Particle and Fibre Toxicology | |
Avian roosting behavior influences vector-host interactions for West Nile virus hosts | |
A Marm Kilpatrick2  Peter P Marra3  William M Janousek1  | |
[1] Current address: Avian Science Center, Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, Montana 59802, USA;Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064, USA;Migratory Bird Center, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20008, USA | |
关键词: Evolution; Fitness; Flocking; Model; Vector:host ratio; Vector-host contact rates; Group size; Sociality; | |
Others : 1150803 DOI : 10.1186/1756-3305-7-399 |
|
received in 2014-06-11, accepted in 2014-08-22, 发布年份 2014 | |
【 摘 要 】
Background
Extensive work has shown that vectors almost never feed at random. Often, a subset of individual hosts and host species are fed on much more frequently than expected from their abundance and this can amplify pathogen transmission. However, the drivers of variation in contact patterns between vectors and their hosts are not well understood, even in relatively well-studied systems such as West Nile virus (WNV).
Methods
We compared roosting height and roost aggregation size of seven avian host species of WNV with patterns of host-seeking mosquito (Culex pipiens) abundance at communal and non-communal roost sites.
Results
First, host-seeking mosquito abundance increased with height and paralleled increased mosquito feeding preferences on species roosting higher in the tree canopy. Second, there were several hundred-fold fewer mosquitoes per bird trapped at American robin (Turdus migratorius) communal roosts compared to non-communal roost sites, which could reduce transmission from and to this key amplifying host species. Third, seasonal changes in communal roost formation may partly explain observed seasonal changes in mosquito feeding patterns, including a decrease in feeding on communal roosting robins.
Conclusions
These results illustrate how variation in habitat use by hosts and vectors and social aggregation by hosts influence vector-host interactions and link the behavioral ecology of birds and the transmission of vector-borne diseases to humans.
【 授权许可】
2014 Janousek et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150405225223201.pdf | 630KB | download | |
Figure 4. | 18KB | Image | download |
Figure 3. | 48KB | Image | download |
Figure 2. | 43KB | Image | download |
Figure 1. | 43KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC: Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annu Rev Ecol Evol Syst 2003, 34:517-547.
- [2]Johnson CK, Tinker MT, Estes JA, Conrad PA, Staedler M, Miller MA, Jessup DA, Mazet JAK: Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. Proc Natl Acad Sci U S A 2009, 106(7):2242-2247.
- [3]Paull SH, Song SJ, McClure KM, Sackett LC, Kilpatrick AM, Johnson PTJ: From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ 2012, 10(2):75-82.
- [4]Venesky MD, Kerby JL, Storfer A, Parris MJ: Can differences in host behavior drive patterns of disease prevalence in tadpoles? Plos One 2011, 6(9):e24991.
- [5]Moore CG: Interdisciplinary research in the ecology of vector-borne diseases: opportunities and needs. J Vector Ecol 2008, 33(2):218-224.
- [6]Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM: Bird-biting mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Inf Gen Evol 2011, 11:1577-1585.
- [7]Cohen JE, Gurtler RE: Modeling household transmission of American trypanosomiasis. Science 2001, 293(5530):694-698.
- [8]Martens P, Hall L: Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 2000, 6(2):103-109.
- [9]Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Soldan VP, Kochel TJ, Kitron U, Elder JP, Scott TW: The role of human movement in the transmission of vector-borne pathogens. PLoS Negl Trop Dis 2009, 3(7):e481.
- [10]Kilpatrick AM, Randolph SE: Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 2012, 380(9857):1946-1955.
- [11]Kilpatrick AM: Globalization, land use, and the invasion of West Nile virus. Science 2011, 334(6054):323-327.
- [12]Takken W, Verhulst NO: Host preferences of blood-feeding mosquitoes. Annu Rev Entomol 2013, 58:433-453.
- [13]Ngom EM, Ndione JA, Ba Y, Konate L, Faye O, Diallo M, Dia I: Spatio-temporal analysis of host preferences and feeding patterns of malaria vectors in the sylvo-pastoral area of Senegal: impact of landscape classes. Paras Vec 2013, 6:332. BioMed Central Full Text
- [14]Kelly DW, Thompson CE: Epidemiology and optimal foraging: modelling the ideal free distribution of insect vectors. Parasitology 2000, 120:319-327.
- [15]Hamilton WD: Geometry for the selfish herd. J Theor Biol 1971, 31(2):295-311.
- [16]Mooring MS, Hart BL: Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 1992, 123:173-193.
- [17]Anderson J, Nilssen A: Do reindeer aggregate on snow patches to reduce harassment by parasitic flies or to thermoregulate? Rangifer 1998, 18:3-17.
