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Ecosphere Volume 10 ,Issue 3 ,2019-03-18
Accounting for heterogeneous invasion rates reveals management impacts on the spatial expansion of an invasive species
Kim M. Pepin 1 David W. Wolfson 2 Ryan S. Miller 2 Michael A. Tabak 2 Nathan P. Snow 1 Kurt C. VerCauteren 1 Amy J. Davis 1
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Received 2019-02-12, accepted for publication 2019-02-15, Published 2019-02-15

Abstract Success of large‐scale control programs for established invasive species is challenging to evaluate because of spatial variability in expansion rates, management techniques, and the strength of management intensity. For a well‐established invasive species in the spreading phase of invasion, a useful metric of impact is the magnitude by which control slows the rate of spatial spread. The prevention of spatial spreading likely results in substantial benefits in terms of ecosystem or economic damage that is prevented by an expanding invasive species. To understand how local management actions could impact the spatial spread of an established invasive species, we analyzed distribution and management data for feral swine across contiguous United States using occupancy analysis. We quantified changes in the rate of spatial expansion of feral swine and its relationship to local management actions. We found that after 4 yr of enhanced control, invasion probability decreased by 8% on average relative to pre‐program rates. This decrease was as high as 15% on average in states with low‐density populations of feral swine. The amount of decrease in invasion rate was attributed to removal intensity in neighboring counties and depended on the extent of neighboring counties with feral swine (spatial heterogeneity in local invasion pressure). Although we did not find a significant overall increase in the probability of elimination, increased elimination probability tended to occur in regions with low invasion pressure. Accounting for spatial heterogeneity in invasion pressure was important for quantifying management impacts (i.e., the relationship between management intensity and spatial spreading processes) because management impacts changed depending on the strength of invasion pressure from neighboring counties. Predicting reduction in spatial spread of an invasive species is an important first step in valuation of overall damage reduction for invasive species control programs by providing estimates of where a species may be, and thus which natural and agricultural resources would be affected, if the control program had not been operating. For minimizing losses from spatial expansion of an invasive species, our framework can be used for adaptive resource prioritization to areas where spatial expansion and underlying damage potential are concurrently highest.


wild pig;Sus scrofa;spatial spread;spatial heterogeneity;management;invasive species;invasion rate;expansion;elimination;control


© 2019 The Ecological Society of America


Raw counts of pigs removed by each removal method. Pie charts show MIS data for each state as the proportion of removals by each method. Size of the pie chart corresponds to the total number of pigs removed in the state during the year (removal counts indicated by the gray scale circles).

Raw counts of pigs removed by ASDs and overlayed onto the pig distribution as observed in NFSMS data. Red shades show removal intensity where there are pigs. Black shows where there are pigs but no removals. Blue shades show removal intensity in areas where there is no distribution data coverage. White represents areas where pigs have not been reported.

Probability of invasion and extinction using space‐time model. (A) Invasion (black circles) and extinction (gray triangles) probabilities for counties on average during transitions for the indicated time frames (X‐axes). Raw data: filled symbols; model predictions: open symbols with 95% prediction intervals. (B and C) Absolute difference in the predicted proportion of counties (Appendix S1: Table S4, S6) with new invasions (B) or extinctions (C) relative to the previous time period (where 2014–2015 is compared against 2012–2013). Gray: no NFSMS data; white: no change. Red scale indicates increased invasion probability (B) or decreased extinction probability (C); blue scale indicates decreased invasion probability (B) or decreased extinction probability (C).

Effects of invasion pressure and management for 2014–2015 (early) and 2016–2017 (late). Predictions of invasion (top) and extinction probabilities (bottom) from the management model (Appendix S1: Table S3) with 95% prediction intervals (shading). Left plots show the relationship of invasion and extinction probabilities as a function of invasion pressure. The vertical lines show the values of invasion pressure that are used in the middle and right plots. Middle and right plots show the effects of management intensity on invasion and extinction probabilities.


Kim M. Pepin.National Wildlife Research Center, USDA‐APHIS, Wildlife Services, 4101 Laporte Avenue, Fort Collins, Colorado, 80521, USA.kim.m.pepin@aphis.usda.gov


Kim M. Pepin,David W. Wolfson,Ryan S. Miller,Michael A. Tabak,Nathan P. Snow,Kurt C. VerCauteren,Amy J. Davis. Accounting for heterogeneous invasion rates reveals management impacts on the spatial expansion of an invasive species. Ecosphere ,Vol.10, Issue 3(2019)



