Ecological correlates of microfilariae prevalence in endangered galpagos birds

Journal of Parasitology

Volumn 96, Issue 2, 2010, Pages 259-272

  Siers, Shane ^a,b   Merkel, Jane ^a,c   Bataille, Arnaud ^a,d,e   Vargas, F H ^a,f,g,h   Parker, P G ^a,c  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^b USGS Brown Treesnake Project   (Guam)

^c SAINT LOUIS ZOO   (United States)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e INSTITUTE OF ZOOLOGY   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g Charles Darwin Foundation   (Ecuador)

^h THE PEREGRINE FUND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD; BIRD; CLIMATE VARIATION; CORRELATION; DISEASE TRANSMISSION; DISEASE VECTOR; ENDANGERED SPECIES; FLIGHTLESSNESS; PARASITE PREVALENCE; RISK FACTOR; SATELLITE SENSOR; WEATHER STATION; WILD POPULATION;

AEDES; AEDES TAENIORHYNCHUS; ARTICLE; BIRD DISEASE; CORRELATION ANALYSIS; ECOLOGY; GEOGRAPHIC DISTRIBUTION; MICROFILARIASIS; NONHUMAN; PARASITE TRANSMISSION; PARASITE VECTOR; PENGUIN; PHALACROCORAX HARRISI; PREDICTION; PREVALENCE; SPHENISCUS MENDICULUS;

AEDES; ANIMALS; BIRD DISEASES; BIRDS; ECUADOR; FILARIASIS; FILARIOIDEA; INSECT VECTORS; MICROFILARIA; PREVALENCE; SPHENISCIDAE;

AEDES TAENIORHYNCHUS; ARTHROPODA; AVES; PHALACROCORACIDAE; PHALACROCORAX HARRISI; SPHENISCIDAE; SPHENISCUS MENDICULUS;

EID: 77953582284     PISSN: 00223395     EISSN: None     Source Type: Journal    
DOI: 10.1645/GE-2070.1     Document Type: Article

References (77)

