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Colonization of Parasites and Vectors

  • Arnaud Bataille
  • Iris I. Levin
  • Eloisa H. R. Sari
Chapter
Part of the Social and Ecological Interactions in the Galapagos Islands book series (SESGI)

Abstract

Colonization comprises the physical arrival of a species in a new area, but also its successful establishment within the local community. Oceanic islands, like the Hawaiian and the Galapagos archipelagos, represent excellent systems to study the mechanisms of colonization because of their historical isolation. In this chapter, we first review some of the major mechanisms by which parasites and vectors could arrive to an oceanic island, both naturally or due to human activities, and the factors that may influence their successful establishment in the insular host community. We then explore examples of natural and anthropogenic colonization of the Galapagos Islands by parasites and vectors, focusing on one or more case studies that best represent the diversity of colonization mechanisms that has shaped parasite distribution in the archipelago. Finally, we discuss future directions for research on parasite and vector colonization in Galapagos Islands.

Keywords

Dispersal Spread Introduction Coevolution |Host specificity Endemism 

References

  1. Alexander DJ, Aldous EW, Fuller CM (2012) The long view: a selective review of 40 years of Newcastle disease research. Avian Pathol 41:329–335PubMedCrossRefGoogle Scholar
  2. Amaral FR, Sheldon FH, Gamauf A, Haring E, Riesing M, Silveira LF, Wajntal A (2009) Patterns and processes of diversification in a widespread and ecologically diverse avian group, the buteonine hawks (Aves, Accipitridae). Mol Phylogenet Evol 53:703–715PubMedCrossRefGoogle Scholar
  3. Anderson JD, Fortner S (1988) Waved albatross egg neglect and associated mosquito ectoparasitism. Condor 90:727–729CrossRefGoogle Scholar
  4. Bar-David S, Lloyd-Smith JO, Getz WM (2006) Dynamics and management of infectious disease in colonizing populations. Ecology 87:1215–1224PubMedCrossRefGoogle Scholar
  5. Bataille A, Cunningham AA, Cedeno V, Patiño L, Constantinou A, Kramer LD, Goodman SJ (2009b) Natural colonization and adaptation of a mosquito species in Galapagos and its implications for disease threats to endemic wildlife. Proc Natl Acad Sci U S A 106:10230–10235PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bataille A, Cunningham AA, Cedeño V, Cruz M, Eastwood G, Fonseca DM, Causton CE, Azuero R, Loayza J, Martinez JD, Goodman SJ (2009a) Evidence for regular ongoing introductions of mosquito disease vectors into the Galapagos Islands. Proc Biol Sci 276:3769–3775PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bataille A, Cunningham AA, Cruz M, Cedeño V, Goodman SJ (2010) Seasonal effects and fine-scale population dynamics of Aedes taeniorhynchus, a major disease vector in the Galapagos Islands. Mol Ecol 19:4491–4504PubMedCrossRefGoogle Scholar
  8. Bataille A, Cunningham AA, Cruz M, Cedeño V, Goodman SJ (2011) Adaptation, isolation by distance and human-mediated transport determine patterns of gene flow among populations of the disease vector Aedes taeniorhynchus in the Galapagos Islands. Infect Genet Evol 11:1996–2003PubMedCrossRefGoogle Scholar
  9. Bataille A, Fournié G, Cruz M, Cedeño V, Parker PG, Cunningham AA, Goodman SJ (2012) Host selection and parasite infection in Aedes taeniorhynchus, endemic disease vector in the Galápagos Islands. Infect Genet Evol 12:1831–1841PubMedCrossRefGoogle Scholar
  10. Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844PubMedCrossRefGoogle Scholar
  11. Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bello FJ, Herrera GA, Sandoval JC, Escovar JE, Ruiz-Garcia M, Corena MD (2005) Colonization of Ochlerotatus taeniorhynchus from Riohacha, Colombia. J Am Mosq Control Assoc 21:28–32PubMedCrossRefGoogle Scholar
  13. Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958PubMedCrossRefGoogle Scholar
  14. Bollmer JL, Kimball RT, Whiteman NK, Sarasola JH, Parker PG (2006) Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands. Mol Phylogenet Evol 39:237–247PubMedCrossRefGoogle Scholar
