Advertisement

EcoHealth

, Volume 11, Issue 4, pp 619–632 | Cite as

Anthropogenic Land Use Change and Infectious Diseases: A Review of the Evidence

  • Nicole L. GottdenkerEmail author
  • Daniel G. Streicker
  • Christina L. Faust
  • C. R. Carroll
Review

Abstract

Humans have altered ecosystems worldwide, and it is important to understand how this land use change impacts infectious disease transmission in humans and animals. We conducted a systematic review 305 scientific articles investigating how specific types of anthropogenic land use change influence infectious disease dynamics. We summarized findings, highlighted common themes, and drew attention to neglected areas of research. There was an increase in publications on this topic over the last 30 years spanning diseases of humans, livestock, and wildlife, including a large number of zoonotic pathogens. Most papers (66.9%) were observational, 30.8% were review or concept papers, and few studies (2.3%) were experimental in nature, with most studies focusing on vector-borne and/or multi-host pathogens. Common land use change types related to disease transmission were deforestation/forest fragmentation/habitat fragmentation, agricultural development/irrigation, and urbanization/suburbanization. In response to anthropogenic change, more than half of the studies (56.9%) documented increased pathogen transmission, 10.4% of studies observed decreased pathogen transmission, 30.4% had variable and complex pathogen responses, and 2.4% showed no detectable changes. Commonly reported mechanisms by which land use change altered infectious disease transmission included alteration of the vector, host, and pathogen niche, changes in host and vector community composition, changes in behavior or movement of vectors and/or hosts, altered spatial distribution of hosts and/or vectors, and socioeconomic factors, and environmental contamination. We discussed observed patterns in the literature and make suggestions for future research directions, emphasizing the importance of ecological and evolutionary theory to understand pathogen responses in changing landscapes.

Keywords

anthropogenic land use change infectious diseases literature assessment 

Notes

Acknowledgments

We thank Corrie Brown, Sonia Altizer, Uriel Kitron, David Peterson, and Rick Tarleton for helpful comments on this manuscript. NLG was funded by an EPA STAR Science to Achieve Results Fellowship FP-91669001, Sigma Xi Scientific Research Grant G200803150739, and a UGA Graduate School Dissertation Completion Award. DGS was supported by an NSF Graduate Research Fellowship a UGA Graduate School Dissertation Completion Award and NSF Grant DEB-1020966. Funding sources have not officially endorsed this publication and the views expressed herein may not reflect their views.

Supplementary material

10393_2014_941_MOESM1_ESM.docx (234 kb)
Supplementary material 1 (DOCX 233 kb)

