Advertisement

EcoHealth

pp 1–12 | Cite as

Land-Use Change Alters Host and Vector Communities and May Elevate Disease Risk

  • Fengyi Guo
  • Timothy C. Bonebrake
  • Luke GibsonEmail author
Original Contribution

Abstract

Land-use change has transformed most of the planet. Concurrently, recent outbreaks of various emerging infectious diseases have raised great attention to the health consequences of anthropogenic environmental degradation. Here, we assessed the global impacts of habitat conversion and other land-use changes on community structures of infectious disease hosts and vectors, using a meta-analysis of 37 studies. From 331 pairwise comparisons of disease hosts/vectors in pristine (undisturbed) and disturbed areas, we found a decrease in species diversity but an increase in body size associated with land-use changes, potentially suggesting higher risk of infectious disease transmission in disturbed habitats. Neither host nor vector abundance, however, changed significantly following disturbance. When grouped by subcategories like disturbance type, taxonomic group, pathogen type and region, changes in host/vector community composition varied considerably. Fragmentation and agriculture in particular benefit host and vector communities and therefore might elevate disease risk. Our results indicate that while habitat disturbance could alter disease host/vector communities in ways that exacerbate pathogen prevalence, the relationship is highly context-dependent and influenced by multiple factors.

Keywords

biodiversity deforestation land-use change dilution effect disease habitat loss 

Notes

Acknowledgements

We thank several anonymous reviewers for constructive feedback on the manuscript. Research was supported by the Seed Funding Programme for Basic Research from the University of Hong Kong. We declare no competing interests for this project.

