Parasite prevalence corresponds to host life history in a diverse assemblage of afrotropical birds and haemosporidian parasites

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Lutz, Holly L ^a,b,c,d   Hochachka, Wesley M ^c   Engel, Joshua I ^d   Bell, Jeffrey A ^e   Tkach, Vasyl V ^e   Bates, John M ^d   Hackett, Shannon J ^d   Weckstein, Jason D ^f  

^a Program on Infrastructure Policy   (United States)

^b Department of Population Medicine and Diagnostic Sciences College of Veterinary Medicine Cornell University ^*  (United States)

^c Fuller Evolutionary Biology Program   (United States)

^d FIELD MUSEUM OF NATURAL HISTORY   (United States)

^e UNIVERSITY OF NORTH DAKOTA   (United States)

^f ACADEMY OF NATURAL SCIENCES OF DREXEL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B;

ANIMAL BEHAVIOR; ARTICLE; BIRD; CONTROLLED STUDY; DNA SEQUENCE; FLOCKING BEHAVIOR; HAEMOPROTEUS; HAEMOSPORIDA; INFECTION RATE; LEUCOCYTOZOON; LIFE HISTORY TRAIT; MALAWI; NESTING; NONHUMAN; PARASITE PREVALENCE; PARASITISM; PLASMODIUM; POLYMERASE CHAIN REACTION; SPECIES HABITAT; ANIMAL; ANIMAL PARASITOSIS; BIODIVERSITY; BIRD DISEASE; CLASSIFICATION; DISEASE CARRIER; ECOSYSTEM; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LIFE CYCLE STAGE; PARASITOLOGY; PHYSIOLOGY; PREVALENCE; TRANSMISSION;

AVES; HAEMOPROTEUS; LEUCOCYTOZOON;

ANIMALS; BEHAVIOR, ANIMAL; BIODIVERSITY; BIRD DISEASES; BIRDS; DISEASE VECTORS; ECOSYSTEM; HAEMOSPORIDA; HOST-PARASITE INTERACTIONS; LIFE CYCLE STAGES; PREVALENCE; PROTOZOAN INFECTIONS, ANIMAL;

EID: 84928911447     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121254     Document Type: Article

References (99)

