Theoretical Ecology

, Volume 9, Issue 2, pp 197–205 | Cite as

Heterogeneity in patch quality buffers metapopulations from pathogen impacts

  • Daniel J. Becker
  • Richard J. Hall


Many wildlife species persist on a network of ephemerally occupied habitat patches connected by dispersal. Provisioning of food and other resources for conservation management or recreation is frequently used to improve local habitat quality and attract wildlife. Resource improvement can also facilitate local pathogen transmission, but the landscape-level consequences of provisioning for pathogen spread and habitat occupancy are poorly understood. Here, we develop a simple metapopulation model to investigate how heterogeneity in patch quality resulting from resource improvement influences long-term metapopulation occupancy in the presence of a virulent pathogen. We derive expressions for equilibrium host–pathogen outcomes in terms of provisioning effects on individual patches (through decreased patch extinction rates) and at the landscape level (the fraction of high-quality, provisioned patches), and highlight two cases of practical concern. First, if occupancy in the unprovisioned metapopulation is sufficiently low, a local maximum in occupancy occurs for mixtures of high- and low-quality patches, such that further increasing the number of high-quality patches both lowers occupancy and allows pathogen invasion. Second, if the pathogen persists in the unprovisioned metapopulation, further provisioning can result in all patches becoming infected and in a global minimum in occupancy. This work highlights the need for more empirical research on landscape-level impacts of local resource provisioning on pathogen dynamics.


Conservation biology Infectious disease Habitat management Metapopulation Resource provisioning Supplemental feeding Mathematical modeling Source–sink dynamics 



We thank Sonia Altizer, Alexandra Bentz, members of the Altizer and Ezenwa labs at the University of Georgia, and two anonymous reviewers for helpful comments on earlier versions of the manuscript. DJB was supported by a National Science Foundation Graduate Research Fellowship and ARCS Foundation Award, and RJH was supported by the James S. McDonnell Foundation grant 220020193 and the National Science Foundation grant DEB-1518611.

Supplementary material

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(DOC 1.82 mb)