References

  1. Allan B, Keesing F, Ostfeld R (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17:267-272.  https://doi.org/10.1046/j.1523-1739.2003.01260.x CrossRefGoogle Scholar
  2. Ameneshewa, B., & Service, M. W. (1996). The relationship between female body size and survival rate of the malaria vector Anopheles arabiensis in Ethiopia. Medical and Veterinary Entomology 10:170-172. ( https://doi.org/10.1111/j.1365-2915.1996.tb00724.x)CrossRefPubMedGoogle Scholar
  3. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-analysis. Chichester, UK: John Wiley & Sons.CrossRefGoogle Scholar
  4. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, Ortega CN, Sauer LE, Sehgal T, Young S, Rohr JR (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences 112:8667-8671. ( https://doi.org/10.1073/pnas.1506279112)CrossRefGoogle Scholar
  5. Cumming G, Guégan J (2006) Food webs and disease: is pathogen diversity limited by vector diversity? EcoHealth 3:163-170. ( https://doi.org/10.1007/s10393-006-0028-6)CrossRefGoogle Scholar
  6. Davies CE, Johnson AF, Wootton EC, Greenwood SJ, Clark KF, Vogan CL, Rowley AF (2015). Effects of population density and body size on disease ecology of the European lobster in a temperate marine conservation zone. ICES Journal of Marine Science 72:i128-i138. ( https://doi.org/10.1093/icesjms/fsu237.)CrossRefGoogle Scholar
  7. De Luca A, Vasconselos H, Barrett T (2003) Distribution of sandflies (Diptera: Phlebotominae) in forest remnants and adjacent matrix habitats in Brazilian Amazonia. Brazilian Journal of Biology 63:401-410. ( https://doi.org/10.1590/s1519-69842003000300006)CrossRefGoogle Scholar
  8. Dunn R, Davies T, Harris N, Gavin M (2010) Global drivers of human pathogen richness and prevalence. Proceedings of the Royal Society of London B: Biological Sciences 277:2587-2595. ( https://doi.org/10.1098/rspb.2010.0340)CrossRefGoogle Scholar
  9. Efron B, Tibshirani R (1991) Statistical data analysis in the computer age. Science 253:390-395. ( https://doi.org/10.1126/science.253.5018.390)CrossRefPubMedGoogle Scholar
  10. Ellis E (2011) Anthropogenic transformation of the terrestrial biosphere. Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 369:1010-1035. ( https://doi.org/10.1098/rsta.2010.0331)CrossRefGoogle Scholar
  11. Ezenwa V, Godsey M, King R, Guptill S (2006) Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proceedings of the Royal Society of London B: Biological Sciences 273:109-117. ( https://doi.org/10.1098/rspb.2005.3284)CrossRefGoogle Scholar
  12. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570-574. ( https://doi.org/10.1126/science.1111772)CrossRefPubMedGoogle Scholar
  13. Froeschke, G., van der Mescht, L., McGeoch, M., & Matthee, S. (2013). Life history strategy influences parasite responses to habitat fragmentation. International Journal for Parasitology 43:1109-1118. ( https://doi.org/10.1016/j.ijpara.2013.07.003)CrossRefPubMedGoogle Scholar
  14. Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJ, Laurance WF, Lovejoy TE, Sodhi NS (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478:378-381. ( https://doi.org/10.1038/nature10425)CrossRefPubMedGoogle Scholar
  15. Gibson L, Lynam AJ, Bradshaw CJ, He F, Bickford DP, Woodruff DS, Bumrungsri S, Laurance WF (2013) Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341:1508-1510. ( https://doi.org/10.1126/science.1240495)CrossRefPubMedGoogle Scholar
  16. Gottdenker N, Streicker D, Faust C, Carroll C (2014) Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth 11:619-632. ( https://doi.org/10.1007/s10393-014-0941-z)CrossRefPubMedGoogle Scholar
  17. Greer, A. L., Briggs, C. J., & Collins, J. P. (2008). Testing a key assumption of host‐pathogen theory: density and disease transmission. Oikos 117: 1667-1673. ( https://doi.org/10.1111/j.1600-0706.2008.16783.x)CrossRefGoogle Scholar
  18. Gubler, D. J. (2011). Dengue, urbanization and globalization: the unholy trinity of the 21st century. Tropical Medicine and Health 39(4 Suppl): 3-11. ( https://doi.org/10.2149/tmh.2011-s05)CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hall SR, Sivars-Becker L, Becker C, Duffy MA, Tessier AJ, Cáceres CE (2007) Eating yourself sick: transmission of disease as a function of foraging ecology. Ecology Letters 10:207-218. ( https://doi.org/10.1111/j.1461-0248.2007.01011.x)CrossRefPubMedGoogle Scholar
  20. Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova S, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850-853. ( https://doi.org/10.1126/science.1244693)CrossRefPubMedGoogle Scholar
  21. Huang ZY, de Boer WF, van Langevelde F, Olson V, Blackburn TM, Prins HH (2013) Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. PLoS One 8:e54341 ( https://doi.org/10.1371/journal.pone.0054341)CrossRefPubMedPubMedCentralGoogle Scholar
  22. Johnson PT, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213:961-970. ( https://doi.org/10.1242/jeb.037721)CrossRefPubMedGoogle Scholar