  15. Brock PM, Hall AJ, Goodman SJ, Cruz M, Acevedo-Whitehouse K (2013) Immune activity, body condition and human-associated environmental impacts in a wild marine mammal. PLoS One 8:e67132PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brown CR, Brown MB (2004) Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85:1619–1626CrossRefGoogle Scholar
  17. Brown JKM, Hovmoller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541PubMedCrossRefGoogle Scholar
  18. Bulgarella M, Quiroga MA, Brito vera GA, Dregni JS, Cunninghame F, Mosquera Munoz DA, Monje LD, Causton CE, Heimpel GE (2015) Philornis downsi (Diptera: Muscidae), an avian nest parasite invasive to the Galapagos Islands, in mainland Ecuador. Ann Entomol Soc Am 108:242–250CrossRefGoogle Scholar
  19. Bunbury N, Jones CG, Greenwood AG, Bell DJ (2008) Epidemiology and conservation implications of Trichomonas gallinae infection in the endangered Mauritian pink pigeon. Biol Conserv 141:153–161CrossRefGoogle Scholar
  20. Carpenter S, Wilson A, Mellor PS (2009) Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol 17:172–178PubMedCrossRefGoogle Scholar
  21. Castelletto ML, Gang SS, Okubo RP, Tselikova AA, Nolan TJ, Platzer EG, Lok JB, Hallem EA (2014) Diverse host-seeking behaviors of skin-penetrating nematodes. PLoS Pathog 10:e1004305PubMedPubMedCentralCrossRefGoogle Scholar
  22. Causton CE, Peck SB, Sinclair BJ, Roque-Albelo L, Hodgson CJ, Landry B (2006) Alien insects: threats and implications for conservation of Galápagos Islands. Ann Ent Soc Am 99:121–143CrossRefGoogle Scholar
  23. Clark TM, Flis BJ, Remold SK (2004) Differences in the effects of salinity on larval growth and developmental programs of a freshwater and a euryhaline mosquito species (Insecta: Diptera, Culicidae). J Exp Biol 207:2289–2295PubMedCrossRefGoogle Scholar
  24. Clark NJ, Clegg SM (2015) The influence of vagrant hosts and weather patterns on the colonization and persistence of blood parasites in an island bird. J Biogeogr 42:641–651CrossRefGoogle Scholar
  25. Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, Jessup DA, Gulland F, Grigg ME (2005) Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int J Parasitol 35:1155–1168PubMedCrossRefGoogle Scholar
  26. Cruz Martinez JD, Causton CE (2007) Análisis del riesgo asociado a las operaciones y rutas aéreas al Archipiélago de Galápagos. Charles Darwin Fundation, Puerto Ayora, Galápagos Islands, Ecuador. Available at http://www.feigalapagos.org/biblioteca.html Google Scholar
  27. Curry RL, Grant PR (1989) Demography of the cooperatively breeding Galapagos mockingbird, Nesomimus parvulus, in a climatically variable environment. J Anim Ecol 58:441–463CrossRefGoogle Scholar
  28. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  29. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116PubMedCrossRefGoogle Scholar
  30. Dearborn DC, Anders AD, Schreiber EA, Adams RM, Mueller UG (2003) Inter-island movements and population differentiation in a pelagic seabird. Mol Ecol 12:2835–2843PubMedCrossRefGoogle Scholar
  31. Deem SL, Merkel J, Ballweber L, Vargas FH, Cruz MB, Parker PG (2010) Exposure to Toxoplasma gondii in Galapagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi) in the Galapagos Islands, Ecuador. J Wildl Dis 46:1005–1011PubMedCrossRefGoogle Scholar
  32. Deem S, Jiménez-Uzcátegui G, Ziemmeck F (2011) CDF checklist of Galapagos zoopathogens and Parasites-FCD lista de especies de zoopatógenos y parásitos de Galápagos. In: Ruiz D, Guézou A, Ziemmeck F (eds) Charles Darwin Foundation Galapagos species checklist–lista de especies de Galápagos de la Fundación Charles Darwin. Charles Darwin Foundation/Fundación Charles Darwin, Puerto Ayora, Galapagos. http://www.darwinfoundation.org/datazone/checklists/pathogens-and-parasites/zoopathogens-and-parasites. Last updated 16 Jun 2011Google Scholar
  33. Deem SL, Cruz MB, Higashiguchi JM, Parker PG (2012) Diseases of poultry and endemic birds in Galapagos: implications for the reintroduction of native species. Anim Conserv 15:73–82CrossRefGoogle Scholar