  1. Altizer S, Hochachka WM, Dhondt AA (2004) Seasonal dynamics of mycoplasmal conjunctivitis in eastern North American house finches. J Anim Ecol 73:309–322CrossRefGoogle Scholar
  2. Angerbjörn A, Eide NE, Dalén L et al (2013) Carnivore conservation in practice: replicated management actions on a large spatial scale. J Appl Ecol 50:59–67. doi: 10.1111/1365-2664.12033 CrossRefGoogle Scholar
  3. Barbraud C, Nichols JD, Hines JE, Hafner H (2003) Estimating rates of local extinction and colonization in colonial species and an extension to the metapopulation and community levels. Oikos 101:113–126. doi: 10.1034/j.1600-0706.2003.12055.x CrossRefGoogle Scholar
  4. Becker DJ, Hall RJ (2014) Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife. Biol Lett 10:20140309. doi: 10.1098/rsbl.2014.0309 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Becker DJ, Streicker DG, Altizer S (2015) Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecol Lett 18:483–495. doi: 10.1111/ele.12428 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Clout MN, Elliott GP, Robertson BC (2002) Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous parrot. Biol Conserv 107:13–18. doi: 10.1016/S0006-3207(01)00267-1 CrossRefGoogle Scholar
  7. Corlatti L, Hackländer K, Frey-Roos F (2009) Ability of wildlife overpasses to provide connectivity and prevent genetic isolation. Conserv Biol 23:548–556. doi: 10.1111/j.1523-1739.2008.01162.x CrossRefPubMedGoogle Scholar
  8. Cortés-Avizanda A, Carrete M, Serrano D, Donázar JA (2009) Carcasses increase the probability of predation of ground-nesting birds: a caveat regarding the conservation value of vulture restaurants. Anim Conserv 12:85–88. doi: 10.1111/j.1469-1795.2008.00231.x CrossRefGoogle Scholar
  9. Dias PC (1996) Sources and sinks in population biology. Trends Ecol Evol 11:326–330CrossRefPubMedGoogle Scholar
  10. Doak DF, Mills LS (1994) A useful role for theory in conservation. Ecology 75:615–626. doi: 10.2307/1941720 CrossRefGoogle Scholar
  11. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 487–515Google Scholar
  12. Galbraith JA, Beggs JR, Jones DN, Stanley MC (2015) Supplementary feeding restructures urban bird communities. Proc Natl Acad Sci 201501489. doi:  10.1073/pnas.1501489112
  13. Gog J, Woodroffe R, Swinton J (2002) Disease in endangered metapopulations: the importance of alternative hosts. Proc R Soc Lond B Biol Sci 269:671–676. doi: 10.1098/rspb.2001.1667 CrossRefGoogle Scholar
  14. Gompper ME, Wright AN (2005) Altered prevalence of raccoon roundworm (Baylisascaris procyonis) owing to manipulated contact rates of hosts. J Zool 266:215–219. doi: 10.1017/S0952836905006813 CrossRefGoogle Scholar
  15. Gonzalez LM, Margalida A, Sánchez R, Oria J (2006) Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biol Conserv 129:477–486CrossRefGoogle Scholar
  16. Hallam TG, McCracken GF (2011) Management of the panzootic white-nose syndrome through culling of bats. Conserv Biol 25:189–194CrossRefPubMedGoogle Scholar
  17. Hanski I (1991) Single-species metapopulation dynamics: concepts, models and observations. Biol J Linn Soc 42:17–38CrossRefGoogle Scholar
  18. Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162. doi: 10.2307/5591 CrossRefGoogle Scholar
  19. Hanski I, Gilpin M (1991) Metapopulation dynamics: brief history and conceptual domain. Biol J Linn Soc 42:3–16CrossRefGoogle Scholar
  20. Hanski I, Ovaskainen O (2000) The metapopulation capacity of a fragmented landscape. Nature 404:755–758. doi: 10.1038/35008063 CrossRefPubMedGoogle Scholar
  21. Haydon DT, Laurenson MK, Sillero-Zubiri C (2002) Integrating epidemiology into population viability analysis: managing the risk posed by rabies and canine distemper to the Ethiopian wolf. Conserv Biol 16:1372–1385. doi: 10.1046/j.1523-1739.2002.00559.x CrossRefGoogle Scholar
  22. Hess G (1996) Disease in metapopulation models: implications for conservation. Ecology 77:1617–1632. doi: 10.2307/2265556 CrossRefGoogle Scholar
  23. Hochachka WM, Dhondt AA (2000) Density-dependent decline of host abundance resulting from a new infectious disease. Proc Natl Acad Sci 97:5303–5306CrossRefPubMedPubMedCentralGoogle Scholar
  24. Holt RD (1985) Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor Popul Biol 28:181–208CrossRefGoogle Scholar
  25. Jones JD, Kauffman MJ, Monteith KL et al (2014) Supplemental feeding alters migration of a temperate ungulate. Ecol Appl 24:1769–1779CrossRefGoogle Scholar
  26. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498. doi: 10.1111/j.1461-0248.2006.00885.x CrossRefPubMedGoogle Scholar
  27. Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull ESA 15:237–240Google Scholar
  28. LoGiudice 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. doi: 10.1073/pnas.0233733100 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49. doi: 10.1111/j.1523-1739.2001.00129.x CrossRefGoogle Scholar
  30. McCallum H, Dobson A (2002) Disease, habitat fragmentation and conservation. Proc R Soc Lond B Biol Sci 269:2041–2049. doi: 10.1098/rspb.2002.2079 CrossRefGoogle Scholar
  31. Moilanen A (2002) Implications of empirical data quality to metapopulation model parameter estimation and application. Oikos 96:516–530. doi: 10.1034/j.1600-0706.2002.960313.x CrossRefGoogle Scholar
  32. Moilanen A, Hanski I (1998) Metapopulation dynamics: effects of habitat quality and landscape structure. Ecology 79:2503–2515CrossRefGoogle Scholar
  33. Mortelliti A, Amori G, Boitani L (2010) The role of habitat quality in fragmented landscapes: a conceptual overview and prospectus for future research. Oecologia 163:535–547. doi: 10.1007/s00442-010-1623-3 CrossRefPubMedGoogle Scholar
  34. Opdam P (1991) Metapopulation theory and habitat fragmentation: a review of holarctic breeding bird studies. Landsc Ecol 5:93–106CrossRefGoogle Scholar
  35. Ovaskainen O, Hanski I (2001) Spatially structured metapopulation models: global and local assessment of metapopulation capacity. Theor Popul Biol 60:281–302. doi: 10.1006/tpbi.2001.1548 CrossRefPubMedGoogle Scholar
  36. Park AW (2012) Infectious disease in animal metapopulations: the importance of environmental transmission. Ecol Evol 2:1398–1407CrossRefPubMedPubMedCentralGoogle Scholar
  37. Plowright RK, Foley P, Field HE et al (2011) Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc R Soc B Biol Sci 278:3703–3712. doi: 10.1098/rspb.2011.0522 CrossRefGoogle Scholar
  38. Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 652–661Google Scholar
  39. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  40. Robb GN, McDonald RA, Chamberlain DE et al (2008) Winter feeding of birds increases productivity in the subsequent breeding season. Biol Lett 4:220–223. doi: 10.1098/rsbl.2007.0622 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Robinson RA, Lawson B, Toms MP et al (2010) Emerging infectious disease leads to rapid population declines of common British birds. PLoS One 5:e12215. doi: 10.1371/journal.pone.0012215 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Satterfield DA, Maerz JC, Altizer S (2015) Loss of migratory behaviour increases infection risk for a butterfly host. Proc R Soc B Biol Sci 282:20141734. doi: 10.1098/rspb.2014.1734 CrossRefGoogle Scholar
  43. Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480. doi: 10.1016/S0169-5347(02)02580-6 CrossRefGoogle Scholar
  44. Soetaert KER, Petzoldt T, Setzer RW (2010) Solving differential equations in R: package deSolveGoogle Scholar
  45. Thomas CD (2000) Dispersal and extinction in fragmented landscapes. Proc R Soc Lond B Biol Sci 267:139–145. doi: 10.1098/rspb.2000.0978 CrossRefGoogle Scholar
  46. Vale PF, Wilson AJ, Best A et al (2011) Epidemiological, evolutionary and co-evolutionary implications of context-dependent parasitism. Am Nat 177:510–521. doi: 10.1086/659002 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wauters LA, Hutchinson Y, Parkin DT, Dhondt AA (1994) The effects of habitat fragmentation on demography and on the loss of genetic variation in the Red squirrel. Proc R Soc Lond B Biol Sci 255:107–111. doi: 10.1098/rspb.1994.0015 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Department of Infectious DiseasesCollege of Veterinary Medicine, University of GeorgiaAthensUSA

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