1. ADLER, P. H. 2005. Black flies, the Simuliidae. In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 127-140.
2. AMARAKOON, D., A. CHEN, S. RAWLINS, D. D. CHADEE, M. TAYLOR, AND R. STENNETT. 2008. Dengue epidemics in the Caribbean-temperature indices to gauge the potential for onset of dengue. Mitigation and Adaptation Strategies for Global Change 13: 341-357.
3. ANDERSON, J. D., AND S. FORTNER. 1988. Waved albatross egg neglect and associated mosquito ectoparasitism. Condor 90: 727-729.
4. ANDERSON, R. C. 2001. Filarioid nematodes. In Parasitic diseases of wild mammals, 2nd ed., W. M. Samuel, M. J. Pybus, and A. A. Kocan (eds.). Iowa State University Press, Ames, Iowa, p. 342-356.
5. ANYAMBA, A., K. J. LINTHICUM, R. MAHONEY, C. J. TUCKER, AND P. W. KELLEY. 1999. Mapping potential risk of rift valley fever outbreaks in African savannas using vegetation index time series data. Photogrammetric Engineering & Remote Sensing 68: 137-145.
6. ATKINSON, C. T., K. L. WOODS, R. J. DUsEK, L. SILEO, AND W. M. IKO. 1995. Wildlife disease and conservation in Hawaii: Pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected 'I'iwi (Vestiaria coccinea). Parasitology 111: S59-S69.
7. BARTHOLOMAY, L. C., AND B. M. CHRISTENSEN. 2002. Vector-parasite interactions in mosquito-borne filariasis. In The filaria, T. R. Klei and T. V. Rajan (eds.). Kluwer, Norwell, Massachusetts, p. 9-20.
8. BARTLETT, C. M. 2008. Filariod nematodes. In Parasitic diseases of wild birds, C. T. Atkinson, N. J. Thomas, and B. D. Hunter (eds.). Wiley-Blackwell, Ames, Iowa, p. 439-462.
9. BATAILLE, A., A. A. CUNNINGHAM, V. CEDENO, L. PATINO, A. CONSTANTINOU, L. D. KRAMER, AND S. J. GOODMAN. 2009. Natural colonization and adaptation of a mosquito species in Galápagos and its implications for disease threats to endemic wildlife. Proceedings of the National Academy of Sciences USA. Available online. DOI: 10.1073/PNAS.0901308106
10. BECK, L. R., B. M. LOBITZ, AND B. L. WOOD. 2000. Remote sensing and human health: New sensors and new opportunities. Emerging Infectious Diseases 6: 217-227.
11. BLACK, W. C., AND C. G. MOORE. 2005. Population biology as a tool to study vector-borne diseases. In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 187-206.
12. -, AND D. W. SEVERSON. 2005. Genetics of vector competence. In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 415-448.
13. BOLLMER, J. L., F. H. VARGAS, AND P. G. PARKER. 2007. Low MHC variation in the endangered Galápagos penguin (Spheniscus mendiculus). Immunogenetics 59: 593-602.
14. BOONE, J. D., K. C.MCGWIRE, E.W. OTTESON, R. S.DEBACA, E.A. KUHN, P. VILLARD, P. F. BRUSSARD, AND S. C. ST. JEOR. 2000. Remote sensing and geographic information systems: Charting sin nombre virus infections in deer mice. Emerging Infectious Diseases 6: 248-258.
15. BORKENT, A. 2005. The biting midges, the Ceratopogonidae (Diptera). In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 113-126.
16. BOUMA, M. J., AND H. J. VAN DER KAAY. 1996. The El Niño southern oscillation and the historic malaria epidemics on the Indian subcontinent and Sri Lanka: An early warning system for future epidemics? Tropical Medicine and International Health 1: 86-96.
17. BROOKER, S., S. I. HAY, W. ISSAE, A. HALL, C. M. KIHAMIA, N. J. S. LWAMBO, W. WINT, D. J. ROGERS, AND D. A. P. BUNDY. 2001. Predicting distribution of urinary schistosomiasis in Tanzania using satellite sensor data. Tropical Medicine and International Health 6: 998-1007.
18. CAUSTON, C. E., S. B. PECK, B. J. SINCLAIR, L. ROQUE-ALBELO, C. J. HODGSON, AND B. LANDRY. 2006. Alien insects: Threats and implications for conservation of the Galápagos Islands. Annals of the Entomological Society of America 99: 121-143.
19. CBSG. 2005. Galápagos penguin population and habitat viability assessment: Draft report. IUCN/SSC Conservation Breeding Specialists Group, Apple Valley, Minnesota, 169 p.