  34. Denkinger J, Gordillo L, Montero-Serra I, Murillo JC, Guevara N, Hirschfeld M, Fietz K, Rubianes F, Dan M (2015) Urban life of Galapagos sea lions (Zalophus wollebaeki) on San Cristobal Island, Ecuador: colony trends and threats. J Sea Res 105:10–14CrossRefGoogle Scholar
  35. Diamond JM, Veitch CR (1981) Extinctions and introductions in the New Zealand avifauna: cause and effect? Science 211:499–501PubMedCrossRefGoogle Scholar
  36. Diaz NM, Mendez GS, Grijalva CJ, Walden HS, Cruz M, Aragon E, Hernandez JA (2016) Dog overpopulation and burden of exposure to canine distemper virus and other pathogens on Santa Cruz Island, Galapagos. Prev Vet Med 123:128–137PubMedCrossRefGoogle Scholar
  37. Dietrich M, Gomez-Diaz E, McCoy KD (2011) Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector Borne Zoonotic Dis 11:453–470PubMedCrossRefGoogle Scholar
  38. Dowler RC, Carroll DS, Edwards CW (2000) Rediscovery of rodents (genus Nesoryzomys) considered extinct in the Galápagos Islands. Oryx 34:109–118Google Scholar
  39. Dubey JP (2002) A review of toxoplasmosis in wild birds. Vet Parasitol 106:121–153PubMedCrossRefGoogle Scholar
  40. Dunn JL, Wolke RE (1976) Dipetalonema spirocauda infection in the Atlantic harbor seal (Phoca vitulina concolor). J Wildl Dis 12:531–538PubMedCrossRefGoogle Scholar
  41. Eastwood G, Kramer LD, Goodman SJ, Cunningham AA (2011) West Nile virus vector competency of Culex quinquefasciatus mosquitoes in the Galapagos Islands. Am J Trop Med Hyg 85:426–433PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, Clarke RH, Pérez-Tris J (2012) Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol Lett 15:1112–1119PubMedCrossRefGoogle Scholar
  43. Fallon SM, Bermingham E, Ricklefs RE (2005) Host specilalization and geographic localization of avian malaria parasites: a regional analysis in the lesser Antilles. Am Nat 165:466–480PubMedCrossRefGoogle Scholar
  44. Farid HA, Hammad RE, Hassan MM, Morsy ZS, Kamal IH, Weil GJ, Ramzy RMR (2001) Detection of Wuchereria bancrofti in mosquitoes by the polymerase chain reaction: a potentially useful tool for large-scale control programmes. Trans R Soc Trop Med Hyg 95:29–32PubMedCrossRefGoogle Scholar
  45. Fenner F, Poole WE, Marshall ID, Dyce AL (1957) Studies in the epidemiology of infectious myxomatosis of rabbits: VI. The experimental introduction of the European strain of myxoma virus into Australian wild rabbit populations. J Hyg 55:192–206PubMedPubMedCentralCrossRefGoogle Scholar
  46. Fessl B, Sinclair BJ, Kleindorfer S (2006) The life-cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin's finches and its impacts on nestling survival. Parasitology 133:739–747PubMedCrossRefGoogle Scholar
  47. Fonseca DM, Lapointe DA, Fleischer RC (2000) Bottlenecks and multiple introductions: population genetics of the vector of avian malaria in Hawaii. Mol Ecol 9:1803–1814PubMedCrossRefGoogle Scholar
  48. Fonseca DM, Smith JL, Wilkerson RC, Fleischer RC (2006) Pathways of expansion and multiple introductions illustrated by large genetic differentiation among worldwide populations of the southern house mosquito. Am J Trop Med Hyg 74:284–289PubMedGoogle Scholar
  49. Font WF (2003) The global spread of parasites: what do Hawaiian streams tell us? Bioscience 53:1061–1067CrossRefGoogle Scholar
  50. Fournié G, Goodman SJ, Cruz M, Cedeño V, Vélez A, Patiño L, Millins C, Gibbons LM, Fox MT, Cunningham AA (2015) Biogeography of parasitic nematode communities in the Galápagos giant tortoise: implications for conservation management. PLoS One 10:e0135684PubMedPubMedCentralCrossRefGoogle Scholar
  51. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327PubMedCrossRefGoogle Scholar
  52. French SS, DeNardo DF, Greives TJ, Strand CR, Demas GE (2010) Human disturbance alters endocrine and immune responses in the Galapagos marine iguana (Amblyrhynchus cristatus). Horm Behav 58:792–799PubMedPubMedCentralCrossRefGoogle Scholar
  53. Godfrey SS, Nelson NJ, Bull CM (2011) Ecology and dynamics of the blood parasite, Hepatozoon tuatarae (Apicomplexa), in tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. J Wildl Dis 47:126–139PubMedCrossRefGoogle Scholar