References

  1. Allan B. F., H. P. Dutra, L. S. Goessling, K. Barnett, J. M. Chase, R. J. Marquis, G. Pang, G. A. Storch, R. E. Thach, J. L. Orrock (2010). Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proceedings of the National Academy of Sciences of the United States of America 107(43):18523-18527.CrossRefPubMedCentralPubMedGoogle Scholar
  2. Amo, L., P. Lopez and J. Martin (2007). “Habitat deterioration affects body condition of lizards: A behavioral approach with Iberolacerta cyreni lizards inhabiting ski resorts.” Biological Conservation 135(1): 77-85.CrossRefGoogle Scholar
  3. Baeza A, Bouma MJ, Dhiman R, Pascual M (2014) Malaria control under unstable dynamics: reactive vs. climate-based strategies. Acta Tropica 129:42–51Google Scholar
  4. Beldomenico, P. M. and M. Begon (2010). “Disease spread, susceptibility and infection intensity: vicious circles?” Trends Ecol Evol 25(1): 21-27.CrossRefGoogle Scholar
  5. Beyer, H. L., K. Hampson, T. Lembo, S. Cleaveland, M. Kaare and D. T. Haydon (2011). “Metapopulation dynamics of rabies and the efficacy of vaccination.” Proc Biol Sci 278(1715): 2182-2190.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Boots, M. and R. G. Bowers (2004). “The evolution of resistance through costly acquired immunity.” Proc Biol Sci 271(1540): 715-723.CrossRefPubMedCentralPubMedGoogle Scholar
  7. Budischak, S. A., A. E. Jolles and V. O. Ezenwa (2012). “Direct and indirect costs of co-infection in the wild: Linking gastrointestinal parasite communities, host hematology, and immune function.” Int J Parasitol Parasites Wildl 1: 2-12.PubMedCentralPubMedGoogle Scholar
  8. Burney, D. A. and T. F. Flannery (2005). “Fifty millennia of catastrophic extinctions after human contact.” Trends Ecol Evol 20(7): 395-401.CrossRefGoogle Scholar
  9. Ceballos, L. A., M. V. Cardinal, G. M. Vazquez-Prokopec, M. A. Lauricella, M. M. Orozco, R. Cortinas, A. G. Schijman, M. J. Levin, U. Kitron and R. E. Gurtler (2006). “Long-term reduction of Trypanosoma cruzi infection in sylvatic mammals following deforestation and sustained vector surveillance in northwestern Argentina.” Acta Trop 98(3): 286-296.CrossRefPubMedCentralPubMedGoogle Scholar
  10. Chaves, L. F., J. M. Cohen, M. Pascual, M. L. Wilson (2008) Social exclusion modifies climate and deforestation impacts on a vector-borne disease. PLoS Neglected Tropical Diseases 2(2):176.CrossRefPubMedCentralPubMedGoogle Scholar
  11. Colwell, R. K. and T. F. Rangel (2009). “Hutchinson’s duality: the once and future niche.” Proceedings of the National Academy of Sciences of the United States of America 106 Suppl 2: 19651-19658.CrossRefPubMedCentralPubMedGoogle Scholar
  12. de Castro MC, Monte-Mor RL, Sawyer DO, Singer BH (2006) Malaria risk on the Amazon frontier. Proceedings of the National Academy of Sciences of the United States of America 103(7):2452–2457Google Scholar
  13. Dennehy, J. J., N. A. Friedenberg, R. D. Holt and P. E. Turner (2006). “Viral ecology and the maintenance of novel host use.” Am Nat 167(3): 429-439.CrossRefPubMedGoogle Scholar
  14. Despommier, D., B. R. Ellis and B. A. Wilcox (2006). “The role of ecotones in emerging infectious diseases.” EcoHealth 3(4): 281-289.CrossRefGoogle Scholar
  15. Dobson, A. (2004). “Population dynamics of pathogens with multiple host species.” Am Nat 164 Suppl 5: S64-78.CrossRefPubMedGoogle Scholar
  16. Dobson, A., I. Cattadori, R. D. Holt, R. S. Ostfeld, F. Keesing, K. Krichbaum, J. R. Rohr, S. E. Perkins, P. J. Hudson (2006) Sacred cows and sympathetic squirrels: the importance of biological diversity to human health. PLoS Med 3(6):e231.CrossRefPubMedCentralPubMedGoogle Scholar