20. COOPER, J. E. 1989. Disease and threatened birds. BirdLife International, Cambridge, U.K., 200 p.
21. CORREIA, V. R. M., M. S. CARVALHO, P. C. SABROZA, AND C. H. VASCONCELOS. 2004. Remote sensing as a tool to survey endemic diseases in Brazil. Cadernos de Saúde Pública 20: 891-904.
22. CRIST, E. P., AND R. C. CICCONE. 1984. A physically-based transformation of Thematic Mapper data-the TM tasseled cap. IEEE Transactions on Geosciences and Remote Sensing 22: 256-263.
23. CROMBIE,M.K., R. R.GILLIES, R. E. ARVIDSON, P.BROOKMEYER, G. J.WEIL, M. SULTAN, AND M. HARB. 1999. An application of remotely derived climatological fields for risk assessment of vector-borne diseases: A spatial study of filariasis prevalence in the Nile Delta, Egypt. Photogrammetric Engineering & Remote Sensing 65: 1401-1409.
24. CURRAN, P. J., P. M. ATKINSON, G. M. FOODY, AND E. J. MILTON. 2000. Linking remote sensing, land cover and disease. Advances in Parasitology 47: 37-80.
25. DASZAK, P., A. A. CUNNINGHAM, AND A. D. HYATT. 2000. Emerging infectious diseases of wildlife-Threats to biodiversity and human health. Science 287: 443-449.
26. -2003. Infectious disease and amphibian population declines. Diversity & Distributions. 9:141-150.
27. DISTER, S. W., D. FISH, S.M. BROS, D.H. FRANK, AND B. L. WOOD. 1997. Landscape characterization of periodomestic risk for Lyme disease using satellite imagery. American Journal of Tropical Medicine and Hygiene. 57: 687-692.
28. DUFFIE, C. V., T. C. GLENN, F. H. VARGAS, AND P. G. PARKER. 2009. Genetic structure within and between island populations of the flightless cormorant (Phalacrocorax harrisi). Molecular Ecology 18: 2103-2111.
29. EARLE, R. A., F. W. HUCHZERMEYER, G. F. BENNETT, AND J. J. BROSSY. 1993. Babesia peircei sp. nov. from the Jackass penguin. South African Journal of Zoology 28: 88-90.
30. ECHOLS, M. S., T. M. CRAIG, AND B. L. SPEER. 2000. Heartworm (Paronchocerca ciconarum) infection in 2 saddle-billed storks (Ephippiorynchus senegalensis). Journal of Avian Medicine and Surgery 14: 42-47.
31. ELDRIDGE, B. F. 2005. Mosquitoes, the Culicidae. In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 95-112.
32. GAO, B., AND Y. J. KAUFMAN. 2003. Water vapor retrievals using Moderate Resolution Imaging Spectroradiometer (MODIS) nearinfrared channels. Journal of Geophysical Research 108: 4389.
33. GILLIES, R. R., AND T. N. CARLSON. 1995. Thermal remote sensing of surface soil water content with partial vegetation coverage for incorporation into climate models. Journal of Applied Meteorology 34: 745-756.
34. GULLAN, P. J., AND P. S. CRANSTON. 2005. The insects: An outline of entomology, 3rd ed. Blackwell, Malden, Massachusetts, 528 p.
35. HAY, S. I., J. A. OMUMBO, M. H. CRAIG, AND R. W. SNOW. 2000. Earth observation, geographic information systems and Plasmodium falciparum malaria in sub-Saharan Africa. Advances in Parasitology 47: 173-215.
36. -, E. C. WERE, M. RENSHAW, A. M. NOOR, S. A. OCHOLA, I. OLUSANMI, N. ALIPUI, AND R. W. SNOW. 2003. Forecasting, warning, and detection of malaria epidemics: A case study. Lancet 362: 580.
37. HIGGS, S., AND B. J. BEATY. 2005. Natural cycles of vector-borne pathogens. In Biology of disease vectors, W. C. Marquardt (ed.). Elsevier, Burlington, Massachusetts, p. 167-186.
38. HIJMANS, R. J., S. E. CAMERON, J. L. PARRA, P. G. JONES, AND A. JARVIS. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
39. HRIBAR, L. J., L. M. STARK, R. L. STONER, D. J.DEMAY, A. L.NORDHOLT, M. J. HEMMEN, J. J. VLACH, AND E. M. FUSSELL. 2004. Isolation of West Nile Virus from mosquitoes (Diptera: Culicidae) in the Florida Keys, Monroe County, Florida. Caribbean Journal of Science 40: 362-367.
40. HUANG, C., B. WYLIE, L. YANG, C. HOMER, AND G. ZYLSTRA. 2002. Derivation of a tasseled cap transformation based on Landsat 7 atsatellite reflectance. International Journal of Remote Sensing 23: 1741-1748.
41. IUCN. 2006. 2006 IUCN Red List of threatened species. Available at: www.iucnredlist.org. Accessed 08 May 2006.
