期刊论文详细信息
Particle and Fibre Toxicology
An experimental test of the effects of behavioral and immunological defenses against vectors: do they interact to protect birds from blood parasites?
Dale H Clayton1  Jeb P Owen3  Autumn R Henry1  Jessica L Waite2 
[1] Department of Biology, University of Utah, Salt Lake City, UT 84112, USA;Center for Infectious Disease Dynamics and Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA;Department of Entomology, Washington State University, Pullman, WA 99164, USA
关键词: Defensive behavior;    Arthropod saliva;    Pseudolynchia canariensis;    Hippoboscid;    Columba livia;    Haemoproteus columbae;   
Others  :  810527
DOI  :  10.1186/1756-3305-7-104
 received in 2013-12-05, accepted in 2014-03-04,  发布年份 2014
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【 摘 要 】

Background

Blood-feeding arthropods can harm their hosts in many ways, such as through direct tissue damage and anemia, but also by distracting hosts from foraging or watching for predators. Blood-borne pathogens transmitted by arthropods can further harm the host. Thus, effective behavioral and immunological defenses against blood-feeding arthropods may provide important fitness advantages to hosts if they reduce bites, and in systems involving pathogen transmission, if they lower pathogen transmission rate.

Methods

We tested whether Rock Pigeons (Columba livia) have effective behavioral and immunological defenses against a blood-feeding hippoboscid fly (Pseudolynchia canariensis) and, if so, whether the two defenses interact. The fly vectors the blood parasite Haemoproteus columbae; we further tested whether these defenses reduced the transmission success of blood parasites when birds were exposed to infected flies. We compared four experimental treatments in which hosts had available both purported defenses, only one of the defenses, or no defenses against the flies.

Results

We found that preening and immunological defenses were each effective in decreasing the survival and reproductive success of flies. However, the two defenses were additive, rather than one defense enhancing or decreasing the effectiveness of the other defense. Neither defense reduced the prevalence of H. columbae, nor the intensity of infection in birds exposed to infected flies.

Conclusions

Flies experience reduced fitness when maintained on hosts with immunological or preening defenses. This suggests that if vectors are given a choice among hosts, they may choose hosts that are less defended, which could impact pathogen transmission in a system where vectors can choose among hosts.