- [18]Helle T, Aspi J: Does herd formation reduce insect harassment among reindeer? A field experiment with animal traps. Acta Zool Fenn 1983, 175:129-131.
- [19]Brown CR, Sethi RA: Mosquito abundance is correlated with Cliff Swallow (Petrochelidon pyrrhonota) colony size. J Med Entomol 2002, 39(1):115-120.
- [20]Poulin R: Group-living and infestation by ectoparasites in Passerines. Condor 1991, 93(2):418-423.
- [21]Cote IM, Poulin R: Parasitism and group size in social animals: a meta-analysis. Behav Ecol 1995, 6(2):159-165.
- [22]Kilpatrick AM, Kramer LD, Campbell S, Alleyne EO, Dobson AP, Daszak P: West Nile virus risk assessment and the bridge vector paradigm. Emerg Infect Dis 2005, 11(3):425-429.
- [23]Turell MJ, Sardelis MR, O'Guinn ML, Dohm DJ: Potential vectors of West Nile virus in North America. In Japanese Encephalitis and West Nile Viruses. Edited by Mackenzie J, Barrett A, Deubel V. Berlin: Springer; 2002:241-252. [Current Topics in Microbiology and Immunology, Volume 267]
- [24]Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED: Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile virus to humans. J Med Entomol 2008, 45(1):125-128.
- [25]Ciota AT, Chin PA, Kramer LD: The effect of hybridization of Culex pipiens complex mosquitoes on transmission of West Nile virus. Paras Vec 2013, 6:305. BioMed Central Full Text
- [26]Hamer GL, Chaves LF, Anderson TK, Kitron UD, Brawn JD, Ruiz MO, Loss SR, Walker ED, Goldberg TL: Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. Plos One 2011, 6(8):e23767.
- [27]Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED: Host selection by Culex pipiens mosquitoes and West Nile virus amplification. Am J Trop Med Hyg 2009, 80(2):268-278.
- [28]Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD: Host heterogeneity dominates West Nile virus transmission. Proc R Soc B 2006, 273(1599):2327-2333.
- [29]Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P: West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol 2006, 4(4):606-610.
- [30]Kent R, Juliusson L, Weissmann M, Evans S, Komar N: Seasonal blood feeding behavior of Culex tarsalis (Diptera: Culicidae) in Weld County, Colorado, 2007. J Med Entomol 2009, 46(2):380-390.
- [31]Kilpatrick AM, LaDeau SL, Marra PP: Ecology of West Nile virus transmission and its impact on birds in the western hemisphere. Auk 2007, 124(4):1121-1136.
- [32]Anderson RA, Brust RA: Interrupted blood feeding by Culex (Diptera: Culicidae) in relation to individual host tolerance to mosquito attack. J Med Entomol 1997, 34(2):95-101.
- [33]Edman J, Webber L, Kale H: Effect of mosquito density of interrelationship of host behavior and mosquito feeding success. Am J Trop Med Hyg 1972, 21(4):487-491.
- [34]Hodgson JC, Spielman A, Komar N, Krahforst CF, Wallace GT, Pollack RJ: Interrupted blood-feeding by Culiseta melanura (Diptera: Culicidae) on European starlings. J Med Entomol 2001, 38(1):59-66.
- [35]Scott TW, Lorenz LH, Edman JD: Effects of house sparrow age and arbovirus infection on attraction of mosquitos. J Med Entomol 1990, 27(5):856-863.
- [36]Anderson JF, Andreadis TG, Main AJ, Ferrandino FJ, Vossbrinck CR: West Nile virus from female and male mosquitoes (Diptera : Culicidae) in subterranean, ground, and canopy habitats in Connecticut. J Med Entomol 2006, 43(5):1010-1019.
- [37]Deegan CS, Burns JE, Huguenin M, Steinhaus EY, Panella NA, Beckett S, Komar N: Sentinel pigeon surveillance for West Nile virus by using lard-can traps at differing elevations and canopy cover classes. J Med Entomol 2005, 42(6):1039-1044.
- [38]Drummond CL, Drobnack J, Backenson PB, Ebel GD, Kramer LD: Impact of trap elevation on estimates of abundance, parity rates, and body size of Culex pipiens and Culex restuans (Diptera : Culicidae). J Med Entomol 2006, 43(2):177-184.
