Skip to main content

Advertisement

SpringerLink
Log in

Anthropogenic disturbance and the risk of flea-borne disease transmission

  • Global change ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Anthropogenic disturbance may lead to the spread of vector-borne diseases through effects on pathogens, vectors, and hosts. Identifying the type and extent of vector response to habitat change will enable better and more accurate management strategies for anthropogenic disease spread. We compiled and analyzed data from published empirical studies to test for patterns among flea and small mammal diversity, abundance, several measures of flea infestation, and host specificity in 70 small mammal communities of five biomes and three levels of human disturbance: remote/wild areas, agricultural areas, and urban areas. Ten of 12 mammal and flea characteristics showed a significant effect of disturbance category (six), biome (four), or both (two). Six variables had a significant interaction effect. For mammal-flea communities in forest habitats (39 of the 70 communities), disturbance affected all 12 characteristics. Overall, flea and mammal richness were higher in remote versus urban sites. Most measures of flea infestation, including percent of infested mammals and fleas/mammal and fleas/mammal species increased with increasing disturbance or peaked at intermediate levels of disturbance. In addition, host use increased, and the number of specialist fleas decreased, as human disturbance increased. Of the three most common biomes (forest, grassland/savanna, desert), deserts were most sensitive to disturbance. Finally, sites of intermediate disturbance were most diverse and exhibited characteristics associated with increased disease spread. Anthropogenic disturbance was associated with conditions conducive to increased transmission of flea-borne diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achuthan C, Chandrahas RK (1971) Seasonal prevalence of rat fleas in Kolar (Mysore State). Indian J Med Res 59:833–837

    CAS  PubMed  Google Scholar 

  • Adler GH, Suntsova NI, Suntsov VV, Mangan SA (2001) Fleas (Siphonaptera) collected from small mammals in Southern Viet Nam in 1997–1998. J Med Entomol 38:210–213

    Article  CAS  PubMed  Google Scholar 

  • Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM (1997) Flea-borne rickettsioses, ecologic considerations. Emerg Infect Dis 3:319–327

    Article  CAS  PubMed  Google Scholar 

  • Bengston SA, Brinck-Lindroth G, Lundquvist L, Nilsson A, Rundgren S (1986) Ectoparasites on small mammals in Iceland: origin and population characteristics of a species-poor insular community. Holarctic Ecol 9:143–148

    Google Scholar 

  • Bossard M (2006) Mammal and flea relationships in the Great Basin Desert: from H. J. Egoscue’s collections. J Parasitol 92:260–266

    Article  PubMed  Google Scholar 

  • Bossi DEP, Linhares AX, de Godoy Bergallo H (2002) Parasitic arthropods of some wild rodents from Juréia-Itatins Ecological Station, State of São Paulo. Braz Mem Instit Oswaldo Cruz 7:959–963

    Google Scholar 

  • Bradley CA, Altizer S (2006) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22:95–102

    Article  PubMed  Google Scholar 

  • Campos EG, Maupin GO, Barnes AM, Eads RB (1985) Seasonal occurrence of fleas (Siphonaptera) on rodents in a foothills habitat in Larimer County, Colorado, USA. J Med Entomol 22:266–270

    Google Scholar 

  • Castleberry SB, Castleberry NI, Wood PB, Ford WM, Mengak MT (1983) Flea (Siphonaptera) of the Allegheny woodrat (Neotoma magister) in West Virginia with comments on host specificity. Am Midl Nat 149:233–236

    Article  Google Scholar 

  • Chandrahas RK, Krishnaswami AK (1971) Host preference of Siphonaptera on wild rodents in the south Indian plague focus. Indian J Med Res 59:1807–1815

    Google Scholar 

  • Chenchijtikul M, Daengpium S, Hasegawa M, Itoh T, Phanthumadchinda B (1983) A study of commensal rodents and shrews with reference to the parasites of medical importance in Chanthaburi Province, Thailand. Southeast Asian J Trop Med Public Health 14:255–259

    Google Scholar 

  • Cole LC, Koepke JA (1947) Problems of interpretation of the data of rodent-ectoparasite surveys and studies of rodent ectoparasites in Honolulu, HI, Savannah, GA, and Dothan, AL. Public Health Rep Suppl 202:1–71