[1] Choquenot, D., J. Hone, and G. Saunders. 1999. Using aspects of predator‐prey theory to evaluate helicopter shooting for feral pig control. Wildlife Research 26:251–261.
[2] Hernandez, F. A., B. M. Parker, C. L. Pylant, T. J. Smyser, A. J. Piaggio, S. L. Lance, M. P. Milleson, J. D. Austin, and S. M. Wisely. 2018. Invasion ecology of wild pigs (Sus scrofa) in Florida, USA: the role of humans in the expansion and colonization of an invasive wild ungulate. Biological Invasions 20:1865–1880.
[3] Choquenot, D., J. McIlroy, and T. Korn. 1996. Managing Vertebrate Pests: feral Pigs. Bureau of Resource Sciences, Australian Government Publishing Service, Canberra, Australian Capital Territory, Australia.
[4] Lavelle, M. J., N. P.Snow, J. W. Fischer, J. M. Halseth, E. H. VanNatta, and K. C. VerCauteren. 2017. Attractants for wild pigs: current use, availability, needs, and future potential.
[5] White, G. C., and K. P. Burnham. 1999. Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139.
[6] Corn, J. L., and T. R. Jordan. 2017. Development of the national feral swine map, 1982–2016. Wildlife Society Bulletin 41:758–763.
[7] Hone, J. 2002. Feral pigs in Namadgi National Park, Australia: dynamics, impacts and management. Biological Conservation 105:231–242.
[8] Lewis, J. S., M. L. Farnsworth, C. L. Burdett, D. M. Theobald, M. Gray, and R. S. Miller. 2017. Biotic and abiotic factors predicting the global distribution and population density of an invasive mammal. Scientific Reports 7:44152.
[9] Hone, J., V. A. Drake, and C. J. Krebs. 2017. The effort‐outcomes relationship in applied ecology: evaluation and implications. BioScience 67:845–852.
[10] MacKenzie, D. I., J. D. Nichols, J. A. Royle, K. H. Pollock, L. Bailey, and J. E. Hines. 2006. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier, Academic Press, Cambridge, USA.
[11] Booy, O., et al. 2017. Risk management to prioritise the eradication of new and emerging invasive non‐native species. Biological Invasions 19:2401–2417.
[12] Pepin, K. M., A. J. Davis, and K. C. VerCauteren. 2017b. Efficiency of different spatial and temporal strategies for reducing vertebrate pest populations. Ecological Modelling 365:106–118.
[13] R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
[14] Keiter, D., J. J. Mayer, and J. C. Beasley. 2016. What's in a common” name? A call for consistent terminology for referring to non‐native Sus scrofa. Wildlife Society Bulletin 40:384–387.
[15] Centner, T. J., and R. M. Shuman. 2015. Governmental provisions to manage and eradicate feral swine in areas of the United States. Ambio 44:121–130.
[16] Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information‐theoretic approach. Second edition. Springer‐Verlag, New York, New York, USA.
[17] Pepin, K. M., A. J. Davis, F. L. Cunningham, K. C. VerCauteren, and D. C. Eckery. 2017a. Potential effects of incorporating fertility control into typical culling regimes in wild pig populations. PLoS ONE 12:e0183441.
[18] West, B. C., A. L. Cooper, and J. B. Armstrong. 2009. Managing wild pigs: a technical guide. Human‐Wildlife Interactions Monograph 1:1–55.
[19] Weeks, P., and J. Packard. 2009. Feral hogs: invasive species or nature's bounty? Human Organization 68:280–292.
[20] Massei, G., and P. V. Genov. 2004. The environmental impact of wild boar. Galemys 16:135–145.
[21] Garnas, J. R., M. A. Auger‐Rozenberg, A. Roques, C. Bertelsmeier, M. J. Wingfield, D. L. Saccaggi, H. E. Roy, and B. Slippers. 2016. Complex patterns of global spread in invasive insects: eco‐evolutionary and management consequences. Biological Invasions 18:935–952.
[22] Massei, G., et al. 2015. Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Management Science 71:492–500.
[23] Hartin, R. E. 2006. Feral hogs ‐ status and distribution in MO. University of Missouri, Columbia, Missouri, USA. https://www.aphis.usda.gov/wildlife_damage/nwrc/downloads/Hardin.pdf
[24] McCann, B. E., and D. K. Garcelon. 2008. Eradication of feral pigs from Pinnacles National Monument. Journal of Wildlife Management 72:1287–1295.
[25] Goedbloed, D. J., P. van Hooft, H. J. Megens, K. Langenbeck, W. Lutz, R. Crooijmans, S. E. van Wieren, R. C. Ydenberg, and H. H. T. Prins. 2013. Reintroductions and genetic introgression from domestic pigs have shaped the genetic population structure of Northwest European wild boar. BMC Genetics 14:10.
[26] Snow, N. P., M. A. Jarzyna, and K. C. VerCauteren. 2017a. Interpreting and predicting the spread of invasive wild pigs. Journal of Applied Ecology 54:2022–2032.
[27] Felix, R. K., S. L. Orzell, E. A. Tillman, R. M. Engeman, and M. L. Avery. 2014. Fine‐scale, spatial and temporal assessment methods for feral swine disturbances to sensitive plant communities in south‐central Florida. Environmental Science and Pollution Research 21:10399–10406.