  17. Eliseev, L. N., M. V. Strelkova, I. I. Zherikhina (1991) The characteristics of the epidemic activation of a natural focus of zoonotic cutaneous leishmaniasis in places with a sympatric dissemination of Leishmania major, L. turanica and L. gerbilli. Meditsinskaia parazitologiia i parazitarnye bolezni 3:24-29.PubMedGoogle Scholar
  18. Ellis, E. C. and N. Ramankutty (2008). “Putting people in the map: anthropogenic biomes of the world.” Frontiers in Ecology and the Environment 6(8): 439-447.CrossRefGoogle Scholar
  19. Ezenwa, V. O. and A. E. Jolles (2011). “From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites.” Integr Comp Biol 51(4): 540-551.CrossRefPubMedGoogle Scholar
  20. Ezenwa, V. O., R. S. Etienne, G. Luikart, A. Beja-Pereira and A. Jolles (2010). “Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo.” Am Nat 176(5): 613-624.CrossRefPubMedGoogle Scholar
  21. Ezenwa, V. O., N. M. Gerardo, D. W. Inouye, M. Medina and J. B. Xavier (2012). “Microbiology. Animal behavior and the microbiome.” Science 338(6104): 198-199.CrossRefPubMedGoogle Scholar
  22. Fenton, A. and A. B. Pedersen (2005). “Community epidemiology framework for classifying disease threats.” Emerging Infectious Diseases 11(12): 1815.CrossRefPubMedCentralPubMedGoogle Scholar
  23. Fokidis, H. B., M. Orchinik and P. Deviche (2009). “Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city.” Gen Comp Endocrinol 160(3): 259-270.CrossRefPubMedGoogle Scholar
  24. Foley, J. A., R. Defries, G. P. Asner, C. Barford, G. Bonan, S. R. Carpenter, F. S. Chapin, M. T. Coe, G. C. Daily, H. K. Gibbs, J. H. Helkowski, T. Holloway, E. A. Howard, C. J. Kucharik, C. Monfreda, J. A. Patz, I. C. Prentice, N. Ramankutty and P. K. Snyder (2005). “Global consequences of land use.” Science 309(5734): 570-574.CrossRefPubMedGoogle Scholar
  25. Goldberg, T. L., T. R. Gillespie, I. B. Rwego, E. L. Estoff and C. A. Chapman (2008). “Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda.” Emerg Infect Dis 14(9): 1375-1382.CrossRefPubMedCentralPubMedGoogle Scholar
  26. Goudie, A. (2000). The Human Impact on the Natural Environment, 5th ed. Cambridge, The MIT PressGoogle Scholar
  27. Grieco, J. P., S. Johnson, N. L. Achee, P. Masuoka, K. Pope, E. Rejmankova, E. Vanzie, R. Andre and D. Roberts (2006). “Distribution of Anopheles albimanus, Anopheles vestitipennis, and Anopheles crucians associated with land use in northern Belize.” J Med Entomol 43(3): 614-622.CrossRefPubMedGoogle Scholar
  28. Hines, A. M., V. O. Ezenwa, P. Cross and J. D. Rogerson (2007). “Effects of supplemental feeding on gastrointestinal parasite infection in elk (Cervus elaphus): preliminary observations.” Vet Parasitol 148(3-4): 350-355.CrossRefPubMedGoogle Scholar
  29. Jardine, A., P. Speldewinde, M. D. Lindsay, A. Cook, C. A. Johansen and P. Weinstein (2008). “Is there an association between dryland salinity and Ross River virus disease in southwestern Australia?” Ecohealth 5(1): 58-68.CrossRefPubMedGoogle Scholar
  30. Johnson, P. T., J. M. Chase, K. L. Dosch, R. B. Hartson, J. A. Gross, D. J. Larson, D. R. Sutherland and S. R. Carpenter (2007). “Aquatic eutrophication promotes pathogenic infection in amphibians.” Proceedings of the National Academy of Sciences of the United States of America 104(40): 15781-15786.CrossRefPubMedCentralPubMedGoogle Scholar
  31. Jolles, A. E., V. O. Ezenwa, R. S. Etienne, W. C. Turner and H. Olff (2008). “Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo.” Ecology 89(8): 2239-2250.CrossRefPubMedGoogle Scholar
  32. Jones, K. E., N. G. Patel, M. A. Levy, A. Storeygard, D. Balk, J. L. Gittleman and P. Daszak (2008). “Global trends in emerging infectious diseases.” Nature 451(7181): 990-993.CrossRefPubMedGoogle Scholar