    Google Scholar 

  • Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, Cully JF Jr, Gage KL, Kosoy MY, Loye JE, Martin AP (2005) Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landsc Ecol 20:941–955

    Article  Google Scholar 

  • Coultrip RL, Emmons RW, Legsters L J, Marshall Jr JD, Murray KF (1973) Survey for the arthropod vectors and mammalian host of Rocky Mountain spotted fever and plague at Fort Ord, California. J Med Entomol 10:303–309

    Google Scholar 

  • Crowl TA, Crist TO, Parmenter RR, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol 6:238–246

    Article  Google Scholar 

  • Cumming GS, Van Vuuren DP (2006) Will climate change affect ectoparasite species ranges? Glob Ecol Biogeogr 15:486–497

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious disease in wildlife. Acta Trop 78:103–116

    Article  CAS  PubMed  Google Scholar 

  • Davis RM, Smith RT, Madon MB, Sitko-Cleugh E (2002) Flea, rodent, and plague ecology at Chuchupate Campground, Ventura County, California. J Vector Ecol 27:107–127

    Google Scholar 

  • Deem SL, Kilbourn AM, Wolfe ND, Cook RA, Karesh WB (2001) Conservation medicine. Ann NY Acad Sci 916:370–377

    Article  Google Scholar 

  • Egoscue HJ (1976) Flea exchange between deer mice and some associated small mammals in western Utah. Gt Basin Nat 36:475–480

    Google Scholar 

  • Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL (2006) Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci 103:15380–15385

    Article  CAS  PubMed  Google Scholar 

  • Ellis EC, Ramankutty N (2008) Putting people in the map: anthropogenic biomes of the world. Front Ecol Environ 6:439–447

    Article  Google Scholar 

  • Epstein PR (2001) Climate change and emerging infectious diseases. Microbes Infect 3:747–754

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Gage K, Kosoy M (2005) Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50:505–528

    Article  CAS  PubMed  Google Scholar 

  • Gage KL, Ostfeld RS, Olson JG (1995) Nonviral vector-borne zoonoses associated with mammals in the United States. J Mammal 76:695–715

    Article  Google Scholar 

  • Gettinger D, Ernest KA (1995) Small-mammal community structure and the specificity of ectoparasite associations in central Brazil. Rev Bras Biol 55:331–341

    Google Scholar 

  • Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000) Climate change and vector-borne diseases: a regional analysis. Bull WHO 78:1136–1147

    CAS  PubMed  Google Scholar 

  • Graves GN, Bennett WC, Wheeler JR, Miller BE, Forcum DL (1974) Sylvatic plague studies in southeast New Mexico: I. Flea-Host relationships from six years' study. J Med Entomol 11:488–498

    Google Scholar 

  • Guègan G, Morand S, Poulin R (2005) Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. In: Thomas F, Renaud F, Guègan J-F (eds) Parasitism and ecosytems. Oxford University Press, USA

    Google Scholar 

  • Harvel D, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risk for terrestrial and marine biota. Science 296:2158–2162

    Article  Google Scholar 

  • Hastriter MW, Frafjord K, Whiting MF (2004) A collection of Norwegian fleas (Siphonaptera) north of the Arctic Circle. Proc Entomol Soc Wash 106:877–883

    Google Scholar 

  • Hawlena H, Abramsky Z, Krasnov BR, Saltz D (2007) Host defense versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on it rodent host Meriones crassus. Int J Parasitol 37:919–925

    Article  CAS  PubMed  Google Scholar 

  • Heisch RB, Grainger WE, D’Souza STA Jr (1953) Results of a plague investigation in Kenya. Trans R Soc Trop Med Hyg 47:503–521

    Article  CAS  PubMed  Google Scholar 

  • Holdenried R, Evans FC, Longanecker DS (1951) Host–parasite–disease relationships in a mammalian community in the central coast range of California. Ecolog Monogr 21:2–13

