Effects of prey metapopulation structure on the viability of black-footed ferrets in plague-impacted landscapes: A metamodelling approach

Journal of Applied Ecology

Volumn 51, Issue 3, 2014, Pages 735-745

  Shoemaker, Kevin T ^a   Lacy, Robert C ^b   Verant, Michelle L ^c   Brook, Barry W ^d   Livieri, Travis M ^e   Miller, Philip S ^f   Fordham, Damien A ^d   Resit Akcakaya H ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b BROOKFIELD ZOO   (United States)

^c NATIONAL WILDLIFE HEALTH CENTER   (United States)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e Prairie Wildlife Research Colorado   (United States)

^f IUCN/SSC Conservation Breeding Specialist Group   (United States)

Author keywords

Connectivity; Disease spread; Oscillatory population dynamics; Predator prey interactions; Sensitivity analysis; Spatial structure

Indexed keywords

ASSESSMENT METHOD; CANID; DISEASE SPREAD; ECOLOGICAL MODELING; EPIDEMIOLOGY; EXTINCTION RISK; LANDSCAPE; MANAGEMENT PRACTICE; METAPOPULATION; MUSTELID; POPULATION STRUCTURE; PREDATOR-PREY INTERACTION; PREY AVAILABILITY; SPATIAL ANALYSIS;

CONATA BASIN; SOUTH DAKOTA; UNITED STATES;

CYNOMYS; MUSTELA; MUSTELA NIGRIPES; YERSINIA PESTIS;

EID: 84900561197     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/1365-2664.12223     Document Type: Article

References (66)