1. Ewald PW. Host-parasite relations vectors and the evolution of disease severity. Annu Rev Ecol Evol Syst. 1983; 14: 465-485.
2. Poulin R. Evolutionary Ecology of Parasites. 2nd ed. Princeton, New Jersey: Princeton University Press; 2007.
3. Combes C. Fitness of parasites: pathology and selection. Int J Parasitol. 1997; 27: 1-10. PMID: 9076524
4. Dobson A. Population dynamics of pathogens with multiple host species. Am Nat. 2004; 164: S64-S78. PMID: 15540143
5. Lafferty KD. The ecology of climate change and infectious diseases. Ecol. 2009; 90: 888-900.
6. Medeiros MCI, Hamer GL, Ricklefs RE. Host compatibility rather than vector-host-encounter rate determines the host range of avian Plasmodium parasites. Proc Roy Soc B. 2013; 280: 20122947 doi: 10. 1098/rspb.2012.2947 PMID: 23595266
7. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD. Host heterogeneity dominates West Nile virus transmission. Proc Roy Soc B. 2006; 273: 2327-2333. PMID: 16928635
8. Janousek WM, Marra PP, Kilpatrick AM. Avian roosting behavior influences vector-host interactions for West Nile virus hosts. Parasit Vectors. 2014; 7: 1-11. doi: 10.1186/1756-3305-7-1 PMID: 24411014
9. Blackmore JS, Dow RP. Differential feeding of Culex tarsalis on nestling and adult birds. Mosq News. 1958; 18: 15-17.
10. Edman JD, Kale HW. Host behavior: its influence on the feeding success of mosquitoes. Ann Entomol Soc Am. 1971; 64: 513-516.
11. Giardina AR, Schmidt KA, Schauber EM, Ostfeld RS. Modeling the role of songbirds and rodents in the ecology of Lyme disease. Can J Zool. 2000; 78: 2184-2197.
12. Ogden NH, Lindsay LR, Hanincová K, Barker IK, Bigras-Poulin M, Charron DF, et al. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol. 2008; 74: 1780-1790. doi: 10.1128/ AEM.01982-07 PMID: 18245258
13. Mahmood F, Chiles RE, Fang Y, Barker CM, Reisen WK. Role of nestling mourning doves and house finches as amplifying hosts of St. Louis encephalitis virus. J Med Entomol. 2004; 41: 965-972. PMID: 15535629
14. Gilbert KL. Effect of predator type season brood size and West Nile Virus infection on the nest defense behavior of male and female Eastern Bluebirds. M. Sc. Thesis, Eastern Kentucky University. 2012. Available: http://encompass.eku.edu/etd/78/.
15. Hayes RO, LaMotte LC Holden P. Ecology of arboviruses in Hale Country Texas during 1965. Am J Trop Med Hyg. 1967; 16: 675-687. PMID: 6053533
16. Unnasch RS, Sprenger T, Katholi CR, Cupp EW, Hill GE, Unnasch TR. A dynamic transmission model of eastern equine encephalitis virus. Ecol Modell. 2006; 192: 425-440. PMID: 16501661
17. Kale HW, Edman JD, Webber LA. Effect of behavior and age of individual Ciconiiform birds on mosquito feeding success. Mosq News. 1972; 32: 343-350.
18. Edman JD, Scott TW. Host defensive behaviour and the feeding success of mosquitoes. Int J Trop Insect Sci. 1987; 8: 617-622.
19. Scott TW, Edman JD. Effects of avian host age and arbovirus infection on mosquito attraction and blood-feeding success. In: Loye JE, Zult M, editors. Bird-Parasite Interactions: ecology, evolution and behavior. Oxford Ornithology Press; 1991. pp. 179-204.
20. Scott TW, Lorenz LH, Edman JD. Effects of house sparrow age and arbovirus infection on attraction of mosquitoes. J Med Entomol. 1990; 27: 856-863. PMID: 1977913
21. Burkett-Cadena ND, Ligon RA, Liu M, Hassan HK, Hill GE, Eubanks MD, et al. Vector-host interactions in avian nests: do mosquitoes prefer nestlings over adults? Am J Trop Med. 2010; 83: 395-399. doi: 10.4269/ajtmh.2010.10-0048 PMID: 20682889
22. Caillouët KA, Riggan AE, Bulluck LP, Carlson JC, Sabo RT. Nesting bird " host funnel" increases mos-quito-bird contact rate. J Med Entomol. 2013; 50: 462-466. PMID: 23540137
23. Day JF, Stark LM. Avian serology in a St. Louis encephalitis epicenter before during and after a widespread epidemic in south Florida USA. J Med Entomol. 1999; 36: 614-624. PMID: 10534957
24. Bennett GF. On some ornithophilic blood-sucking diptera in Algonquin Park, Ontario, Canada. Can J Zool. 1960; 38: 377-389.
