vol 7, Kreier JP (editor), San Diego, CA: Academic Press, pp 73–140.
van Riper C III, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56:327–344.
Verra F, Mangano VD, Modiano D (2009) Genetics of susceptibility to Plasmodium falciparum: from classical malaria resistance genes towards genome-wide association studies. Parasite Immunology 31:234–253
Warner RE (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70:101–120
Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proceedings of the National Academy of Sciences 102:1531–1536.
We thank numerous former interns for assistance with capture and care of experimental birds, Amy Savage and Christy Wykoff for technical assistance caring for birds and collecting data during the experiment, and Kathy Jurist and Leayne Patch-Highfill for assistance with data summary and analysis. This project was funded by the U.S. Geological Survey Wildlife and Terrestrial Resources Program and NSF Grant DEB 0083944. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Rights and permissions
About this article
Cite this article
Atkinson, C.T., Saili, K.S., Utzurrum, R.B. et al. Experimental Evidence for Evolved Tolerance to Avian Malaria in a Wild Population of Low Elevation Hawai‘i ‘Amakihi (Hemignathus virens). EcoHealth 10, 366–375 (2013). https://doi.org/10.1007/s10393-013-0899-2
- avian malaria
- Hawai‘i ‘Amakihi
- Plasmodium relictum
- climate change