[28] McIntosh, E. J., R. L. Pressey, S. Lloyd, R. J. Smith, and R. Grenyer. 2017. The impact of systematic conservation planning. Pages 677–697 in , and T. P. Tomich, editors. Annual Review of Environment and Resources, Volume 42. Annual Reviews, Palo Alto, California, USA.
[29] Shigesada, N., K. Kawasaki, and Y. Takeda. 1995. Modelling stratified diffusion in biological invasions. American Naturalist 146:229–251.
[30] McClure, M. L., C. L. Burdett, M. L. Farnsworth, M. W. Lutman, D. M. Theobald, P. D. Riggs, D. A. Grear, and R. S. Miller. 2015. Modeling and mapping the probability of occurrence of invasive wild pigs across the contiguous United States. PLoS ONE 10:e0133771.
[31] Snow, N. P., J. A. Foster, J. C. Kinsey, S. T. Humphrys, L. D. Staples, D. G. Hewitt, and K. C. VerCauteren. 2017b. Development of toxic bait to control invasive wild pigs and reduce damage. Wildlife Society Bulletin 41:256–263.
[32] McClure, M. L., C. L. Burdett, M. L. Farnsworth, S. J. Sweeney, and R. S. Miller. 2018. A globally‐distributed alien invasive species poses risks to United States imperiled species. Scientific Reports 8:5331.
[33] Gallardo, B., and D. C. Aldridge. 2013. Priority setting for invasive species management: risk assessment of Ponto‐Caspian invasive species into Great Britain. Ecological Applications 23:352–364.
[34] Miller, R. S., S. M. Opp, and C. T. Webb. 2018. Determinants of invasive species policy: Print media and agriculture determine U.S. invasive wild pig policy. Ecosphere 9:e02379.
[35] Fielding, A. H., and J. F. Bell. 1997. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation 24:38–49.
[36] Adams, C. E., B. J. Higginbotham, D. Rollins, R. B. Taylor, R. Skiles, M. Mapston, and S. Tuman. 2005. Regional perspectives and opportunities for feral hog management in Texas. Wildlife Society Bulletin 33:1312–1320.
[37] Anderson, A., C. Slootmaker, E. Harper, J. Holderieath, and S. A. Shwiff. 2016. Economic estimates of feral swine damage and control in 11 US states. Crop Protection 89:89–94.
[38] Ramsey, D. S., J. Parkes, and S. A. Morrison. 2009. Quantifying eradication success: the removal of feral pigs from Santa Cruz Island, California. Conservation Biology 23:449–459.
[39] Tabak, M. A., A. J. Piaggio, R. S. Miller, R. A. Sweitzer, and H. B. Ernest. 2017. Anthropogenic factors predict movement of an invasive species. Ecosphere 8:e01844.
[40] Decker, D. J., and L. C. Chase. 1997. Human dimensions of living with wildlife: a management challenge for the 21st century. Wildlife Society Bulletin 25:788–795.
[41] National Agricultural Statistics Service. 2018. https://www.nass.usda.gov/Charts_and_Maps/Crops_County/indexpdf.php
[42] Morrison, S. A., N. Macdonald, K. Walker, L. Lozier, and M. R. Shaw. 2007. Facing the Dilemma at Eradication's End: uncertainty of Absence and the Lazarus Effect. Frontiers in Ecology and the Environment 5:271–276.
[43] Tabak, M. A., C. T. Webb, and R. S. Miller. 2018. Propagule size and structure, life history, and environmental conditions affect establishment success of an invasive species. Scientific Reports 8:10313.
[44] Miller, R. S., S. J. Sweeney, C. Slootmaker, D. A. Grear, P. A. Salvo, D. Kiser, and S. A. Shwiff. 2017. Cross‐species transmission potential between wild pigs, livestock, poultry, wildlife, and humans: implications for disease risk management in North America. Scientific Reports 7:7821.
[45] Elliott, G., and J. Kemp. 2016. Large‐scale pest control in New Zealand beech. Ecological Management & Restoration 17:200–209.
[46] Efford, M. G., and D. K. Dawson. 2012. Occupancy in continuous habitat. Ecosphere 3:e32.
[47] Andow, D., P. Kareiva, S. A. Levin, and A. Okubo. 1990. Spread of invading organisms. Landscape Ecology 4:177–188.
[48] Early, R., et al. 2016. Global threats from invasive alien species in the twenty‐first century and national response capacities. Nature Communications 7:12485.
[49] Bankovich, B., E. Boughton, R. Boughton, M. L. Avery, and S. M. Wisely. 2016. Plant community shifts caused by feral swine rooting devalue Florida rangeland. Agriculture, Ecosystems and Environment 220:45–54.
[50] Bieber, C., and T. Ruf. 2005. Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. Journal of Applied Ecology 42:1203–1213.
[51] Barrios‐Garcia, M. N., and S. A. Ballari. 2012. Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biological Invasions 14:2283–2300.
[52] Spencer, P. B. S., and J. O. Hampton. 2005. Illegal translocation and genetic structure of feral pigs in Western Australia. Journal of Wildlife Management 69:377–384.