1. Abbott, R.C. & Rocke, T.E. (2012) Plague: U.S. Geological Survey Circular 1372, 79 p., plus appendix. (Also available at http://pubs.usgs.gov/circ/1372.)
2. Akçakaya, H.R. & Root, W. (2013) RAMAS Metapop: Viability Analysis for Stage-Structured Metapopulations (Version 6.0). Applied Biomathematics, Setauket, New York.
3. Barnes, A.M. (1982) Surveillance and control of plague in the United States. Animal Disease in Relation to Animal Conservation. Symposia of the Zoological Society of London 50 (eds M.A. Edwards & U. McDonnell ), pp. 237-270. Academic Press, New York.
4. Biggins, D.E., Livieri, T.M. & Breck, S.W. (2011b) Interface between black-footed ferret research and operational conservation. Journal of Mammalogy, 92, 699-704.
5. Biggins, D.E., Lockhart, J.M. & Godbey, J.L. (2006) Evaluating habitat for black-footed ferrets: revision of an existing model. Recovery of the Black-Footed Ferret - Progress and Continuing Challenges (eds J.E. Roelle, B.J. Miller, J.L. Godbey & D.E. Biggins ), pp. 143-150. U.S. Geological Survey, Scientific Investigations Report 2005-5293, Reston, VA
6. Biggins, D.E., Vargas, A., Godbey, J.L. & Anderson, S.H. (1999) Influence of prerelease experience on reintroduced black-footed ferrets (Mustela nigripes). Biological Conservation, 89, 121-129.
7. Biggins, D.E., Godbey, J.L., Matchett, M.R. & Livieri, T.M. (2006a) Habitat preferences and intraspecific competition in black-footed ferrets. Recovery of the Black-Footed Ferret - Progress and Continuing Challenges (eds J.E. Roelle, B.J. Miller, J.L. Godbey & D.E. Biggins ), pp. 129-140. U.S. Geological Survey, Scientific Investigations Report 2005-5293, Reston, VA.
8. Biggins, D.E., Sidle, J.G., Seery, D.B. & Ernst, A.E. (2006b) Estimating the abundance of prairie dogs. Conservation of the Black-tailed Prairie Dog: Saving North America's Western Grasslands (ed. J.L. Hoogland ), pp. 94-107. Island Press, Washington, DC.
9. Biggins, D.E., Godbey, J.L., Gage, K.L., Carter, L.G. & Montenieri, J.A. (2010) Vector control improves survival of prairie dogs (Cynomys) in areas considered enzootic for plague. Vector-Borne and Zoonotic Diseases, 10, 17-26.
10. Biggins, D.E., Godbey, J.L., Horton, B.M. & Livieri, T.M. (2011a) Movements and survival of black-footed ferrets associated with an experimental translocation in South Dakota. Journal of Mammalogy, 92, 742-750.
11. Breiman, L. (2001) Random forest. Machine Learning, 45, 5-32.
12. Burgman, M., Ferson, S. & Akçakaya, H.R. (1993) Risk Assessment in Conservation Biology. Chapman and Hall, New York.
13. Chadès, I., Curtis, J.M.R. & Martin, T.G. (2012) Setting realistic recovery targets for two interacting endangered species, sea otter and northern abalone. Conservation Biology, 26, 1016-1025.
14. Clark, T.W. (1989) Conservation Biology of the Black-footed Ferret Mustela nigripes. Wildlife Preservation Trust Special Scientific Report No. 3, Wildlife Preservation Trust International, Philadelphia, PA, USA, 175
15. Conservation Breeding Specialist Group (2004) Black-footed Ferret Population Management Planning Workshop. Final Report. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley, MN. 130pp.
16. Cooper, J. & Gabriel, L. (2005) South Dakota Black-Tailed Prairie Dog Conservation and Management Plan. South Dakota Department of Game, Fish and Parks and South Dakota Department of Agriculture, Pierre, South Dakota. 68p.
17. Cully, J.F. & Williams, E.S. (2001) Interspecific comparisons of sylvatic plague in prairie dogs. Journal of Mammalogy, 82, 894-905.
18. Cully, J.F., Johnson, T.L., Collinge, S.K. & Ray, C. (2010) Disease limits populations: plague and black-tailed prairie dogs. Vector Borne Zoonotic Disease, 10, 7-15.
19. Eads, D.A., Millspaugh, J.J., Biggins, D.E., Livieri, T.M. & Jachowski, D.S. (2011) Post-breeding resource selection by adult black-footed ferrets in the Conata Basin, South Dakota. Journal of Mammalogy, 92, 760-770.
20. Fahrig, L. (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487-515.
21. Fordham, D.A., Akçakaya, H.R., Brook, B.W., Rodríguez, A., Alves, P.C., Civantos, E., Triviño, M., Watts, M.J. & Araújo, M.B. (2013) Adapted conservation measures are required to save the Iberian lynx in a changing climate. Nature Climate Change, 3, 899-903.