  23. Johnson PT, Preston DL, Hoverman JT, Richgels K (2013a) Biodiversity decreases disease through predicTable changes in host community competence. Nature 494:230-233. ( https://doi.org/10.1038/nature11883)CrossRefPubMedGoogle Scholar
  24. Johnson PT, Preston DL, Hoverman JT, LaFonte BE (2013b) Host and parasite diversity jointly control disease risk in complex communities. Proceedings of the National Academy of Sciences 110:16916-16921. ( https://doi.org/10.1073/pnas.1310557110)CrossRefGoogle Scholar
  25. Johnson PT, Ostfeld RS, Keesing F (2015) Frontiers in research on biodiversity and disease. Ecology Letters 18:1119-1133. ( https://doi.org/10.1111/ele.12479)CrossRefPubMedPubMedCentralGoogle Scholar
  26. Keesing F, Holt R and Ostfeld RS (2006) Effects of species diversity on disease risk. Ecology Letters 9:485-488. ( https://doi.org/10.1111/j.1461-0248.2006.00885.x)CrossRefPubMedGoogle Scholar
  27. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652. ( https://doi.org/10.1038/nature09575)CrossRefPubMedGoogle Scholar
  28. Kilpatrick A (2011) Globalization, land use, and the invasion of West Nile virus. Science 334: 323-327. ( https://doi.org/10.1126/science.1201010)CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lacroix C, Jolles A, Seabloom EW, Power AG, Mitchell CE, Borer ET (2014) Non-random biodiversity loss underlies predictable increases in viral disease prevalence. Journal of the Royal Society Interface 11:20130947. ( https://doi.org/10.1098/rsif.2013.0947)CrossRefPubMedCentralGoogle Scholar
  30. Linard C, Lamarque P, Heyman P, Ducoffre G, Luyasu V, Tersago K, Vanwambeke S, Lambin E (2007) Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6:15. ( https://doi.org/10.1186/1476-072x-6-15)CrossRefPubMedPubMedCentralGoogle Scholar
  31. Liu X, Lyu S, Zhou S, Bradshaw CJ (2016) Warming and fertilization alter the dilution effect of host diversity on disease severity. Ecology 97:1680-1689. ( https://doi.org/10.1890/15-1784.1)CrossRefPubMedGoogle Scholar
  32. Liu X, Lyu S, Sun D, Bradshaw CJ, Zhou S (2017) Species decline under nitrogen fertilization increases community-level competence of fungal diseases. Proceedings of the Royal Society of London B: Biological Sciences 284:20162621 ( https://doi.org/10.1098/rspb.2016.2621)CrossRefGoogle Scholar
  33. LoGiudice K, Ostfeld RS, Schmidt K, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences 100:567-571. ( https://doi.org/10.1073/pnas.0233733100)CrossRefGoogle Scholar
  34. Maher, J. M., Markey, J. C., & Ebert-May, D. (2013). The other half of the story: effect size analysis in quantitative research. CBE-Life Sciences Education 12: 345-351. ( https://doi.org/10.1187/cbe.13-04-0082)CrossRefPubMedPubMedCentralGoogle Scholar
  35. Malcolm JR (1997) Biomass and diversity of small mammals in forest fragments. In: Laurance WF, Bierregaard Jr RO (eds.), Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities. University of Chicago Press, Chicago, III. USA, pp. 207-221.Google Scholar
  36. McKinney M (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation 127:247-260. ( https://doi.org/10.1016/j.biocon.2005.09.005)CrossRefGoogle Scholar
  37. Meyer Steiger D, Ritchie S, Laurance S (2016) Mosquito communities and disease risk influenced by land use change and seasonality in the Australian tropics. Parasites Vectors 9:(387). ( https://doi.org/10.1186/s13071-016-1675-2)CrossRefPubMedPubMedCentralGoogle Scholar
  38. Murray K, Daszak P (2013) Human ecology in pathogenic landscapes: two hypotheses on how land use change drives viral emergence. Current Opinion in Virology 3:79-83. ( https://doi.org/10.1016/j.coviro.2013.01.006)CrossRefPubMedPubMedCentralGoogle Scholar
  39. Newbold T, Hudson LN, Hill SL, Contu S, Lysenko I, Senior RA, Börger L, Bennett DJ, Choimes A, Collen B, Day J et al. (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45-50. ( https://doi.org/10.1038/nature14324)CrossRefPubMedGoogle Scholar
  40. Nunn C, Altizer S (2006) Infectious Diseases in Primates. Oxford: Oxford University Press.CrossRefGoogle Scholar
  41. Nupp T, Swihart R (1996) Effect of forest patch area on population attributes of white-footed mice (Peromyscus leucopus) in fragmented landscapes. Canadian Journal of Zoology 74: 467-472. ( https://doi.org/10.1139/z96-054)CrossRefGoogle Scholar
  42. Ostfeld RS, Keesing F (2000a) Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722-728. ( https://doi.org/10.1046/j.1523-1739.2000.99014.x)CrossRefGoogle Scholar
  43. Ostfeld RS, Keesing F (2000b) Biodiversity series: The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78:2061-2078. ( https://doi.org/10.1139/z00-172)CrossRefGoogle Scholar
  44. Ostfeld RS, Keesing F (2012) Effects of host diversity on infectious disease. Annual Review of Ecology, Evolution, and Systematics 43:157-182. ( https://doi.org/10.1146/annurev-ecolsys-102710-145022)CrossRefGoogle Scholar