25. Bennett GF, Fallis AM. Blood parasites of birds in Algonquin Park Canada and a discussion of their transmission. Can J Zool. 1960; 38: 261-273.
26. Ricklefs RE. Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci U S A. 1992; 89: 4722-4725. PMID: 1584808
27. Garvin MC, Remsen JV. An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. Auk 1997; 114: 179-191.
28. Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science 1982; 218: 384-387. PMID: 7123238
29. Read AF. Sexual selection and the role of parasites. Trends in Ecology and Evolution 1988; 3: 97-102. doi: 10.1016/0169-5347(88)90115-2 PMID: 21227157
30. Pruett-Jones SG, Pruett-Jones MA, Jones HI. Parasites and sexual selection in a New Guinea avifauna. Current Ornithology 1991; 8: 213-245.
31. Scheuerlein A, Ricklefs RE. Prevalence of blood parasites in European passeriform birds. Proc Roy Soc B. 2004; 271: 1363-1370. PMID: 15306334
32. Atkinson CT, van Riper C III. Pathogenicity and epizootiology of avian haematozoa: Plasmodium Leucocytozoon and Haemoproteus. In: Loye JE, Zult M, editors. Bird-Parasite Interactions: ecology, evolution and behavior. Oxford Ornithology Press, New York; 1991. pp. 19-48.
33. Miller LH, Baruch DI, Marsh K, Doumbo OK. The pathogenic basis of malaria. Nature 2002; 415: 673-679. PMID: 11832955
34. Jasinskiene N, Coleman J, Ashikyan A, Salampessy M, Marinotti O, James AA. Genetic control of malaria parasite transmission: threshold levels for infection in an avian model system. Am J Trop Med Hyg. 2007; 76: 1072-1078. PMID: 17556613
35. Fallon SM, Ricklefs RE, Latta SC, Bermingham E. Temporal stability of insular avian malaria parasite communities. Proc Roy Soc B. 2004; 271: 493-500.
36. Beadell JS, Covas R, Gebhard C, Ishtiaq F, Melo M, Schmidt BK, et al. Host associations and evolutionary relationships of avian blood parasites from West Africa. Int J Parasitol. 2009; 39: 257-266. doi: 10.1016/j.ijpara.2008.06.005 PMID: 18713636
37. Ishtiaq F, Gering E, Rappole JH, Rahmani AR, Jhala YV, Dove CJ, et al. Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. J Wild Dis. 2007; 43: 382-398.
38. 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. 2004; 58: 1617-1621. PMID: 15341164
39. Valkiunas G. Avian Malaria Parasites and Other Haemosporidia. Boca Raton, Florida: CRC Press; 2005.
40. Chasar A, Loiseau C, Valki nas G, Iezhova T, Smith TB, Sehgal RNM. Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Mol Ecol. 2009; 18: 4121-4133. doi: 10.1111/j.1365-294X.2009.04346.x PMID: 19754513
41. Loiseau C, Iezhova T, Valki nas G, Chasar A, Hutchinson A, BuermannW, et al. Spatial variation of haemosporidian parasite infection in African rainforest bird species. J Parasitol. 2010; 96; 21-29. doi: 10.1645/GE-2123.1 PMID: 19860532
42. Loiseau C, Harrigan RJ, Robert A, Bowie RCK, Thomassen HA, Smith TB, et al. Host and habitat specialization of avian malaria in Africa. Mol Ecol. 2011; 21: 431-441. doi: 10.1111/j.1365-294X.2011.05341.x PMID: 22142265
43. Belo NO, Pinheiro RT, Reis ES, Ricklefs RE, Braga ÉM. Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil. PLOS ONE. 2011; 6: e17654. doi: 10.1371/ journal.pone.0017654 PMID: 21408114
44. Ishtiaq F, Beadell JS, Warren BH, Fleischer RC. Diversity and distribution of avian haematozoan parasites in the Western Indian Ocean region: a molecular survey. Parasitol. 2012; 139: 221-231.
45. Lacorte GA, Félix GMF, Pinheiro RRB, Chaves AV, Almeida-Neto G, Neves FS, et al. Exploring the diversity and distribution of neotropical avian malaria parasites-a molecular survey from Southeast Brazil. PLOS ONE 2013; 8: e57770. doi: 10.1371/journal.pone.0057770 PMID: 23469235
46. Fecchio A, Lima MR, Svensson-Coelho M, Marini MA, Ricklefs RE. Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitol. 2013; 140: 181-192.
47. Svensson-Coelho M, Blake JG, Loiselle BA, Penrose AS, Parker PG, Ricklefs RE. Diversity Prevalence and Host-specificity of Avian Plasmodium and Haemoproteus in a Western Amazon Assemblage. Ornithol Monogr. 2013; No. 76.
48. Clark NJ, Clegg SM, Lima MR. A review of global diversity in avian haemosporidians Plasmodium and Haemoproteus: Haemosporida: new insights from molecular data. Int J Parasitol. 2014; 44: 329-38. doi: 10.1016/j.ijpara.2014.01.004 PMID: 24556563