  54. Gottdenker NL, Walsh T, Jiménez-Uzcátegui G, Betancourt F, Cruz M, Soos C, Miller RE, Parker PG (2008) Causes of mortality of wild birds submitted to the Charles Darwin Research Station, Santa Cruz, Galápagos, Ecuador from 2002–2004. J Wildl Dis 44:1024–1031PubMedCrossRefGoogle Scholar
  55. Gottdenker NL, Walsh T, Vargas H, Merkel J, Jimenez R, Gustavo U, Miller RE, Dailey M, Parker PG (2005) Assessing the risks of introduced chickens and their pathogens to native birds in the Galápagos archipelago. Biol Conserv 126:429–439CrossRefGoogle Scholar
  56. Hailer F, Schreiber EA, Miller JM, Levin II, Parker PG, Chesser RT, Fleischer RC (2010) Long-term isolation of a highly mobile seabird on the Galapagos. Proc Biol Sci 278:817–825PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hall-Stoodley L, Stoodley P (2005) Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 13:7–10PubMedCrossRefGoogle Scholar
  58. Hardy DE (1960) Insects of Hawaii, Diptera, vol 10. University of Hawaii Press, Honolulu, HIGoogle Scholar
  59. Hardy JL, Rosen L, Reeves WC, Scrivani RP, Presser SB (1984) Experimental transovarial transmission of St. Louis encephalitis virus by Culex and Aedes mosquitoes. Am J Trop Med Hyg 33:166–175PubMedCrossRefGoogle Scholar
  60. Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. J Biogeogr 35:1533–1550CrossRefGoogle Scholar
  61. Howard LO (1889) Scientific results of explorations by the U.S. fish commission steamer “albatross”. No. V. Annotated catalogue of the insects collected in 1887–88. Proc US Natl Mus 12:185–216CrossRefGoogle Scholar
  62. Iqbal M, Austin AD (2002) New species of the Australian endemic wasp genus Notosigalphus van Achterberg and Austin (hymenoptera: Braconidae) from Flinders Island, Tasmania. Aust J Entomol 41:149–154CrossRefGoogle Scholar
  63. Ishtiaq F, Guillaumot L, Clegg M, Phillimore AB, Black RA, Owens IPF, Mundy NI, Sheldon BC (2008) Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Mol Ecol 17:4545–4555PubMedCrossRefGoogle Scholar
  64. Ishtiaq F, Clegg SM, Phillimore AB, Black RA, Owens IPF, Sheldon BC (2010) Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. J Biogeogr 37:120–132CrossRefGoogle Scholar
  65. Harris JD, Joao PMCM, Ana P (2011) Molecular characterization of Hepatozoon species in reptiles from the Seychelles. J Parasitol 97:106–110PubMedCrossRefGoogle Scholar
  66. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993PubMedCrossRefGoogle Scholar
  67. Juliano SA, Lounibos PL (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kay BH, Farrow RA (2000) Mosquito (Diptera: Culicidae) dispersal: implications for the epidemiology of Japanese and Murray valley encephalitis viruses in Australia. J Med Entomol 37:797–801PubMedCrossRefGoogle Scholar
  69. Keeling MJ, Woolhouse MEJ, Shaw DJ, Matthews L, Chase-Topping M, Haydon DT, Cornell SJ, Kappey J, Wilesmith J, Grenfell BT (2001) Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294:813–817PubMedCrossRefGoogle Scholar
  70. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652PubMedCrossRefGoogle Scholar
  71. Kier G, Kreft H, Lee TM, Jetz W, Ibisch PL, Nowicki C, Mutke J, Barthlott W (2009) A global assessment of endemism and species richness across island and mainland regions. Proc Natl Acad Sci U S A 106:9322–9327PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kilpatrick AM, Kramer LD, Campbell SR, Alleyne EO, Dobson AP, Daszak P (2005) West Nile virus risk assessment and the bridge vector paradigm. Emerging Infect Dis 11:425–429PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kilpatrick AM, Chmura AA, Gibbons DW, Fleischer RC, Marra PP, Daszak P (2006a) Predicting the global spread of H5N1 avian influenza. Proc Natl Acad Sci U S A 103:19368–19373PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kilpatrick AM, Daszak P, Goodman SJ, Roog H, Kramer LD, Cedeno V, Cunningham AA (2006b) Predicting pathogen introduction: West Nile virus spread in Galápagos. Conserv Biol 20:1224–1231PubMedCrossRefGoogle Scholar
  75. Klassen GT (1992) Coevolution: a history of the macroevolutionary approach to studying host–parasite associations. J Parasitol 78:573–587PubMedCrossRefGoogle Scholar