22. Forrest, S.C., Clark, T.W., Richardson, L. & Campbell III, T.M. (1985) Black-footed ferret habitat: some management and reintroduction considerations. Wyoming Bureau of Land Management, Wildlife Technical Bulletin 2 Wyoming Bureau of Land Mangement, Cheyenne, WY. 49p.
23. Frick, W.F., Pollock, J.F., Hicks, A.C., Langwig, K.E., Reynolds, D.S., Turner, G.G. et al. (2010) An emerging disease causes regional population collapse of a common North American bat species. Science, 329, 679-682.
24. Gage, K.L. & Kosoy, M.Y. (2005) Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology, 50, 505-528.
25. Garrett, M.G. & Franklin, W.L. (1988) Behavioral ecology of dispersal in the black-tailed prairie dog. Journal of Mammalogy, 69, 236-250.
26. Godbey, J.L., Biggins, D.E. & Garelle, D. (2006) Exposure of captive black-footed ferrets to plague and implications for species recovery. Recovery of the Black-Footed Ferret - Progress and Continuing Challenges (eds J.E. Roelle, B.J. Miller, J.L. Godbey & D.E. Biggins ), pp. 233-237. U.S. Geological Survey, Scientific Investigations Report 2005-5293, Reston, VA.
27. Grenier, M.B., McDonald, D.B. & Buskirk, S.W. (2007) Rapid population growth of a critically endangered carnivore. Science, 317, 779.
28. Hanski, I., Moilanen, A. & Gyllenberg, M. (1996) Minimum viable metapopulation size. American Naturalist, 147, 527-541.
29. Haydon, D.T., Laurenson, M.K. & Sillero-Zubiri, C. (2002) Integrating epidemiology into population viability analysis: managing the risk posed by rabies and canine distemper to the Ethiopian wolf. Conservation Biology, 16, 1372-1385.
30. Hoogland, J.L. (1995) The Black-Tailed Prairie Dog: Social Life of A Burrowing Mammal. The University of Chicago Press, Chicago, IL.
31. Hoogland, J.L. (2001) Black-tailed, Gunnison's, and Utah prairie dogs reproduce slowly. Journal of Mammalogy, 82, 917-927.
32. Hothorn, T., Hornik, K. & Zeileis, A. (2006) Unbiased recursive partitioning: a conditional inference framework. Journal of Computational and Graphical Statistics, 15, 651-674.
33. Jachowski, D.S., Millspaugh, J.J., Biggins, D.E., Livieri, T.M. & Matchett, M.R. (2010) Home-range size and spatial organization of black-footed ferrets Mustela nigripes in South Dakota, USA. Wildlife Biology, 16, 1-11.
34. Jachowski, D.S., Gitzen, R.A., Grenier, M.B., Holmes, B. & Millspaugh, J.J. (2011a) The importance of thinking big: large-scale prey conservation drives black-footed ferret reintroduction success. Biological Conservation, 144, 1560-1566.
35. Jachowski, D.S., Millspaugh, J.J., Biggins, D.E., Livieri, T.M., Matchett, M.R. & Rittenhouse, C.D. (2011b) Resource selection by black-footed ferrets in South Dakota and Montana. Natural Areas Journal, 31, 218-225.
36. Knowles, C., Proctor, J. & Forest, S. (2002) Black-tailed prairie dog abundance and distribution in the great plains based on historic and contemporary information. Great Plains Research: A Journal of Natural and Social Sciences Paper 608. http://digitalcommons.unl.edu/greatplainsresearch/608 (accessed 23 May 2012).
37. Kotliar, N.B., Baker, B.W. & Whicker, A.D. (1999) A critical review of assumptions about the prairie dog as a keystone species. Environmental Management, 24, 177-192.
38. Lacy, R.C., Miller, P.S., Nyhus, P.J., Pollak, J.P., Raboy, B.E. & Zeigler, S. (2013) Metamodels for transdisciplinary analysis of wildlife population dynamics. PLoS One, 8, e84211.
39. Livieri, T.M. (2006) Ten-Year History of the Conata Basin Black-Footed Ferret Population: 1996-2005. Prairie Wildlife Research, Wall, South Dakota. 49
40. Livieri, T.M. (2011) Black-footed ferret recovery in North America. Global Re-Introduction Perspectives: 2011. More Case Studies from Around the Globe (ed. P. Soorae ), pp. 157-164. IUCN/SSC Re-introduction Specialist Group and Abu Dhabi, UAE: Environment, Abu Dhabi, United Arab Emirates. 250p.
41. Livieri, T.M. & Anderson, E.M. (2012) Black-footed ferret home ranges in Conata Basin, South Dakota. Western North American Naturalist, 72, 196-205.
42. Lomolino, M.V. & Smith, G.A. (2001) Dynamic biogeography of prairie dog (Cynomys ludovicianus) towns near the edge of their range. Journal of Mammalogy, 82, 937-945.
43. Matchett, M.R., Biggins, D.E., Carlson, V., Powell, B. & Rocke, T. (2010) Enzootic plague reduces black-footed ferret (Mustela nigripes) survival in Montana. Vector-Borne and Zoonotic Diseases, 10, 27-35.