49. Engel JI, Bates JM, Weckstein JD, Gnoske TP, Kaliba PM. An avifaunal survey of Vwaza Marsh Wildlife Reserve Malawi. J East Afr Nat Hist 2012; 101: 223-240.
50. Hellgren O, Waldenström H, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. J Parasitol. 2004; 90: 797-802. PMID: 15357072
51. Waldenström J, Bensch S, Hasselquist D, Östman Ö. A new nested polymerase chain reaction methods very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol. 2004; 90: 191-194. PMID: 15040694
52. Fallon SM, Ricklefs RE, Swanson BL, Bermingham E. Detecting avian malaria: an improved polymerase chain reaction diagnostic. J Parasitol. 2003; 89: 1044-1047. PMID: 14627154
53. Richard FA, Sehgal RNM, Jones HI, Smith TB. A comparative analysis of PCR-based detection methods for avian malaria. J Parasitol. 2002; 88: 819-822. PMID: 12197145
54. Freed LA, Cann RL. DNA quality and accuracy of avian malaria PCR diagnostics: a review. Condor 2006; 108: 459-473.
55. Hellgren O, Križanauskiene A, Valki nas G, Bensch S. Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus Haemosporida: Haemoproteidae. J Parasitol. 2007; 93: 889-896. PMID: 17918371
56. Valkiunas G, Zehtindjiev P, Dimitrov D, Križanauskienė A, Iezhova TA, Bensch S. Polymerase chain re-action-based identification of Plasmodium Huffia elongatum with remarks on species lineages deposited in GenBank. Parasitol Res. 2008; 102: 1185-1193. doi: 10.1007/s00436-008-0892-9 PMID: 18270739
57. 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. Molecular Ecology Res. 2009; 9: 1353-1358. doi: 10.1111/j.1755-0998.2009.02692.x PMID: 21564906
58. Withers PC. Models of diffusion-mediated gas exchange in animal burrows. Am Nat. 1978; 112: 1101-1112.
59. Wickler SJ, Marsh RL. Effects of nestling age and burrow depth on CO2 and O2 concentrations in the burrows of bank swallows Riparia riparia. Physiol Zool. 1980; 54: 132-136.
60. Logan JG, Cook JI, Mordue (Luntz) AJ, Kline DL. Understanding and exploiting olfaction for the surveillance and control of Culicoides biting midges. Olfaction in vector-host interactions. In: Takken W, Knols BGJ, editors. Ecology and control of vector-borne diseases Vol. 2. Wageningen, Netherlands: Wageningen Academic Publishers; 2010. pp. 217-246.
61. Brown L, Urban EK, Newman K. The Birds of Africa: Vol. I. Academic Press London UK; 1982.
62. Fry CH, Keith S, Urban EK. The Birds of Africa: Vol. III. Academic Press London UK; 1988.
63. Urban EK, Fry CH, Keith S. The Birds of Africa: Vol. II. Academic Press London UK; 1986.
64. Keith S, Urban EK, Fry CH. The Birds of Africa. Vol. IV. Academic Press London UK; 1992.
65. Urban EK, Fry CH, Keith S. The Birds of Africa Vol. V. Academic Press London UK; 1997.
66. Fry CH, Keith S, Urban EK. The Birds of Africa: Vol. VI. Academic Press London UK; 2002.
67. Fry CH, Keith S. The Birds of Africa: Vol. VII. Academic Press London UK; 2004.
68. Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd ed. New York: Springer-Verlag; 2002.
69. Bates D, Maechler M, Bolker BM, Walker S. lme4: Linear mixed-effects models using S4 classes; 2012. R package version 1.1-7. Available: http://CRAN.R-project.org/package = lme4.
70. Mazerolle MJ. AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c); 2013. R package version 1.21. Available: http://CRAN.R-project.org/package=AICcmodavg.
71. Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest: Tests in linear mixed effects models; 2013. R package version 2.0-20, http://CRAN.R-project.org/package=lmerTest.
72. Read AF. Passerine polygyny: A role for parasites? Am Nat. 1991; 138: 434-459.
73. Ricklefs RE, Swanson BL, Fallon SM, Martínez-Abraín A, Scheuerlein A, Gray J, et al. Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr. 2005; 75: 543-559.
74. Sehgal RNM, Buermann W, Harrigan RJ, Bonneaud C, Loiseau C, Chasar A, et al. Spatially explicit predictions of blood parasites in a widely African rainforest bird. Proc Roy Soc B. 2011; 10: 1025-1033.