    Google Scholar 

  • Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498

    Article  CAS  PubMed  Google Scholar 

  • Koontz FW, Daszak P (2005) Sprawl and Disease. In: Johnson EA, Klemens MW (eds) Nature in fragments: the legacy of sprawl. Columbia University Press, New York, pp 144–156

    Google Scholar 

  • Kotti VK, Kovalevskiy YV (1996) Flea of small mammals in the AmurBureya Interfluve. Entomol Rev 75:121–127

    Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004a) Flea species richness and parameters of host body, host geography and host ‘milieu’. J Anim Ecol 73:1121–1128

    Article  Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS, Degen A (2004b) Relationship between host diversity and parasite diversity: flea assemblages on small mammals. J Biogeogr 31:1857–1866

    Article  Google Scholar 

  • Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2004c) Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. Am Nat 164:506–516

    Article  PubMed  Google Scholar 

  • Krasnov BR, Stanko M, Miklisova D, Morand S (2006a) Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecol Res 21:460–469

    Article  Google Scholar 

  • Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R (2006b) Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 149:474–481

    Article  PubMed  Google Scholar 

  • Krasnov BR, Stanko M, Miklisova D, Morand S (2006c) Host specificity, parasite community size and the relation between abundance and its variance. Evol Ecol 20:75–91

    Article  Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS, Poulin R (2007) Geographical variation in the “bottom-up” control of diversity: fleas and their small mammalian hosts. Glob Ecol Biogeogr 16:179–186

    Article  Google Scholar 

  • Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900

    Google Scholar 

  • Liat LB, Sustriayu N, Hadi TR, Bang YH (1980) A study of small mammals in the Ciloto Field station area, West Java, Indonesia, with special reference to vectors of plague and scrub typhus. Southeast Asian J Trop Med Public Health 11:71–80

    CAS  PubMed  Google Scholar 

  • Lindsay LR, Galloway TD (1997) Seasonal activity and temporal separation of four species of fleas (Insecta: Siphonaptera) infesting Richardson’s ground squirrels, Spermophilus richardsonii (Rodentia: sciuridae), in Manitoba. Can J Zool 75:1310–1322

    Article  Google Scholar 

  • Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models, 4th edn. SAS Institute Inc., Cary, NC, 466

  • LoGuidice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci 100:567–571

    Article  Google Scholar 

  • Lorange EA (2005) Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis 191:1907–1912

    Article  PubMed  Google Scholar 

  • Molyneux DH (2003) Climate change and tropical disease: common themes in changing vector-borne disease scenarios. Trans R Soc Trop Med Hyg 97:129–132

    Article  PubMed  Google Scholar 

  • Morrone JJ, Gutiérrez A (2005) Do fleas (Insecta: Siphonaptera) parallel their mammal host diversification in the Mexican transition zone? J Biogeogr 32:1315–1325

    Article  Google Scholar 

  • Murray KF (1957) An ecological appraisal of host-ectoparasite relationships in a zone of epizootic plague in central California. Am J Trop Med Hyg 6:1068–1086

    CAS  PubMed  Google Scholar 

  • Nava S, Lareschi M, Voglino D (2003) Interrelationship between ectoparasites and wild rodents from northeastern Buenos Aires Province, Argentina. Mem Inst Oswaldo Cruz 98:45–49

    Article  PubMed  Google Scholar 

  • Nieto NC, Dabritz H, Foley P, Drazenovich N, Calder L, Adjemian J, Conrad PA, Foley JE (2007) Ectoparasite diversity and exposure to vector-borne disease agents in wild rodents in central coastal California. J Med Entomol 44:328–335

    Article  CAS  PubMed  Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world. A new map of life on earth. Bioscience 51:933–938

    Article  Google Scholar 

  • Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmental change on emerging parasitic diseases. Intern J Parasitol 30:1395–1405

    Article  CAS  Google Scholar 

  • Perry RD, Fetherston JD (1997) Yersinia pestis—etiological agent of plague. Clin Microbiol Rev 10:35–66

    CAS  PubMed  Google Scholar 

  • Poorbaugh JH, Gier HT (1961) Fleas (Siphonaptera) of small mammals in Kansas. J Kansas Entomol Soc 39:1–10