44. McCallum, H.I. & Dobson, A.P. (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology & Evolution, 10, 190-194.
45. McCallum, H.I. & Dobson, A.P. (2002) Disease, habitat fragmentation and conservation. Proceedings of the Royal Society of London Series B, 269, 2041-2049.
46. McCarthy, M.A. & Thompson, C. (2001) Expected minimum population size as a measure of threat. Animal Conservation, 4, 351-355.
47. Miller, P.S. & Lacy, R.C. (2003) Metamodels as a tool for risk assessment. Experiments in Consilience: Integrating Social and Scientific Responses to Save Endangered Species (eds F.R. Westley & P.S. Miller ), pp. 333-351. Island Press, Washington, DC.
48. Morris, W.F. & Doak, D.F. (2002) Quantitative Conservation Biology. Theory and Practice of Population Viability Analysis. Sinauer, Sunderland, MA.
49. Pauli, J.N., Buskirk, S.W., Williams, E.S. & Edwards, W.H.A. (2006) A plague epizootic in the black-tailed prairie dog (Cynomys ludovicianus). Journal of Wildlife Diseases, 42, 74-80.
50. Pollak, J.P., Miller, P.S., Lacy, R.C., Hungerford, L. & Bright, P. (2008) Outbreak Version 0.99. IUCN SSC Conservation Breeding Specialist Group, Apple Valley, MN.
51. Proctor, J., Haskins, B. & Forrest, S.C. (2006) Focal areas for conservation of prairie dogs and the grassland ecosystem. Conservation of the Black-Tailed Prairie Dog: Saving North America's Western Grasslands (ed. J.L. Hoogland ), pp. 232-247. Island Press, Washington, DC.
52. Prowse, T.A.A., Johnson, C.N., Lacy, R.C., Bradshaw, C.J.A., Pollak, J.P., Watts, M.J. & Brook, B.W. (2013) No need for disease: testing extinction hypotheses for the thylacine using multi-species metamodels. Journal of Animal Ecology, 82, 355-364.
53. Rocke, T.E., Williamson, J., Cobble, K.R., Busch, J.D., Antolin, M.F. & Wagner, D.M. (2012) Resistance to plague among black-tailed prairie dog populations. Vector-Borne and Zoonotic Diseases, 12, 111-116.
54. Richardson, L., Clark, T.W., Forrest, S.C. & Campbell, T.M. III (1986) Black-footed ferret recovery: a discussion of some options and considerations. Great Basin Naturalist Memoirs, 8, 169-184.
55. Sabo, J.L. (2008) Population viability and species interactions: life outside the single-species vacuum. Biological Conservation, 141, 276-286.
56. Salkeld, D.J., Salathé, M., Stapp, P. & Jones, J.H. (2010) Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance. Proceedings of the National Academy of Sciences USA, 107, 14247-14250.
57. Seery, D.B. & Matiatos, D.J. (2000) Response of wintering buteos to plague epizootics in prairie dogs. Western North American Naturalist, 60, 420-425.
58. Seery, D.B., Biggins, D.E., Montenieri, J.A., Enscore, R.E., Tanda, D.T. & Gage, K.L. (2003) Treatment of black-tailed prairie dog burrows with Deltamethrin to control fleas (Insecta: Siphonaptera) and plague. Journal of Medical Entomology, 40, 718-722.
59. Sidle, J.G., Johnson, D.H. & Euliss, B.R. (2001) Estimated areal extent of colonies of black-tailed prairie dogs in the northern great plains. Journal of Mammalogy, 82, 928-936.
60. Smith, K.F., Acevedo-Whitehouse, K. & Pedersen, A.B. (2009) The role of infectious diseases in biological conservation. Animal Conservation, 12, 1-12.
61. Soulé, M.E., Estes, J.A., Miller, B. & Honnold, D.L. (2005) Strongly interacting species. conservation policy, management, and ethics. BioScience, 55, 168-176.
62. Stromberg, M.R., Rayburn, R.L. & Clark, T.W. (1983) Black-footed ferret prey requirements-an energy balance estimate. Journal of Wildlife Management, 47, 67-73.
63. U.S. Fish & Wildlife Service (1988) Black-footed ferret recovery plan. U.S. Fish & Wildlife Service, Denver, Colorado.
64. U.S. Fish and Wildlife Service (2013) Recovery Plan for the Black-Footed Ferret (Mustela nigripes). U.S. Fish and Wildlife Service, Denver, CO U.S.A.
65. Williams, E.S., Kwiatkowski, D.R., Thome, E.T. & Boerger-Fields, A. (1994) Plague in a black-footed ferret. Journal of Wildlife Diseases, 30, 581-585.
66. Wisely, S.M., Santymire, R.M., Livieri, T.M., Mueting, S.A. & Howard, J. (2008) Genotypic and phenotypic consequences of reintroduction history in the black-footed ferret (Mustela nigripes). Conservation Genetics, 9, 389-399.