- [39]Savage HM, Anderson M, Gordon E, McMillen L, Colton L, Delorey M, Sutherland G, Aspen S, Charnetzky D, Burkhalter K, Godsey M: Host-seeking heights, host-seeking activity patterns, and West Nile virus infection rates for members of the Culex pipiens complex at different habitat types within the hybrid zone, Shelby County, TN, 2002 (Diptera: Culicidae). J Med Entomol 2008, 45(2):276-288.
- [40]Diuk-Wasser MA, Molaei G, Simpson JE, Folsom-O'Keefe CM, Armstrong PM, Andreadis TG: Avian communal roosts as amplification foci for West Nile virus in urban areas in northeastern United States. Am J Trop Med Hyg 2010, 82(2):337-343.
- [41]Benson TJ, Ward MP, Lampman RL, Raim A, Weatherhead PJ: Implications of spatial patterns of roosting and movements of American robins for West Nile virus transmission. Vector-Borne Zoonotic Dis 2012, 12(10):877-885.
- [42]MacDonald G: The Epidemiology and Control of Malaria. London: Oxford University Press; 1957.
- [43]Ross R: The prevention of malaria. London: John Murray; 1910.
- [44]Savage HM, Aggarwal D, Apperson CS, Katholi CR, Gordon E, Hassan HK, Anderson M, Charnetzky D, McMillen L, Unnasch EA, Unnasch TR: Host choice and West Nile virus infection rates in blood fed mosquitoes, including members of the Culex pipiens complex, from Memphis and Shelby County, Tennessee 2002–2003. Vector-Borne Zoonotic Dis 2007, 7(3):365-386.
- [45]Bernard KA, Maffei JG, Jones SA, Kauffman EB, Ebel GD, Dupuis AP, Ngo KA, Nicholas DC, Young DM, Shi PY, Kulasekera VL, Edison M, White DJ, Stone WB, Kramer LD, NY State West Nile Virus Surveillance Team: West Nile virus infection in birds and mosquitoes, New York State, 2000. Emerg Infect Dis 2001, 7(4):679-685.
- [46]Cochran W: Wildlife Telemetry. In The Wildlife Management Techniques Manual. 4th edition. Edited by SD S. Washington: The Wildlife Society; 1980:507-520.
- [47]Hamer GL, Walker ED, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Schotthoefer AM, Brown WM, Wheeler E, Kitron UD: Rapid amplification of West Nile virus: the role of hatch-year birds. Vector-Borne Zoonotic Dis 2008, 8(1):57-67.
- [48]Rappole JH, Tipton AR: New harness design for attachment of radio transmitters to small passerines. J Field Ornithology 1991, 62(3):335-337.
- [49]Wanless S, Harris MP, Morris JA: Foraging range and feeding locations of shags Phalacrocorax aristotelis during chick rearing. Ibis 1991, 133(1):30-36.
- [50]Smith JAM, Reitsma LR, Rockwood LL, Marra PP: Roosting behavior of a Neotropical migrant songbird, the northern waterthrush Seiurus noveboracensis, during the non-breeding season. J Avian Biol 2008, 39(4):460-465.
- [51]Gillies M, Wilkes T: The range of attraction of single baits for some West African mosquitoes. Bull Entomol Res 1970, 60:225-235.
- [52]Darsie RFJ, Ward RA: Identification and geographic distribution of mosquitoes of North America, north of Mexico. Mosq Syst Suppl 1981, 1:1-313.
- [53]Crabtree MB, Savage HM, Miller BR: Development of a species-diagnostic polymerase chain reaction assay for the identification of Culex vectors of St. Louis encephalitis virus based on interspecies sequence variation in ribosomal DNA spacers. Am J Trop Med Hyg 1995, 53:105-109.
- [54]Nagy KA, Girard IA, Brown TK: Energetics of free-ranging mammals, reptiles and birds. Annu Rev Nutr 1999, 19:247-277.
- [55]Ward MP, Raim A, Yaremych-Hamer S, Lampman R, Novak RJ: Does the roosting behavior of birds affect transmission dynamics of West Nile virus? Am J Trop Med Hyg 2006, 75(2):350-355.
- [56]Morrison D, Caccamise D: Comparison of roost use by three species of communal roostmates. Condor 1990, 92:405-412.
- [57]Ward P, Zahavi A: The importance of certain assemblages of birds as “information-centres” for food-finding. Ibis 1973, 115(4):517-534.
- [58]VanDalen KK, Hall JS, Clark L, McLean RG, Smeraski C: West Nile virus infection in American robins: new insights on dose response. Plos One 2013, 8(7):e68537.
- [59]Kilpatrick AM: Facilitating the evolution of resistance to avian malaria in Hawaiian birds. Biol Conserv 2006, 128(4):475-485.