  76. Koop JAH, Huber SK, Laverty SM, Clayton DH (2011) Experimental demonstration of the fitness consequences of an introduced parasite of Darwin’s finches. PLoS One 6:e19706PubMedPubMedCentralCrossRefGoogle Scholar
  77. Labarthe N, Guerrero J (2005) Epidemiology of heartworm: what is happening in South America and Mexico? Vet Parasitol 133:149–156PubMedCrossRefGoogle Scholar
  78. Labarthe N, Serrao ML, Melo YF, de Oliveira SJ, Lourenço-de-Oliveira R (1998) Potential vectors of Dirofilaria immitis (Leidy, 1856) in Itacoatiara, oceanic region of Niterói municipality, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 93:425–432PubMedCrossRefGoogle Scholar
  79. Lang JD (2003) Factors affecting immatures of (Diptera: Culicidae) in San Diego County, California. J Med Entomol 40(4):387–394PubMedCrossRefGoogle Scholar
  80. Levin II, Colborn RE, Kim D, Perlut NG, Renfrew RB, Parker PG (2016) Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium. Ecol Evol 6:716–726PubMedPubMedCentralCrossRefGoogle Scholar
  81. Levin II, Parker PG (2014) Infection with Haemoproteus iwa affects vector movement in a hippoboscid fly-frigatebird system. Mol Ecol 23:947–953PubMedCrossRefGoogle Scholar
  82. Levin II, Outlaw DC, Vargas FH, Parker PG (2009) Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biol Conserv 142:3191–3195CrossRefGoogle Scholar
  83. Levin II, Valkiunas G, Iezhova TA, O'Brien SL, Parker PG (2012) Novel Haemoproteus species (Haemosporida: Haemoproteidae) from the swallow-tailed gull (Lariidae), with remarks on the host range of hippoboscid-transmitted avian Hemoproteids. J Parasitol 98:847–854PubMedCrossRefGoogle Scholar
  84. Levin II, Valkiunas G, Santiago-Alarcon D, Cruz LL, Iezhova TA, O'Brien SL, Hailer F, Dearborn D, Schreiber EA, Fleischer RC, Ricklefs RE, Parker PG (2011) Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Int J Parasitol 41:1019–1027PubMedCrossRefGoogle Scholar
  85. Levin II, Zwiers P, Deem SL, Geest EA, Higashiguchi JM, Iezhova TA, Jiménez-Uzcátegui G, Kim DH, Morton JP, Perlut NG, Renfrew RB, Sari EH, Valkiunas G, Parker PG (2013) Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos Islands and evidence for arrival via migratory birds: plasmodium in Galapagos birds. Conserv Biol 27:1366–1377PubMedCrossRefGoogle Scholar
  86. Levy JK, Crawford PC, Lappin MR, Dubovi EJ, Levy MG, Alleman R, Tucker SJ, Clifford EL (2008) Infectious diseases of dogs and cats on Isabela Island, Galapagos. J Vet Intern Med 22:60–65PubMedCrossRefGoogle Scholar
  87. Lindsay DS, Dubey JP (2009) Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. J Parasitol 95:1019–1020PubMedCrossRefGoogle Scholar
  88. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20(5):223–228PubMedCrossRefGoogle Scholar
  89. Lounibos LP (2002) Invasions by insect vectors of human disease. Annu Rev Entomol 47:233–266PubMedCrossRefGoogle Scholar
  90. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, NJGoogle Scholar
  91. MacLeod CJ, Paterson AM, Tompkins DM, Duncan RP (2010) Parasites lost–do invaders miss the boat or drown on arrival? Ecol Lett 13:516–527PubMedCrossRefGoogle Scholar
  92. Mangili A, Gendreau MA (2005) Transmission of infectious diseases during commercial air travel. Lancet 365:989–996PubMedCrossRefGoogle Scholar
  93. Masner L, Johnson N (2007) Xentor, a new endemic genus from Fiji (hymenoptera: Platygastroidea: Scelionidae) and description of three new species. Occas pap Bernice P. Bishop Mus 94:11–20Google Scholar
  94. Matson KD (2006) Are there differences in immune function between continental and insular birds? Proc Biol Sci 273:2267–2274PubMedPubMedCentralCrossRefGoogle Scholar
  95. McCoy KD, Dietrich M, Jaeger A, Wilkinson DA, Bastien M, Lagadec E, Boulinier T, Pascalis H, Tortosa P, Le Corre M, Dellagi K, Lebarbenchon C (2016) The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens. Acta Oecol 72:98–109CrossRefGoogle Scholar
  96. McDowall RM (2000) Biogeography of the southern cool-temperate galaxioid fishes: evidence from metazoan macroparasite faunas. J Biogeogr 27(5):1221–1229CrossRefGoogle Scholar
