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Mitigating road impacts on animals through learning principles

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Abstract

Roads are a nearly ubiquitous feature of the developed world, but their presence does not come without consequences. Many mammals, birds, reptiles, and amphibians suffer high rates of mortality through collision with motor vehicles, while other species treat roads as barriers that reduce gene flow between populations. Road effects extend beyond the pavement, where traffic noise is altering communities of songbirds, insects, and some mammals. Traditional methods of mitigation along roads include the creation of quieter pavement and tires and the construction of physical barriers to reduce sound transmission and movement. While effective, these forms of mitigation are costly and time-consuming. One alternative is the use of learning principles to create or extinguish aversive behaviors in animals living near roads. Classical and operant conditioning are well-documented techniques for altering behavior in response to novel cues and signals. Behavioral ecologists have used conditioning techniques to mitigate human–wildlife conflict challenges, alter predator–prey interactions, and facilitate reintroduction efforts. Yet, these principles have rarely been applied in the context of roads. We suggest that the field of road ecology is ripe with opportunity for experimentation with learning principles. We present tangible ways that learning techniques could be utilized to mitigate negative roadside behaviors, address the importance of evaluating fitness within these contexts, and evaluate the longevity of learned behaviors. This review serves as an invitation for empirical studies that test the effectiveness of learning paradigms as a mitigation tool in the context of roads.

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References

  • Adkins-Regan E, MacKillop EA (2003) Japanese quail (Coturnix japonica) inseminations are more likely to fertilize eggs in a context predicting mating opportunities. P Roy Soc B-Biol Sci 270:1685–1689. doi:10.1098/rspb.2003.2421

    Article  Google Scholar 

  • Alonso R, Orejas P, Lopes F, Sanz C (2011) Pre-release training of juvenile little owls Athene noctua to avoid predation. Anim Biodiv Conserv 34:389–393

    Google Scholar 

  • Anderson DC, Crowell CR, Cunningham CL, Lupo JV (1979) Behavior during shock exposure as a determinant of subsequent interference with shuttle box escape–avoidance learning in the rat. J Exp Psychol Anim Behav 5:243–257. doi:10.1037/0097-7403.5.3.243

    Article  Google Scholar 

  • Anisman H, DeCatanzaro D, Remington G (1978) Escape performance following exposure to inescapable shock: deficits in motor response maintenance. J Exp Psychol Anim Behav 4:197–218. doi:10.1037/0097-7403.4.3.197

    Article  Google Scholar 

  • Baskaran N, Boominathan D (2010) Road kill of animals by highway traffic in the tropical forests of Mudumalai Tiger Reserve, southern India. J Threat Taxa 2:753–759

    Article  Google Scholar 

  • Beckmann J, Clevenger AP, Huijser MP, Hilty JA (2010) Safe passages: highways, wildlife, and habitat connectivity. Island Press, Washington

    Google Scholar 

  • Berger-Tal O, Blumstein DT, Carroll S, Fisher RN, Mesnick SL, Owen MA, Saltz D, St. Claire CC, Swaisgood RR (2015) A systematic survey of the integration of behavior into wildlife conservation and management. Conserv Biol doi: 10.1111/cobi.12654

  • Biedenweg TA, Parsons MH, Fleming PA, Blumstein DT (2011) Sounds scary? Lack of habituation following the presentation of novel sounds. PLoS One 6:e14549. doi:10.1371/journal.pone.0014549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blumstein DT, Berger-Tal O (2015) Understanding sensory mechanisms to develop effective conservation and management tools. Curr Opin Behav Sci 6:13–18. doi:10.1016/j.cobeha.2015.06.008

    Article  Google Scholar 

  • Book DL, Freeberg TM (2015) Titmouse calling and foraging are affected by head and body orientation of cat predator models and possible experience with real cats. Anim Cognit 18:1155–1164. doi:10.1007/s10071-015-0888-7

    Article  CAS  Google Scholar 

  • Braun ME, Walsh SJ, Horner JL, Chuter R (2013) Noise source characteristics in the ISO 362 vehicle pass-by noise test: literature review. Appl Acoust 74:1241–1265. doi:10.1016/j.apacoust.2013.04.005

    Article  Google Scholar 

  • Bruinderink GWTAG, Hazebroek E (1996) Ungulate traffic collisions in Europe. Conserv Biol 10:1059–1067. doi:10.1046/j.1523-1739.1996.10041059.x

    Article  Google Scholar 

  • Brumm H (2004) Causes and consequences of song amplitude adjustment in a territorial bird: a case study in nightingales. An Acad Bras Cienc 76:289–295

    Article  PubMed  Google Scholar 

  • Bugnyar T, Huber L (1997) Push or pull: an experimental study on imitation in marmosets. Anim Behav 54:817–831. doi:10.1006/anbe.1996.0497

    Article  CAS  PubMed  Google Scholar 

  • Burke DM, Nol E (2000) Landscape and fragment size effects on reproductive success of forest-breeding birds in Ontario. Ecol Appl 10:1749–1761. doi:10.1890/1051-0761(2000)010[1749:LAFSEO]2.0.CO;2

    Article  Google Scholar 

  • Cardoso GC (2014) Nesting and acoustic ecology, but not phylogeny, influence passerine urban tolerance. Global Change Biol 20:803–810

    Article  Google Scholar 

  • Chan AA, Giraldo-Perez P, Smith S, Blumstein DT (2010) Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol Lett 6:458–461. doi:10.1098/rsbl.2009.1081

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen HL, Koprowski JL (2015) Animal occurrence and space use change in the landscape of anthropogenic noise. Biol Conserv 192:315–322. doi:10.1016/j.biocon.2015.10.003

    Article  Google Scholar 

  • Coffin AW (2007) From roadkill to road ecology: a review of the ecological effects of roads. J Transp Geogr 15:396–406. doi:10.1016/j.jtrangeo.2006.11.006

    Article  Google Scholar 

  • