Abstract
Large-scale restoration programs have been implemented worldwide to counteract habitat loss and fragmentation from expansion and intensification of agriculture. These agri-environment programs create habitat patches imbedded in an agricultural matrix. The assumption is these patches benefit wildlife and that individuals either avoid agricultural fields or use them to increase their fitness. We selected eastern cottontails (Sylvilagus floridanus) as a focal species on restored grasslands in Illinois, USA to assess survival and to determine if maladaptive habitat selection for agricultural fields could create an ecological trap. We also investigated whether a mismatch between real and perceived predation risk could explain their habitat selection. We radiotracked 95 cottontails and estimated habitat-specific survival using known-fate models, and measured habitat selection using Manly’s standardized selection ratios. We also assessed perceived predation risk with giving-up density experiments. Survival of cottontails was higher in restored grasslands relative to agricultural and developed areas. Habitat selection did not reflect this spatial variation in mortality risk, however, when crops were present on the landscape. Agricultural lands created an equal-preference trap. Cottontails did not accurately assess predation risk; they did not recognize that agricultural fields were risky. This mismatch could be due to cottontails’ emphasis on protecting themselves from avian predators rather than from coyotes (Canis latrans), which currently are their main predator. Our novel study demonstrates how dynamic landscape context can create ecological traps. Such unexpected outcomes can reduce the conservation benefits of restoration programs.
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References
Abu Baker MA, Brown JS (2009) Patch area, substrate depth, and richness affect giving-up densities: a test with mourning doves and cottontail rabbits. Oikos 118:1721–1731
Abu Baker MA, Emerson SE, Brown JS (2015) Foraging and habitat use of eastern cottontails (Sylvilagus floridanus) in an urban landscape. Urban Ecosyst 18:977–987
Althoff DP (1983) Daytime home range, habitat selection, and microenvironments used by cottontail rabbits in central Pennsylvania. Dissertation, The Pennsylvania State University
Althoff DP, Storm GL, Dewalle DR (1997) Daytime habitat selection by cottontails in central Pennsylvania. J Wildl Manage 61:450–459
Arias-Del Razo I, Hernández L, Laundré JW, Myers O (2011) Do predator and prey foraging activity patterns match? A study of coyotes (Canis latrans), and lagomorphs (Lepus californicus and Sylvilagus audobonii). J Arid Environ 75:112–118
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manage 74:1175–1178
Arthur SM, Manly BFJ, McDonald LL, Garner GW (1996) Assessing habitat selection when availability changes. Ecology 77:215–227
Batschelet E (1981) Circular statistics in biology. Academic Press, London
Battin J (2004) When good animals love bad habitats: ecological traps and the conservation of animal populations. Conserv Biol 18:1482–1491
Baundry J, Burel F, Aviron S, Martin M, Ouin A, Pain G, Thenail C (2003) Temporal variability of connectivity in agricultural landscapes: do farming activities help? Landsc Ecol 18:303–314
Bedoya-Perez MA, Carthey AJR, Mella VSA et al (2013) A practical guide to avoid giving up on giving-up densities. Behav Ecol Sociobiol 67:1541–1553
Bell SS, Fonseca MS, Moten LB (1997) Linking restoration and landscape ecology. Restor Ecol 5:318–323
Berry WB, Schooley RL, Ward MP (2017) Landscape context affects use of restored grasslands by mammals in a dynamic agroecosystem. Am Midl Nat 177:165–182
Boland KM, Litvaitis JA (2008) Role of predation and hunting on eastern cottontail mortality at Cape Cod National Seashore, Massachusetts. Can J Zool 86:918–927
Bond BT, Burger LW, Leopold BD, Godwin KD (2001a) Survival of cottontail rabbits (Sylvilagus floridanus) in Mississippi and an examination of latitudinal variation. Am Midl Nat 145:127–136
Bond BT, Leopold BD, Burger LW, Godwin KD (2001b) Movements and home range dynamics of cottontail rabbits in Mississippi. J Wildl Manage 65:1004–1013
Brillhart DE, Kaufman DW (1995) Spatial and seasonal variation in prey use by coyotes in north-central Kansas. Southwest Nat 40:160–166
Brooks TM, Mittermeier RA, Mittermeier CG et al (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16:909–923
Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47
Brown JS, Alkon PU (1990) Testing values of crested porcupine habitats by experimental food patches. Oecologia 83:512–518
Brudvig LA (2011) The restoration of biodiversity: where has research been and where does it need to go? Am J Bot 98:549–558
Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information theoretic approach, 2nd edn. Springer, New York
Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519
Celis-Murillo A, Stodola KW, Pappadopoli B, Burton JM, Ward MP (2016) Seasonal and daily patterns of nocturnal singing in the field Sparrow (Spizella pusilla). J Ornithol 157:853–860
Chapman JA, Hockma JG, Edwards WR (1982) Cottontails (Sylvilagus floridanus and allies). In: Chapman JA, Feldhammer GA (eds) Wild mammals of North America. Johns Hopkins University Press, Baltimore, pp 83–123
Concepción ED, Díaz M, Baquero RA (2008) Effects of landscape complexity on the ecological effectiveness of agri-environment schemes. Landsc Ecol 23:135–148
Cosentino BJ, Schooley RL, Phillips CA (2011) Connectivity of agroecosystems: dispersal costs can vary among crops. Landsc Ecol 26:371–379
Cox EW, Garrott RA, Cary JR (1997) Effect of supplemental cover on survival of snowshoe hares and cottontail rabbits in patchy habitat. Can J Zool 75:1357–1363
Crawford JC, Nielsen CK, Schauber EM (2018) Survival and habitat use of sympatric lagomorphs in bottomland hardwood forests. Can J Zool 96:713–722
Deppe JL, Ward MP, Bolus RT et al (2015) Fat, weather, and date affect migratory songbirds’ departure decisions, routes, and time it takes to cross the Gulf of Mexico. Proc Natl Acad Sci 112:E6331–E6338
Donald PF, Evans AD (2006) Habitat connectivity and matrix restoration: the wider implications of agri-environment schemes. J Appl Ecol 43:209–218
Duggan JM, Heske EJ, Schooley RL (2012) Gap-crossing decisions by adult Franklin’s ground squirrels in agricultural landscapes. J Mammal 93:1231–1239
Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175
Dusi JL (1952) The food habits of several populations of cottontail rabbits in Ohio. J Wildl Manage 16:180–186
Duvick DN, Cassman KG (1999) Post-green revolution trends in yield potential of temperate maize in the north-central United States. Crop Sci 39:1622–1630
Elbroch LM, Lendrum PE, Alexander P, Quigley H (2015) Cougar den site selection in the Southern Yellowstone Ecosystem. Mamm Res 60:89–96
Ellis EC, Goldewijk KK, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606
Fahrig L, Baudry J, Brotons L et al (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112
Ferris J, Siikamaki J (2009) Conservation reserve program and wetland reserve program: primary land retirement programs for promoting farmland conservation. Resources For the Future, Washington, DC
Fritsky RS (2006) Effects of the conservation reserve enhancement program on abundance and survival of Eastern Cottontails in Pennsylvania. The Pennsylvania State University, Thesis
Gosselink TE, Van Deelen TR, Warner RE, Joselyn MG (2003) Temporal habitat partitioning and spatial use of coyotes and red foxes in east-central Illinois. J Wildl Manage 67:90–103
Griffin PC, Mills SL (2009) Sinks without borders: snowshoe hare dynamics in a complex landscape. Oikos 118:1487–1498
Hale R, Swearer SE (2016) Ecological traps: current evidence and future directions. Proc R Soc B 283:20152647
Hale R, Swearer SE (2017) When good animals love bad restored habitat: how maladaptive habitat selection can constrain restoration. J Appl Ecol 54:1478–1486
Henke SE, Bryant FC (1999) Effects of coyote removal on the faunal community in western Texas. J Wildl Manage 63:1066–1081
Heske E, Miller M (1995) Coyotes in the corn-fields. Ill Nat Hist Surv Rep 334:1
Hiron M, Berg Å, Pärt T (2012) Do skylarks prefer autumn sown cereals? Effects of agricultural land use, region and time in the breeding season on density. Agric Ecosyst Environ 150:82–90
Hobbs RJ, Norton DA (1996) Towards a conceptual framework for restoration ecology. Restor Ecol 4:93–110
Hoekstra JM, Boucher TM, Ricketts TH, Roberts C (2005) Confronting a biome crisis: global disparities of habitat loss and protection. Ecol Lett 8:23–29
Humberg LA, Devault TL, Macgowan BJ, Beasley JC, Rhodes OE (2007) Crop depredation by wildlife in northcentral Indiana. In: Stewart A (ed) Proceedings of the national wild turkey symposium. pp 199–205
Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503
Illinois State Geological Survey, Illinois Natural Resources Geospatial Data Clearinghouse. 2015. NAIP Digital Orthophoto Quadrangle Data. https://clearinghouse.isgs.illinois.edu/data/imagery/2015-illinois-naip-digital-orthophoto-quadrangle-data. Accessed Feb 2017
Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71
Keith LB, Bloomer SEM (1993) Differential mortality of sympatric snowshoe hares and cottontail rabbits in central Wisconsin. Can J Zool 71:1694–1697
Kleijn D, Sutherland WJ (2003) How effective are European agri-environment schemes in conserving and promoting biodiversity? J Appl Ecol 40:947–969
Korschgen LJ (1957) Food habits of the coyote in Missouri. J Wildl Manage 21:424–435
Korschgen LJ (1980) Food and nutrition of cottontail rabbits in Missouri. Mo Dept Conserv Terr Ser 6:1–16
Kovach WL (2009) Oriana—circular statistics for windows, version 3. Kovach Computing Services, Pentraeth
Kuussaari M, Bommarco R, Heikkinen RK et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571
Laundré JW, Calderas JMM, Hernández L (2009) Foraging in the landscape of fear, the predator’s dilemma: where should I hunt? Open Ecol J 2:1–6
Laundré JW, Hernández L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7
Longland WS (1991) Risk of predation and food consumption by black-tailed jackrabbits. J Range Manage 44:447–450
Lord RD (1963) The cottontail rabbit in Illinois. Ill Dept Conserv Tech Bull 3:1–94
MacCracken J, Hansen R (1987) Coyote feeding strategies in southeastern Idaho: optimal foraging by an opportunistic predator? J Wildl Manage 51:278–285
Mankin PC, Warner RE (1999a) Responses of eastern cottontails to intensive row-crop farming. J Mamm 80:940–949
Mankin PC, Warner RE (1999b) A regional model of the eastern cottontail and land-use changes in Illinois. J Wildl Manage 63:956–963
Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP (2002) Resource selection by animals: statistical design and analysis for field studies, 2nd edn. Kluwer Academic Publishers, Dordrecht
Marsden HM, Holler NR (1964) Social behavior in confined populations of the cottontail and the swamp rabbit. Wildl Monogr 27:938–942
Medve KA (1987) Eastern cottontail habitat use and survival in southern Illinois. Dissertation, Southern Illinois University
Menz MHM, Dixon KW, Hobbs RJ (2013) Hurdles and opportunities for landscape-scale restoration. Science 339:526–527
Mulligan MP, Schooley RL, Ward MP (2013) Effects of connectivity and regional dynamics on restoration of small mammal communities in midwestern grasslands. Restor Ecol 21:678–685
Nawrocki JA (2017) Dangerous misperceptions with consequences: survival of eastern cottontails on restored grasslands surrounded by agriculture. Thesis, University of Illinois
Newbold T, Hudson LN, Hill SLL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50
Nisi AC, Hernandez DL, English LP, Rogers ES (2015) Patterns of selective herbivory on five prairie legume species. Am Midl Nat 173:110–121
NOAA National Weather Service Forecast Office (2017) Annual Climate Report. http://w2.weather.gov/climate/index.php?wfo=ilx. Accessed March 2017
Noon BR (1981) Techniques for sampling avian habitats. In: Capen DE (ed) The use of multivariate statistics in studies of wildlife habitat. USDA For Ser Gen Tech Rep RM-57
Northrup JM, Stenhouse GB, Boyce MS (2012) Agricultural lands as ecological traps for grizzly bears. Anim Conserv 15:369–377
Petersen L (1979) Ecology of great horned owls and red-tailed hawks in southeastern Wisconsin. Tech Bull Dept Nat Res Wis 111:1–63
Randa LA, Cooper DM, Meserve PL, Yunger JA (2009) Prey switching of sympatric canids in response to variable prey abundance. J Mamm 90:594–603
Robertson BA, Hutto RL (2006) A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87:1075–1085
Samson F, Knopf F (1994) Prairie conservation in North America. Bioscience 44:418–421
Santangeli A, Lehikoinen A, Bock A, Peltonen-Sainio P, Jauhiainen L, Girardello M, Valkama J (2018) Stronger response of farmland birds than farmers to climate change leads to the emergence of an ecological trap. Biol Conserv 217:166–172
Sauer JR, Fallon JE, Johnson R (2003) Use of North American breeding bird survey data to estimate population change for bird conservation regions. J Wildl Manage 67:372–389
Schipper J, Chanson JS, Chiozza F et al (2008) The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322:225–230
Schooley RL (1994) Annual variation in habitat selection: patterns concealed by pooled data. J Wildl Manage 58:367–374
Sikes RS, Gannon WL, the Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253
Stephens DW, Brown JS, Ydenberg RC (2007) Foraging behavior and ecology. The University of Chicago Press, Chicago
Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786
Thibault I, Ouellet J-P (2005) Hunting behaviour of eastern coyotes in relation to vegetation cover, snow conditions, and hare distribution. Ecoscience 12:466–475
Trent TT, Rongstad OJ (1974) Home range and survival of cottontail rabbits in southwestern Wisconsin. J Wildl Manage 38:459–472
Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8:857–874
USDA Farm Service Agency (2017) State acres for wildlife enhancement (SAFE) program. United States Department of Agriculture. Washington, DC. Available from https://www.fsa.usda.gov/Assets/USDA-FSA-Public/usdafiles/FactSheets/2017/safe_fact_sheet_jan2017.pdf. Accessed March 2017
USDA NASS [U.S. Department of Agriculture National Agricultural Statistics Service] (2012) 2012 census of agriculture. https://www.agcensus.usda.gov/Publications/2012/Full_Report/Volume_1,_Chapter_1_US/usv1.pdf. Accessed Feb 2017
Villafuerte R, Litvaitis JA, Smith DF (1997) Physiological responses by lagomorphs to resource limitations imposed by habitat fragmentation: implications for condition-sensitive predation. Can J Zool 75:148–151
Wagner F, Stoddart L (1972) Influence of coyote predation on black-tailed jackrabbit populations in Utah. J Wildl Manage 36:329–342
Ward MP, Sperry JH, Weatherhead PJ (2013) Evaluation of automated radio telemetry for quantifying movements and home ranges of snakes. J Herpetol 47:337–345
Warner RE (1994) Agricultural land use and grassland habitat in Illinois: future shock for Midwestern birds? Conserv Biol 8:147–156
Washburn BE (2000) Ecological relationships among eastern cottontail rabbits, tall fescue, and native warm-season grasses. Dissertation, University of Kentucky
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139
Wibbicombe W, Thelen K (2002) Row width and plant density effects on corn grain production in the northern corn belt. Agron J 94:1020–1023
Windberg LA, Mitchell CD (1990) Winter diets of coyotes in relation to prey abundance in southern Texas. J Mammal 71:439–447
Young JK, Andelt WF, Terletzky PA, Shivik JA (2006) A comparison of coyote ecology after 25 years: 1978 versus 2003. Can J Zool 84:573–585
Acknowledgements
Funding was provided by the U.S. Fish and Wildlife Service (Federal Aid in Wildlife Restoration Program) through the Illinois Department of Natural Resources. We thank S. Beyer, S. Chow, C. Dempsey, and L. Kelter for field assistance, C. Miller for providing cottontail trend data, and B. Berry for collecting the camera trap data. We are grateful to T. J. Benson, A. Ahlers, T. Lyons, and M. Whitby for help with statistical analysis. E. Heske, B. Robertson, and anonymous reviewer provided helpful comments on an earlier version of the manuscript.
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Nawrocki, J.A., Schooley, R.L. & Ward, M.P. When good animals love restored habitat in bad neighborhoods: ecological traps for eastern cottontails in agricultural landscapes. Biodivers Conserv 28, 953–973 (2019). https://doi.org/10.1007/s10531-019-01704-z
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DOI: https://doi.org/10.1007/s10531-019-01704-z