  97. Merkel J, Jones HI, Whiteman NK, Gottdenker NL, Vargas FH, Travis EK, Miller RE, Parker PG (2007) Microfilariae in Galápagos penguins (Spehniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi): genetics, morphology, and prevalence. J Parasitol 93:495–503PubMedCrossRefGoogle Scholar
  98. Milberg P, Tyrberg T (1993) Naïve birds and noble savages–a review of man-caused prehistoric extinctions of island birds. Ecography 16:229–250CrossRefGoogle Scholar
  99. Miller GD, Hofkin BV, Snell H, Hahn A, Miller RD (2001) Avian malaria and Marek’s disease: potential threats to Galápagos penguins Sphenicus mendiculus. Marine Ornithol 29:43–46Google Scholar
  100. Olsen B, Duffy DC, Jaenson TG, Gylfe A, Bonnedahl J, Bergstrom S (1995) Transhemispheric exchange of Lyme disease spirochetes by seabirds. J Clin Microbiol 33:3270–3274PubMedPubMedCentralGoogle Scholar
  101. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus ADME, Fouchier RAM (2006) Global patterns of influenza a virus in wild birds. Science 312:384–388PubMedCrossRefGoogle Scholar
  102. Parker PG, Buckles EL, Farrington H, Petren K, Whiteman NK, Ricklefs RE, Bollmer JL, Jimenez-Uzcategui G (2011) 110 years of Avipoxvirus in the Galapagos Islands. PLoS One 6:e15989PubMedPubMedCentralCrossRefGoogle Scholar
  103. Parker PG, Whiteman NK, Miller RE (2006) Conservation medicine on the Galápagos Islands: partnerships among behavioural, population, and veterinary scientists. Auk 123:625–638CrossRefGoogle Scholar
  104. Paterson AM, Palma RL, Gray RD (1999) How frequently do avian lice miss the boat? Implications for coevolutionary studies. Syst Biol 48:214–223CrossRefGoogle Scholar
  105. Peck SB (1994) Aerial dispersal of insects between and to islands in the Galápagos archipelago, Ecuador. Ann Ent Soc Amer 87:218–224CrossRefGoogle Scholar
  106. Peck SB, Heraty J, Landry B, Sinclair BJ (1998) Introduced insect fauna of an oceanic archipelago: the Galápagos Islands, Ecuador. Am Entomol 44:218–227CrossRefGoogle Scholar
  107. Philip CB (1976) Horse-flies, too, take some victims in cold-blood, as on Galapagos isles. Pan-Pac Entomol 52:83–88Google Scholar
  108. Philip CB (1983) A unique, divergent developmental dependence of a Galapagos horse fly (Diptera, Tabanidae). Wasmann J Biol 41:47–49Google Scholar
  109. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15PubMedCrossRefGoogle Scholar
  110. Poulakakis N, Glaberman S, Russello M, Beheregaray LB, Ciofi C, Powell JR, Caccone A (2008) Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise. Proc Natl Acad Sci U S A 105:15464–15469PubMedPubMedCentralCrossRefGoogle Scholar
  111. Poulin R (2004) Macroecological patterns of species richness in parasite assemblages. Basic Appl Ecol 5:423–434CrossRefGoogle Scholar
  112. Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) The chewing lice: world checklist and biological overview. Illinois Natural History Survey, Champaign, ILGoogle Scholar
  113. Provost MW (1951) The occurrence of salt marsh mosquitoes in the interior of Florida. Fla Entomol 34:48–53CrossRefGoogle Scholar
  114. Reperant LA (2009) Applying the theory of island biogeography to emerging pathogens: toward predicting the sources of future emerging zoonotic and vector-borne diseases. Vector Borne Zoonotic Dis 10:105–110CrossRefGoogle Scholar
  115. Ricklefs RE, Outlaw DC (2010) A molecular clock for malaria parasites. Science 329(5988):226–229PubMedCrossRefGoogle Scholar
  116. Ritchie SA, Rochester W (2001) Wind-blown mosquitoes and introduction of Japanese encephalitis into Australia. Emerg Infect Dis 7:900–903PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rivera-Parra JL, Levin II, Johnson KP, Parker PG (2015) Lineage sorting in multihost parasites: Eidmanniella albescens and Fregatiella aurifasciata on seabirds from the Galapagos Islands. Ecol Evol 5:3264–3271PubMedPubMedCentralCrossRefGoogle Scholar
  118. Rivera-Parra JL, Levin II, Parker PG (2014) Comparative ectoparasite loads of five seabird species in the Galapagos Islands. J Parasitol 100:569–577PubMedCrossRefGoogle Scholar
  119. Ruiz GM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq A, Colwell RR (2000) Global spread of microorganisms by ships. Nature 408:49–50PubMedCrossRefGoogle Scholar