75. Fecchio A, Lima MR, Silveria P, Braga ÉM, Marini MÂ. High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu 2011; 111: 132-138.
76. González AD, Matta NE, Ellis VA, Miller ET, Ricklefs RE, Gutiérrez HR. Mixed species flock nest height and elevation partially explain avian haemoparasite prevalence in Colombia. PLOS ONE 2014; 9: e100695. doi: 10.1371/journal.pone.0100695 PMID: 24950223
77. Khan AA. Mosquito attractants and repellents. In: Shorey HH, McKelvey JJ, editors. Chemical Control of Insect Behavior. New York: John Wiley & Sons; 1977. pp. 91-98.
78. Takken W. The role of olfaction in host-seeking mosquitoes -a review. Int J Trop Insect Sci. 1991; 12: 287-295.
79. Muir LE, Thorne JE, Kay BH. Aedes aegypti Diptera: Culicidae vision-spectral sensitivity and other perceptual parameters of the female eye. J Med Entomol. 1992; 29: 278-281. PMID: 1495042
80. Bidlingmayer WL. How mosquitoes see traps-role of visual responses. J Am Mosq Control Assoc. 1994; 10: 272-279. PMID: 8965079
81. Bernier UR, Booth MM, Yost RA. Analysis of human skin emanations by gas chromatography mass spectrometry. 1. Thermal desorption of attractants for the yellow fever mosquito Aedes aegypti from handled glass beads. Anal Chem. 1999; 71: 1-7. PMID: 9921122
82. Bishop AL. The response of Culicoides brevitarsis to livestock under cover. Report to Biosecurity Australia, Canberra, ACT, Australia. 2002.
83. Bishop AL, McKenzie HJ, Spohr LJ. Attraction of Culicoides brevitarsis Kieffer Diptera: Ceratopogonidae and Culex annulirostris Skuse Diptera: Culicidae to simulated visual and chemical stimuli from cattle. Aust J Entomol. 2008; 47: 121-127.
84. Muller M. Report of the Bluetongue Research Management Committee 11-13 September Brisbane Australia. 1991.
85. Savage AF, Robert V, Goodman SM, Raharimanga V, Raherilalao MJ, Andrianarimisa A, et al. Blood parasites in birds from Madagascar. J Wildl Dis. 2009; 45: 907-920. PMID: 19901367
86. Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, et al. Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol. 2004; 13: 3289-3844.
87. Ewen JG, Bensch S, Blackburn TM, Bonneaud C, Brown R, Cassey P, et al. Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecol Lett 2012; 15: 1112-1119. doi: 10.1111/j.1461-0248.2012.01833.x PMID: 22788956
88. Greiner EC, Bennett GF, White EM, Coombs RF. Distribution of avian hematozoa of North America. Can J Zool. 1975; 53: 1762-1787. PMID: 1212636
89. Young BE, Garvin MC, McDonald DB. Blood parasites in birds from Monteverde Costa Rica. J Wildl Dis. 1993; 29: 555-560. PMID: 8258853
90. Fallon SM, Bermingham E, Ricklefs RE. Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat. 2005; 165: 466-480. PMID: 15791538
91. Sousa OE, Herman CM. Blood parasites of birds from Chiriqui and Panama provinces in the Republic of Panama. J Wildl Dis. 1982; 18: 205-221. PMID: 7097883
92. Bennett GF, Garvin M, Bates JM. Avian hematozoa from east-central Bolivia. The J Parasitol. 1991; 77: 207-211. PMID: 1901358
93. Ribeiro SF, Sabaio F, Branquinho FCS, Marini MÂ, Vago AR, Braga ÉM. Avian malaria in Brazilian passerine birds: parasitism detected by nest PCR using DNA from stained blood smears. Parasitol. 2004; 130: 261-267.
94. Durrant KL, Beadell JS, Ishtiaq F, Graves GR, Olson SL, Gering E, et al. Avian hematozoa in South America: a comparison of temperate and tropical zones. Ornithol Monogr. 2006; 60: 98-111.
95. Londoño A, Pulgarin-R PC, Blair S. Blood parasites in birds from the lowlands of Northern Colombia. Caribb J Sci. 2007; 43: 87-93.
96. Merino S, Moreno J, Vásquez RA, Martínez J, Sánchez-Monsálvez I, Estades CF, et al. Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecol. 2008; 33: 329-340.
97. Rodríguez OA, Moya H, Matta NE. Avian blood parasite in the National Natural Park Chingaza: high Andes of Colombia. Hornero 2009; 24: 1-6.
98. Mijares A, Rosales R, Silva-Iturriza A. Hemosporidian parasites in forest birds from Venezuala: genetic lineage analyses. Avian Dis. 2012; 56: 583-588. PMID: 23050478
99. Dowsett-Lemaire F, Dowsett RJ. The Birds of Malawi. Liége Belgium: Tauraco Press & Aves; 2006.