    Google Scholar 

  • Poulin R (1998) Host specificity; evolutionary ecology of parasites—from individuals to communities. Chapman Hall, London, pp 41–69

    Google Scholar 

  • Poulin R, Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS (2006) Evolution of host specificity in fleas: is it directional and irreversible? Intern J Parasit 36:185–191

    Article  Google Scholar 

  • Shayan A, Rafinejad J (2006) Arthropod parasites of rodents in Khorram Abbad district Lorestan Provincen of Iran. J Public Health 35:70–76

    Google Scholar 

  • Schwan TG (1986) Seasonal abundance of fleas (Siphonaptera) on grassland rodents in Lake Nakuru National Park, Kenya, and potential for plague transmission. Bull Entomol Res 76:633–648

    Article  Google Scholar 

  • Stanko M, Miklisova D, Gouey de Bellocq J, Morand S (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131:289–295

    Article  Google Scholar 

  • Stunstov VV, Huong LT, Suntsova NI, Gratz HG (1997) Plague foci in Viet Nam: zoological and parasitological aspects. Bull WHO 75:117–123

    Google Scholar 

  • Tikhonova GN, Tikhonov IA, Pogomolov PL (2006) Impact of a small city on the structure of small mammal fauna in forests of the northeastern Moscow region. Russ J Ecol 37:278–2893

    Article  Google Scholar 

  • Trpis M (1994) Host specificity and ecology of fleas (Siphonaptera) of small mammals in mountains of north-central Slovakia. Bull Soc Vector Ecol 19:18–22

    Google Scholar 

  • Vazquez DP, Poulin R, Krasnov BR, Shenbrot GI (2005) Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol 74:946–955

    Article  Google Scholar 

  • Walton DW, Hong HK (1976) Fleas of small mammals form the endemic hemorrhagic fever zones of Kyonggi and Kanwon provinces of the republic of Korea. WHO 2766 9:10

    Google Scholar 

  • Watve MG, Sukumar R (1995) Parasite abundance and diversity in mammals: correlates with host ecology. Proc Natl Acad Sci Ecol 92:8945–8949

    Article  CAS  Google Scholar 

  • Wilcox BA, Colwell RR (2005) Emerging and reemerging infectious diseases: biocomplexity as an interdisciplinary paradigm. Ecohealth 2:244–257

    Article  Google Scholar 

  • Wilcox BA, Gubler DJ (2005) Disease ecology and the global emergence of zoonotic pathogens. Environ Health Prev Med 10:263–272

    Article  CAS  Google Scholar 

  • Zhonglai L, Yaozing (1997) Analysis on the yearly dynamics relation between body flea index and population of Citellus dauricus. Acta Entomol Sin 40:166–170

    Google Scholar 

Download references

Acknowledgments

We thank Dave Wagner, Robert Parmenter, Paulette Ford, Boris Krasnov, and two anonymous reviewers for their helpful comments which greatly improved this paper. The Sevilleta Wildlife Refuge and Long-Term Ecological Research Site provided analysis software and support. Many articles used in analysis were provided by the electronic library of the Center for Disease Control (Vector borne and Zoonotic Diseases), Fort Collins, Colorado, USA. This research was funded by the Ecology of Infectious Diseases program of the NSF/NIH (EF-0326757) and the U.S. Forest Service, Rocky Mountain Research Station.

Author information

Authors and Affiliations

  1. School of Forestry, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Megan M. Friggens & Paul Beier

  2. Rocky Mountain Research Station, United States Forest Service, Albuquerque, NM, 87102, USA

    Megan M. Friggens

Authors
  1. Megan M. Friggens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Beier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Megan M. Friggens.

Additional information

Communicated by Roland Brandl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Articles used in comparative analysis of anthropogenic disturbance and fleas. (PDF 69 kb)

442_2010_1747_MOESM2_ESM.pdf

Fig. 4 Scatter plots of mammal captures (sampling effort) and various mammal and flea community characteristics. (PDF 34 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Friggens, M.M., Beier, P. Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164, 809–820 (2010). https://doi.org/10.1007/s00442-010-1747-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1747-5

Keywords

Search

Navigation