42. KAUTH, R. J., AND G. S. THOMAS. 1976. The tasseled cap-A graphic description of the spectral-temporal development of agricultural crops as seen by LANDSAT. In Proceedings of the symposium on machine processing of remotely sensed data. Purdue University, West Lafayette, Indiana, p. 4B41-4B51.
43. KILPATRICK, A. M., P. DASZAK, S. J. GOODMAN, H. ROGG, L. D. KRAMER, V. CEDENO, AND A. A. CUNNINGHAM. 2006. Predicting pathogen introduction: West Nile virus spread in Galápagos. Conservation Biology 20: 1224-1231.
44. KING, M. D., J. CLOSS, S. SPANGLER, R. GREENSTONE, S. WHARTON, AND M. MYERS. 2004. EOS Data Products Handbook Vol. I. NASA/ Goddard Space Flight Center, Maryland.
45. KITRON, U., AND J. J. KAZMIERCZAK. 1997. Spatial analysis of the distribution of Lyme disease in Wisconsin. American Journal of Epidemiology 145: 558-566.
46. KORPIMAKI, E., P. TOLONEN, AND G. F. BENNETT. 1995. Blood parasites, sexual selection and reproductive success of European kestrels. Ecoscience 2: 335-343. (Pubitemid 3010531)
47. LABARTHE, N., M. L. SERRAO, Y. F. MELO, S. J. DE OLIVEIRA, AND R. LOURENÇO-DE OLIVERA. 1998. Potential vectors of Dirofilaria immitis (Leidy, 1856) in Itacoatiara, oceanic region of Niterói municipality, State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 93: 425-432.
48. LEVIN, I. I., D. C. OUTLAW, F. H. VARGAS, AND P. G. PARKER. 2009. Plasmodium blood parasite found in endangered Galápagos penguins (Spheniscus mendiculus). Biological Conservation. doi:10.1016/j. biocon.2009.06.017.
49. MERKEL, J., H. JONES, N. WHITEMAN, N. GOTTDENKER, H. VARGAS, E. TRAVIS, E.MILLER, AND P. PARKER. 2007. Microfilariae in Galápagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi): Genetics, morphology, and prevalence. Journal of Parasitology 93: 495-503.
50. MILLER, R. E., P. PARKER, M. DUNCAN, J. MERKEL, H. VARGAS, AND H. SNELL. 2002. Monitoring avian health in the Galápagos Islands-Developing an "early warning system." In Proceedings of the American Association of Zoo Vets. Media, Pennsylvania, p. 233-243.
51. MONCAYO, A. C., J. D. EDMAN, AND J. T. FINN. 2000. Application of geographic information technology in determining risk of eastern equine encephalomyelitis virus transmission. Journal of the American Mosquito Control Association 16: 28-35.
52. NAYAR, J. K., L. ROSEN, AND J. W. KNIGHT. 1986. Experimental vertical transmission of Saint Louis encephalitis virus by Florida mosquitoes. American Journal of Tropical Medicine and Hygiene 35: 1296-1301.
53. NIMS, B., F. H. VARGAS, AND P. G. PARKER. 2008. Low genetic diversity and lack of population structure in the endangered Galápagos penguin (Spheniscus mendiculus). Conservation Genetics 9: 1413-1420.
54. PADILLA, L. R., K. P. HUYVAERT, J. MERKEL, R. E. MILLER, AND P. G. PARKER. 2003. Hematology, plasma chemistry, serology and Chlamydophila status of the waved albatross (Phoebastria irrorata) on the Galápagos Islands. Journal of Zoo and Wildlife Medicine 34: 278-283.
55. -, D. SANTIAGO, J. F. MERKEL, R. E. MILLER, AND P. G. PARKER. 2004. Survey for Trichomonas gallinae, Chlamydophila psitacci, Salmonella spp. and Haemoproteus organisms in Columbiformes from the Galápagos Islands. Journal of Zoo and Wildlife Medicine 35: 60-64.
56. -, N. K. WHITEMAN, J. F. MERKEL, K. P. HUYVAERT, AND P. G. PARKER. 2006. Health assessment of seabirds on Genovesa, Galápagos Islands. Ornithological Monographs 60: 86-97.
57. PARKER, P. G., N. K. WHITEMAN, AND R. E. MILLER. 2006. Perspectives in ornithology: Conservation medicine in the Galápagos Islands: Partnerships among behavioral, population and veterinary scientists. The Auk 123: 625-638.
58. PERNEGER, T. V. 1998. What's wrong with Bonferroni adjustments. British Medical Journal 316: 1236-1238.
59. RANDOLPH, S. E. 2001. The shifting landscape of tick-borne zoonoses: Tick-borne encephalitis and Lyme borreliosis in Europe. Philosophical Transactions of the Royal Society of London, Series B 356: 1045-1056.