  33. Keesing, F., L. K. Belden, P. Daszak, A. Dobson, C. D. Harvell, R. D. Holt, P. Hudson, A. Jolles, K. E. Jones, C. E. Mitchell, S. S. Myers, T. Bogich and R. S. Ostfeld (2010). “Impacts of biodiversity on the emergence and transmission of infectious diseases.” Nature 468(7324): 647-652.CrossRefPubMedGoogle Scholar
  34. Klinkenberg, E., F. Konradsen, N. Herrel, M. Mukhtar, W. van der Hoek and F. P. Amerasinghe (2004). “Malaria vectors in the changing environment of the southern Punjab, Pakistan.” Trans R Soc Trop Med Hyg 98(7): 442-449.CrossRefPubMedGoogle Scholar
  35. Kowalewski, M. M., J. S. Salzer, J. C. Deutsch, M. Rano, M. S. Kuhlenschmidt and T. R. Gillespie (2011). “Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of human-primate contact.” Am J Primatol 73(1): 75-83.CrossRefPubMedGoogle Scholar
  36. Linard, C., P. Lamarque, P. Heyman, G. Ducoffre, V. Luyasu, K. Tersago, S. O. Vanwambeke and E. F. Lambin (2007). “Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium.” Int J Health Geogr 6: 15-15.CrossRefPubMedCentralPubMedGoogle Scholar
  37. Matson, P. A., W. J. Parton, A. G. Power and M. J. Swift (1997). “Agricultural intensification and ecosystem properties.” Science 277(5325): 504-509.CrossRefPubMedGoogle Scholar
  38. Mayo, C. E., I. A. Gardner, B. A. Mullens, C. M. Barker, A. C. Gerry, A. J. Guthrie and N. J. MacLachlan (2012). “Anthropogenic and meteorological factors influence vector abundance and prevalence of bluetongue virus infection of dairy cattle in California.” Vet Microbiol 155(2-4): 158-164.CrossRefPubMedGoogle Scholar
  39. McCallum, H. and A. Dobson (2002). “Disease, habitat fragmentation and conservation.” Proc Biol Sci 269(1504): 2041-2049.CrossRefPubMedCentralPubMedGoogle Scholar
  40. Miller, M. A., W. A. Miller, P. A. Conrad, E. R. James, A. C. Melli, C. M. Leutenegger, H. A. Dabritz, A. E. Packham, D. Paradies, M. Harris, J. Ames, D. A. Jessup, K. Worcester and M. E. Grigg (2008). “Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters.” Int J Parasitol 38(11): 1319-1328.CrossRefPubMedGoogle Scholar
  41. Mutero, C. M., C. Kabutha, V. Kimani, L. Kabuage, G. Gitau, J. Ssennyonga, J. Githure, L. Muthami, A. Kaida, L. Musyoka, E. Kiarie and M. Oganda (2004). “A transdisciplinary perspective on the links between malaria and agroecosystems in Kenya.” Acta Trop 89(2): 171-186.CrossRefPubMedGoogle Scholar
  42. Ostfeld, R. S. (2013). “A Candide response to Panglossian accusations by Randolph and Dobson: biodiversity buffers disease.” Parasitology 140(10): 1196-1198.CrossRefPubMedGoogle Scholar
  43. Patz, J. A., T. K. Graczyk, N. Geller and A. Y. Vittor (2000). “Effects of environmental change on emerging parasitic diseases.” Int J Parasitol 30(12-13): 1395-1405.CrossRefPubMedGoogle Scholar
  44. Plowright, R., S. Sokolow, M. Gorman, P. Daszek, J. Foley (2008) Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6: 420–429.CrossRefGoogle Scholar
  45. Plowright, R. K., P. Foley, H. E. Field, A. P. Dobson, J. E. Foley, P. Eby and P. Daszak (2011). “Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.).” Proc Biol Sci 278(1725): 3703-3712.CrossRefPubMedCentralPubMedGoogle Scholar
  46. Pongsiri, M. J., J. Roman, V. O. Ezenwa, T. L. Goldberg, H. S. Koren, S. C. Newbold, R. S. Ostfeld, S. K. Pattanayak and D. J. Salkeld (2009). “Biodiversity loss affects global disease ecology.” Bioscience 59(11): 945-954.CrossRefGoogle Scholar
  47. Pulliam J. R., J. H. Epstein, J. Dushoff, S. A. Rahman, M. Bunning, A. A. Jamaluddin, A. D. Hyatt, H. E. Field, A. P. Dobson, P. Daszak, the Henipavirus Ecology Research (2012) Agricultural intensification, priming for persistence and the emergence of Nipah virus: a lethal bat-borne zoonosis. Journal of the Royal Society Interface 9(66):89–101.CrossRefPubMedCentralGoogle Scholar