  120. Santiago-Alarcon D, Outlaw DC, Ricklefs RE, Parker PG (2010) Phylogenetic relationships of haemosporidian parasites in new world Columbiformes, with emphasis on the endemic Galapagos dove. Int J Parasitol 40:463–470PubMedCrossRefGoogle Scholar
  121. Sardelis MR, Turell MJ, Dohm DJ, O'Guinn ML (2001) Vector competence of selected north American Culex and Coquillettidia mosquitoes for West Nile virus. Emerging Infect Dis 7:1018–1022PubMedPubMedCentralCrossRefGoogle Scholar
  122. Sari EHR, Klompen H, Parker PG (2013) Tracking the origins of lice, haemosporidian parasites and feather mites of the Galápagos flycatcher (Myiarchus magnirostris). J Biogeogr 40:1082–1093CrossRefGoogle Scholar
  123. Sari HER, Parker PG (2012) Understanding the colonization history of the Galápagos flycatcher (Myiarchus Magnirostris). Mol Phylogenet Evol 63:244–254PubMedCrossRefGoogle Scholar
  124. Sato T, Higuchi T, Shibuya H, Ohba S, Nogami S, Shirai W, Watanabe H, Honda S (2002) Lingual squamous cell carcinoma in a california sea lion (zalophus californianus). J Zoo Wildl Med 33:367–370PubMedCrossRefGoogle Scholar
  125. Siers SR, Merkel J, Bataille A, Vargas FH, Parker PG (2010) Ecological correlates of microfilarial prevalence in endangered Galapagos birds. J Parasitol 96:259–272PubMedCrossRefGoogle Scholar
  126. Sinclair BJ (2017) Checklist of Galapagos Flies–FCD Lista de especies de Moscas y mosquitos de Galapagos. In: Bungartz F, Herrera H, Jaramillo P, Tirado N, Jimenez-Uzcategui G, Ruiz D, Guezou A, Ziemmeck F (eds) Charles Darwin foundation Galapagos species checklist–Lista de Especies de Galapagos de la Fundacion Charles Darwin. Charles Darwin Foundation/Fundacion Charles Darwin, Puerto Ayora, Galapagos. http://darwinfoundation.org/datazone/checklists/terrestrial-invertebrates/diptera/ Last updated 12 May 2017Google Scholar
  127. Smith KF, Carpenter SM (2006) Potential spread of introduced black rat (Rattus rattus) parasites to endemic deer mice (Peromyscus maniculatus) on the California Channel islands. Divers Distrib 12:742–748CrossRefGoogle Scholar
  128. Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol 82:565–585PubMedCrossRefGoogle Scholar
  129. Soos C, Padilla L, Iglesias A, Gottdenker N, Don MC, Rios A, Parker PG (2008) Comparison of pathogens in broiler and backyard chickens on the Galapagos Islands: implications for transmission to wildlife. Auk 125:445–455CrossRefGoogle Scholar
  130. Strona G, Fattorini S (2014) A few good reasons why species-area relationships do not work for parasites. Biomed Res Int 2014:271680PubMedPubMedCentralCrossRefGoogle Scholar
  131. Tatem AJ, Hay SI, Rogers DJ (2006a) Global traffic and disease vector dispersal. Proc Natl Acad Sci U S A 103:6242–6247PubMedPubMedCentralCrossRefGoogle Scholar
  132. Tatem AJ, Rogers DJ, Hay SI (2006b) Global transport networks and infectious disease spread. Adv Parasitol 62:345–381CrossRefGoogle Scholar
  133. Telford SR Jr, Wozniak EJ, Butler JF (2001) Haemogregarine specificity in two communities of Florida snakes, with descriptions of six new species of Hepatozoon (Apicomplexa: Hepatozoidae) and a possible species of Haemogregarina (Apicomplexa: Haemogregarinidae). J Parasitol 87:890–905PubMedCrossRefGoogle Scholar
  134. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30:1217–1258PubMedPubMedCentralCrossRefGoogle Scholar
  135. Thiel T, Whiteman NK, Tirape A, Baquero M, Cedeno V, Walsh T, Jimenez Uzcátegui G, Parker PG (2005) Characterization of canarypox-like viruses infecting endemic birds in the Galápagos Islands. J Wildl Dis 41:342–353PubMedCrossRefGoogle Scholar
  136. Turell MJ, Beaman JR, Neely GW (1994) Experimental transmission of eastern equine encephalitis virus by strains of Aedes albopictus and Aedes taeniorhynchus (Diptera: Culicidae). J Med Entomol 31:287–290PubMedCrossRefGoogle Scholar
  137. Turell MJ, O'Guinn ML, Dohm DJ, Jones JW (2001) Vector competence of north American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38:130–134PubMedCrossRefGoogle Scholar
  138. United Nations Educational, Scientific, and Cultural Organisation (UNESCO) (2006) Joint IUCN/UNESCO mission report: Galápagos Islands. United Nations Educational, Scientific and Cultural Organization, ParisGoogle Scholar