  45. Ostfeld, RS (2017). Biodiversity loss and the ecology of infectious disease. The Lancet Planetary Health 1: e2-e3.CrossRefGoogle Scholar
  46. Parker IM, Saunders M, Bontrager M, Weitz AP, Hendricks R, Magarey R, Suiter K, Gilbert GS (2015) Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520:542-544. ( https://doi.org/10.1038/nature14372)CrossRefPubMedGoogle Scholar
  47. Patz JA, Daszak P, Tabor GM, Aguirre AA, Pearl M, Epstein J, Wolfe ND, Kilpatrick AM, Foufopoulos J, Molyneux D, Bradley DJ (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112:1092-1098. ( https://doi.org/10.1289/ehp.6877)CrossRefPubMedPubMedCentralGoogle Scholar
  48. Patz J, Olson S (2006) Malaria risk and temperature: influences from global climate change and local land use practices. Proceedings of the National Academy of Sciences 103:5635-5636. ( https://doi.org/10.1073/pnas.0601493103)CrossRefGoogle Scholar
  49. Patz J, Olson S, Uejio C, Gibbs H (2008) Disease emergence from global climate and land use change. Medical Clinics of North America 92:1473-1491. ( https://doi.org/10.1016/j.mcna.2008.07.007)CrossRefPubMedGoogle Scholar
  50. Pienkowski T, Dickens BL, Sun H, Carrasco LR (2017). Empirical evidence of the public health benefits of tropical forest conservation in Cambodia: a generalised linear mixed-effects model analysis. The Lancet Planetary Health, 1:e180-e187.CrossRefGoogle Scholar
  51. Poulin R, Morand S (2004) Parasite Biodiversity. Washington [D.C.]: Smithsonian Books.Google Scholar
  52. Power A, Flecker A (2008) The role of vector diversity in disease dynamics. In: Ostfeld R S, Keesing F and Eviner V (eds.), Infectious Disease Ecology: The Effects of Ecosystems on Disease and of Disease on Ecosystems. Princeton, N.J.: Princeton University Press.Google Scholar
  53. Randolph S, Dobson A (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139:847-863. ( https://doi.org/10.1017/s0031182012000200)CrossRefPubMedGoogle Scholar
  54. Rubio A, Ávila-Flores R, Suzán G (2014) Responses of small mammals to habitat fragmentation: epidemiological considerations for rodent-borne hantaviruses in the Americas. EcoHealth 11:526-533. ( https://doi.org/10.1007/s10393-014-0944-9)CrossRefPubMedGoogle Scholar
  55. Rottstock T, Joshi J, Kummer V, Fischer M (2014) Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:907-1917. ( https://doi.org/10.1890/13-2317.1)CrossRefGoogle Scholar
  56. Ryder J, Miller M, White A, Knell R, Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017-2026. ( https://doi.org/10.1111/j.2007.0030-1299.15863.x)CrossRefGoogle Scholar
  57. Swaddle J, Calos S (2008) Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3:e2488. ( https://doi.org/10.1371/journal.pone.0002488)CrossRefPubMedPubMedCentralGoogle Scholar
  58. Thongsripong P, Green A, Kittayapong P, Kapan D, Wilcox B, Bennett S (2013) Mosquito vector diversity across habitats in central Thailand endemic for dengue and other arthropod-borne diseases. PLoS Neglected Tropical Diseases 7:e2507. ( https://doi.org/10.1371/journal.pntd.0002507)CrossRefPubMedPubMedCentralGoogle Scholar
  59. Van der Mescht L, Le Roux PC, Matthee S (2013) Remnant fragments within an agricultural matrix enhance conditions for a rodent host and its fleas. Parasitology 140:368-377. ( https://doi.org/10.1017/s0031182012001692 CrossRefGoogle Scholar
  60. Wood CL, Lafferty KD (2013) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology & Evolution 28:239-247. ( https://doi.org/10.1016/j.tree.2012.10.011)CrossRefGoogle Scholar
  61. Wood CL, Lafferty KD, DeLeo G, Young H, Hudson P, Kuris A (2014) Does biodiversity protect humans against infectious disease? Ecology 95:817-832. ( https://doi.org/10.1890/13-1041.1)CrossRefPubMedGoogle Scholar
  62. Wood CL, McInturff A, Young HS, Kim D, Lafferty KD (2017). Human infectious disease burdens decrease with urbanization but not with biodiversity. Philosophical Transactions of the Royal Society B: Biological Sciences 372:20160122. ( https://doi.org/10.1098/rstb.2016.0122)CrossRefGoogle Scholar
  63. Yasuoka J, Levins R (2007) Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. The American Journal of Tropical Medicine and Hygiene 76:450-460.PubMedGoogle Scholar
  64. Young H, Griffin R, Wood C, Nunn C (2013) Does habitat disturbance increase infectious disease risk for primates? Ecology Letters 16:656-663. ( https://doi.org/10.1111/ele.12094)CrossRefPubMedGoogle Scholar
  65. Zargar U, Chishti M, Ahmad F, Rather M (2015) Does alteration in biodiversity really affect disease outcome? – A debate is brewing. Saudi Journal of Biological Sciences 22:14-18. ( https://doi.org/10.1016/j.sjbs.2014.05.004)CrossRefPubMedGoogle Scholar

Copyright information

© EcoHealth Alliance 2018

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of Hong KongHong KongChina
  2. 2.School of Environmental Science and EngineeringSouthern University of Science and TechnologyShenzhenChina

Personalised recommendations