  48. Randolph, S. E. and A. D. M. Dobson (2012). “Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm.” Parasitology 139(7): 847-863.CrossRefPubMedGoogle Scholar
  49. Raoult, D. and V. Roux (1997). “Rickettsioses as paradigms of new or emerging infectious diseases.” Clin Microbiol Rev 10(4): 694-719.PubMedCentralPubMedGoogle Scholar
  50. Restif, O., D. T. Hayman, J. R. Pulliam, R. K. Plowright, D. B. George, A. D. Luis, A. A. Cunningham, R. A. Bowen, A. R. Fooks, T. J. O’Shea, J. L. Wood and C. T. Webb (2012). “Model-guided fieldwork: practical guidelines for multidisciplinary research on wildlife ecological and epidemiological dynamics.” Ecol Lett 15(10): 1083-1094.CrossRefPubMedCentralPubMedGoogle Scholar
  51. Salkeld, D. J., K. A. Padgett and J. H. Jones (2013). “A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic.” Ecol Lett 16(5): 679-686.CrossRefPubMedGoogle Scholar
  52. Sorensen, A., F. M. van Beest and R. K. Brook (2014). “Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: A synthesis of knowledge.” Prev Vet Med 113(4): 356-363.CrossRefPubMedGoogle Scholar
  53. Suzan, G., E. Marce, J. T. Giermakowski, B. Armien, J. Pascale, J. Mills, G. Ceballos, A. Gomez, A. A. Aguirre, J. Salazar-Bravo, A. Armien, R. Parmenter and T. Yates (2008). “The effect of habitat fragmentation and species diversity loss on hantavirus prevalence in Panama.” Ann N Y Acad Sci 1149: 80-83.CrossRefPubMedGoogle Scholar
  54. Telfer, S., X. Lambin, R. Birtles, P. Beldomenico, S. Burthe, S. Paterson and M. Begon (2010). “Species interactions in a parasite community drive infection risk in a wildlife population.” Science 330(6001): 243-246.CrossRefPubMedCentralPubMedGoogle Scholar
  55. Tersago, K., A. Schreurs, C. Linard, R. Verhagen, S. Van Dongen and H. Leirs (2008). “Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence.” Vector Borne Zoonotic Dis 8(2): 235-244.CrossRefPubMedGoogle Scholar
  56. Tilman, D. (1999). “Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices.” Proceedings of the National Academy of Sciences of the United States of America 96(11): 5995-6000.CrossRefPubMedCentralPubMedGoogle Scholar
  57. Vaz, V. C., P. S. D’Andrea, A. M. Jansen (2007) Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi. Parasitology 134(12):1785–1793.CrossRefPubMedGoogle Scholar
  58. Vittor, A. Y., R. H. Gilman, J. Tielsch, G. Glass, T. Shields, W. S. Lozano, V. Pinedo-Cancino and J. A. Patz (2006). “The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of Falciparum malaria in the Peruvian Amazon.” Am J Trop Med Hyg 74(1): 3-11.Google Scholar
  59. Woolhouse, M. E., L. H. Taylor and D. T. Haydon (2001). “Population biology of multihost pathogens.” Science 292(5519): 1109-1112.CrossRefPubMedGoogle Scholar
  60. Xia, Y., O. N. Bjornstad and B. T. Grenfell (2004). “Measles metapopulation dynamics: a gravity model for epidemiological coupling and dynamics.” Am Nat 164(2): 267-281.CrossRefPubMedGoogle Scholar
  61. Yasuoka, J. and R. Levins (2007). “Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology.” American Journal of Tropical Medicine and Hygiene 76(3): 450-460.PubMedGoogle Scholar

Copyright information

© International Association for Ecology and Health 2014

Authors and Affiliations

  • Nicole L. Gottdenker
    • 1
    Email author
  • Daniel G. Streicker
    • 2
    • 3
  • Christina L. Faust
    • 4
  • C. R. Carroll
    • 5
  1. 1.Department of Veterinary Pathology, College of Veterinary MedicineThe University of GeorgiaAthensUSA
  2. 2.Institute of Biodiversity, Animal Health and Comparative MedicineUniversity of GlasgowGlasgowUK
  3. 3.2 MRC-University of Glasgow Centre for Virus ResearchGlasgowUK
  4. 4.Princeton UniversityPrincetonUSA
  5. 5.River Basin Center, Odum School of EcologyUniversity of GeorgiaAthensUSA

Personalised recommendations