  139. United Nations Educational, Scientific, and Cultural Organisation (UNESCO) (2010) State of conservation of world heritage properties inscribed on the list of world heritage in danger. United Nations Educational, Scientific, and Cultural Organisation, ParisGoogle Scholar
  140. Valkiunas G (2005) Avian malaria parasites and other Haemosporidia. CRC Press, Boca Raton, FLGoogle Scholar
  141. Valkiunas G, Santiago-Alarcon D, Levin II, Iezhova TA, Parker PG (2010) A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagos dove, Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. J Parasitol 96:783–792PubMedCrossRefGoogle Scholar
  142. van Riper C, van Riper SG, Hansen WR (2002) Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119:929–942CrossRefGoogle Scholar
  143. van Riper C, van Riper SG, Lee Goff M, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344CrossRefGoogle Scholar
  144. Warner RE (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70:101–120CrossRefGoogle Scholar
  145. Weimerskirch H, Le Corre M, Maras F, Barbraud C, Tostain O, Chastel O (2006) Postbreeding movements of frigatebirds tracked with satellite telemetry. Condor 108:220–225CrossRefGoogle Scholar
  146. Wheeler E, Hong P-Y, Bedon LC, Mackie RI (2012) Carriage of antibiotic-resistant enteric bacteria varies among sites in Galapagos reptiles. J Wildl Dis 48:56–67PubMedCrossRefGoogle Scholar
  147. Whiteman NK, Dosanjh VS, Palma RL, Hull JM, Kimball RT, Sánchez P, Sarasola JH, Parker PG (2009) Molecular and morphological divergence in a pair of bird species and their ectoparasites. J Parasitol 95:1372–1382PubMedCrossRefGoogle Scholar
  148. Whiteman NK, Goodman SJ, Sinclair BJ, Walsh TIM, Cunningham AA, Kramer LD, Parker PG (2005) Establishment of the avian disease vector Culex quinquefasciatus say, 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador. Ibis 147:844–847CrossRefGoogle Scholar
  149. Whiteman NK, Kimball RT, Parker PG (2007) Co-phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Mol Ecol 16:4759–4773PubMedCrossRefGoogle Scholar
  150. Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Conserv 8:175–118CrossRefGoogle Scholar
  151. Whiteman NK, Sánchez P, Merkel J, Klompen H, Parker PG (2006) Cryptic host specificity of an avian skin mite (Epidermoptidae) vectored by louseflies (Hippoboscidae) associated with two endemic Galapagos bird species. J Parasitol 92:1218–1228PubMedCrossRefGoogle Scholar
  152. Wikelski M (1999) Influences of parasites and thermoregulation on grouping tendencies in marine iguanas. Behav Ecol 10:22–29CrossRefGoogle Scholar
  153. Wikelski M, Foufopoulos J, Vargas H, Snell H (2004) Galápagos birds and diseases: invasive pathogens as threats for island species. Ecol Soc 9(1) 5: http://www.ecologyandsociety.org/vol9/iss1/art5 CrossRefGoogle Scholar
  154. Williams ES, Yuill T, Artois M, Fischer J, Haigh SA (2002) Emerging infectious diseases in wildlife. Rev Off Int Epizoot 21:139–157PubMedCrossRefGoogle Scholar
  155. Work TM, Massey JG, Rideout BA, Gardiner CH, Ledig DB, Kwok OCH, Dubey JP (2000) Fatal toxoplasmosis in free-ranging endangered ‘Alala from Hawaii. J Wildl Dis 36:205–212PubMedCrossRefGoogle Scholar
  156. Wyatt KB, Campos PF, Gilbert MTP, Kolokotronis S-O, Hynes WH, DeSalle R, Daszak P, MacPhee RDE, Greenwood AD (2008) Historical mammal extinction on Christmas Island (Indian ocean) correlates with introduced infectious disease. PLoS One 3:e3602PubMedPubMedCentralCrossRefGoogle Scholar
  157. Ypma RJF, Jonges M, Bataille A, Stegeman A, Koch G, van Boven M, Koopmans M, van Ballegooijen WM, Wallinga J (2013) Genetic data provide evidence for wind-mediated transmission of highly pathogenic avian influenza. J Infect Dis 207:730–735PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Arnaud Bataille
    • 1
  • Iris I. Levin
    • 2
  • Eloisa H. R. Sari
    • 3
  1. 1.CIRAD, UMR ASTREMontpellierFrance
  2. 2.Department of BiologyAgnes Scott CollegeDecaturUSA
  3. 3.Departamento de Biologia GeralUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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