60. ROGERS, D. J. 2000. Satellites, space, time and the African trypanosomiases. Advances in Parasitology 47: 129-171.
61. STEINFURTH, A., F. H. VARGAS, R. P. WILSON, M. SPINDLER, AND D. W. MACdONALD. 2007. Space use by foraging Galápagos penguins during chick rearing. Endangered Species Research 4: 105-112.
62. SNELL, H. L., A. TYE, C. E. CAUSTON, AND R. BENSTED-SMITH. 2002. Current status of and threats to the terrestrial biodiversity of Galápagos. In A biodiversity vision for the Galápagos Islands. Charles Darwin Foundation and World Wildlife Fund, Puerto Ayora, Galápagos, Ecuador, p. 30-47.
63. THOMPSON, D. F., J. B. MALONE, M. HARB, R. FARIS, O. K. HUH, A. A. BUCK, AND B. L. CLINE. 1996. Bancroftian filariasis distribution and diurnal temperature differences in the Southern Nile Delta. Emerging Infectious Diseases 2: 234-235.
64. THOMPSON, R. A., J. W. DEOLIVEIRA LIMA, J. H.MAGUIRE, D. H. BRAUD, AND D. T. SCHOLL. 2002. Climatic and demographic determinants of American visceral leishmaniasis in northeastern Brazil using remote sensing technology for environmental categorization of rain and region influences on leishmaniasis. American Journal of Tropical Medicine and Hygiene 67: 648-655.
65. TRAVIS, E. K., F. H. VARGAS, J.MERKEL, N. GOTTDENKER, R. E.MILLER, AND P. G. PARKER. 2006a. Hematology, serum chemistry, andserology of the Galápagos penguin in the Galápagos Islands, Ecuador. Journal of Wildlife Diseases 42: 625-632.
66. -,-,-,-,-, AND-. 2006b. Hematology, plasma chemistry, and disease serology of the flightless cormorant (Phalacrocorax harrisi) in the Galápagos Islands, Ecuador. Journal of Wildlife Diseases 42: 133-141.
67. TUCKER, C. J. 1979. Red and photographic infrared linear combinations for monitoring vegetation. Remote Sensing of Environment 8: 127-150.
68. TURRELL, M. J., M. L. O'GUINN, D. J. DOHM, AND J. W. JONES. 2001. Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. Journal of Medical Entomology 38: 130-134.
69. VALLE, C. A., AND M. C. COULTER. 1987. Present status of the flightless cormorant, Galapagos penguin and greater flamingo populations in the Galapagos Islands, Ecuador, after the 1982-83 El Niño. Condor 89: 276-281.
70. VAN RIPER, C. III, S. G. VAN RIPER, M. L.GOFF, AND M. LAIRD. 1986. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56: 327-344.
71. VARGAS, F. H., S. HARRISON, S. REA, AND D. W. MACDONALD. 2006. Biological effects of El Niño on the Galápagos penguin. Biological Conservation 127: 107-114.
72. -, R. C. LACY, P. J. JOHNSON, A. STEINFURTH, R. J.M. CRAWFORD, P. D. BOERSMA, AND D. W.MACDONALD. 2007. Modelling the effect of El Niño on the persistence of small populations: The Galapagos penguin as a case study. Biological Conservation 137: 138-148.
73. VOTYPKA, J., J. SIMEK, AND P. TRYJANOWSKI. 2003. Blood parasites, reproduction and sexual selection in the red-backed shrike (Lanius collurio). Annales Zoologici Fennici 40: 431-439.
74. WHITEMAN, N. K., S. J. GOODMAN, B. J. SINCLAIR, T. WALSH, A. A. CUNNINGHAM, L.D.KRAMER, AND P. G. PARKER. 2005. Establishment of the avian disease vector Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador. Ibis 147: 844-847.
75. WIKELSKI, M., J. FOUFOPOULOS, H. VARGAS, AND H. SNELL. 2004. Galápagos birds and diseases: Invasive pathogens as threats for island species. Ecology and Society 9: 5.
76. WILSON, R. P., F. H. VARGAS, A. STEINFURTH, P. RIORDAN, Y. ROPERTCOUDERT, AND D. W. MACDONALD. 2008. What grounds some birds for life? Movement and diving in the sexually dimorphic Galápagos cormorant. Ecological Monographs 78: 633-652.
77. YARBROUGH, L. D., G. EASSON, AND J. S. KUSZMAUL. 2005. Using at-sensor radiance and reflectance tasseled cap transforms applied to change detection for the ASTER sensor. In IEEE 2005 international workshop on the analysis of multi-temporal remote sensing images, R. L. King and N. H. Younan (eds.). Biloxi, Mississippi, p. 141-145.