【 授权许可】

   
2014 Waite et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P: Global trends in emerging infectious diseases. Nature 2008, 451:990-993.
  • [2]Townson H, Nathan MB, Zaim M, Guillet P, Manga L, Bos R, Kindhauser M: Exploiting the potential of vector control for disease prevention. Bull World Health Organ 2005, 83:942-947.
  • [3]Dobson A, Foufopoulos J: Emerging infectious pathogens of wildlife. Philos Trans R Soc Lond B Biol Sci 2001, 356:1001-1012.
  • [4]Clayton DH, Tompkins DM: Comparative effects of mites and lice on the reproductive success of rock doves (Columba livia). Parasitology 1995, 110:195-206.
  • [5]Koop JAH, Huber SK, Clayton DH: Does sunlight enhance the effectiveness of avian preening for ectoparasite control? J Parasitol 2012, 98:46-48.
  • [6]Gillespie RD, Mbow ML, Titus RG: The immunomodulatory factors of bloodfeeding arthropod saliva. Parasite Immunol 2000, 22:319-331.
  • [7]Champagne DE: Antihemostatic strategies of blood-feeding arthropods. Curr Drug Targets Cardiovasc Haematol Disord 2004, 4:375-396.
  • [8]Owen JP, Nelson AC, Clayton DH: Ecological immunology of bird-ectoparasite systems. Trends Parasitol 2010, 26:530-539.
  • [9]Moreno-Cid JA, de JMP l L, Villar M, Jiménez M, Pinal R, Estrada-Peña A, Molina R, Lucientes J, Gortázar C, la Fuente de J, the SUB/AKR Vaccine Study Group: Control of multiple arthropod vector infestations with subolesin/akirin vaccines. Vaccine 2013, 31:1187-1196.
  • [10]Edman J, Kale H II: Host behavior: its influence on the feeding success of mosquitoes. Ann Entomol Soc Am 1970, 64:513-516.
  • [11]Darbro JM, Harrington LC: Avian defensive behavior and blood-feeding success of the West Nile vector mosquito, Culex pipiens. Behav Ecol 2007, 18:750-757.
  • [12]Leitner WW, Wali T, Costero-Saint Denis A: Is arthropod saliva the Achilles’ heel of vector-borne diseases? Front Immunol 2013, 4:255.
  • [13]Andrade BB, Teixeira CR, Barral A, Barral-Netto M: Haematophagous arthropod saliva and host defense system: a tale of tear and blood. An Acad Bras Cienc 2005, 77:665-693.
  • [14]Trager W: Acquired immunity to ticks. J Parasitol 1939, 25:57-81.
  • [15]Milleron R, Ribeiro J, Elnaime D, Soong L, Lanzaro G: Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. Am J Trop Med Hyg 2004, 70:278-285.
  • [16]Acton HW, Knowles R: Studies on the halteridium parasite of the pigeon, Haemoproteus columbae Celli and San Felice. Indian J Med Res 1914, 1:663-690.
  • [17]Sol D, Jovani R, Torres J: Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds. Oecologia 2003, 135:542-547.
  • [18]Coatney GR: Relapse and associated phenomena in the Haemoproteus infection of the pigeon. Am J Hyg 1933, 18:133-160.
  • [19]Arcoverde AR, Rodrigues AFSF, Daemon E: Feeding and breeding aspects of Pseudolynchia canariensis (Macquart, 1839) (Diptera, Hippoboscidae) under laboratory conditions. Parasitol Res 2009, 104:277-280.
  • [20]Adie H: The sporogony of Haemoproteus columbae. Indian J Med Res 1915, 2:671-680.
  • [21]Herath PRJ: Colonizing Pseudolynchia canariensis on hosts other than the pigeon, Columba livia. Detroit, MI: Wayne State University; 1966.
  • [22]Klei TR: Studies on Haemoproteus columbae of the pigeon, Columba livia, and the intermediate host Pseudolynchia canariensis. Detroit, MI: Wayne State University; 1971.
  • [23]Bishopp FC: The pigeon fly - an important pest of pigeons in the United States. J Econ Entomol 1929, 22:947-987.
  • [24]Waite JL, Henry AR, Clayton DH: How effective is preening against mobile ectoparasites? An experimental test with pigeons and hippoboscid flies. Int J Parasitol 2012, 42:463-467.
  • [25]Bush SE, Clayton DH: The role of body size in host specificity: reciprocal transfer experiments with feather lice. Evolution 2006, 60:2158-2167.
  • [26]Mohammed A-H: Systematic and Experimental Studies on Protozoal Blood Parasites of Egyptian Birds. Cairo, Egypt: Cairo University Press; 1958.
  • [27]Schat K, Kaspers B, Kaiser P: Avian Immunology. 2nd edition. London: Elsevier Ltd; 2013.
  • [28]Adie H: The sporogony of Haemoproteus columbae. Bull Soc Pathol Exot 1924, 17:605-613.
  • [29]Moyer B, Gardiner D, Clayton DH: Impact of feather molt on ectoparasites: looks can be deceiving. Oecologia 2002, 131:203-210.
  • [30]Ahmed FE, Mohammed A-HH: Haemoproteus columbae: course of infection, relapse and immunity to reinfection in the pigeon. Z Parasitenkd 1978, 57:229-236.
  • [31]Ahmed FE, Mohammed A-HH: Studies of growth and development of gametocytes in Haemoproteus columbae Kruse. J Protozool 1978, 25:174-177.
  • [32]Huber SK, Owen JP, Koop JAH, King MO, Grant PR, Grant BR, Clayton DH: Ecoimmunity in Darwin’s finches: invasive parasites trigger acquired immunity in the medium ground finch (Geospiza fortis). PLoS ONE 2010, 5:e8605.
  • [33]Development Core Team R: R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria. 2011 http://www.R-project.org/ webcite
  • [34]Therneau T, Lumley T: Survival: survival analysis including penalized likelihood. R package version 2.36-5. 2011 http://CRAN.R-project.org/package=survival webcite
  • [35]Waite JL, Henry AR, Adler FR, Clayton DH: Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis. Ecology 2012, 93:2448-2455.
  • [36]Bates D, Maechler M, Bolker B: lme4: Linear mixed-effects models using S4 classes. 2011 http://CRAN.R-project.org/package=lme4 webcite
  • [37]Pollitt LC, Reece SE, Mideo N, Nussey DH, Colegrave N: The problem of auto-correlation in parasitology. PLoS Pathog 2012, 8:e1002590.
  • [38]Sachs J, Malaney P: The economic and social burden of malaria. Nature 2002, 415:680-685.
  • [39]Mans BJ: Evolution of vertebrate hemostatic and inflammatory control mechanisms in blood-feeding arthropods. J Innate Immun 2011, 3:41-51.
  • [40]Randolph SE, Nuttall PA: Nearly right or precisely wrong? Natural versus laboratory studies of vector-borne diseases. Parasitol Today 1994, 10:458-462.
  • [41]Titus R, Bishop J, Mejia J: The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol 2006, 28:131-141.
  • [42]Alger NE, Harant JA, Willis LC, Jorgensen GM: Sporozoite and normal salivary gland induced immunity in malaria. Nature 1972, 238:341.
  • [43]Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D: Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 2000, 290:1351-1354.
  • [44]Donovan MJ, Messmore AS, Scrafford DA, Sacks DL, Kamhawi S, McDowell MA: Uninfected mosquito bites confer protection against infection with malaria parasites. Infect Immun 2007, 75:2523-2530.
  • [45]Gomes R, Teixeira C, Teixeira M, Oliveira F, Menezes M, Silva C, de Oliveira C, Miranda J, Elnaiem D-E, Kamhawi S, Valenzuela J, Brodskyn C: Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc Natl Acad Sci U S A 2008, 105:7845-7850.
  • [46]Davies C, Mazloumi Gavgani A: Age, acquired immunity and the risk of visceral leishmaniasis: a prospective study in Iran. Parasitology 1999, 119:247-257.
  • [47]Ferguson HM, Mackinnon MJ, Chan BH, Read AF: Mosquito mortality and the evolution of malaria virulence. Evolution 2003, 57:2792-2804.
  • [48]Vardo-Zalik AM, Schall JJ: Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology 2009, 90:529-536.
  • [49]Levin I, Parker J: Infection with Haemoproteus iwa affects vector movement in a hippoboscid fly - frigatebird system. Mol Ecol 2014, 23:750-752.
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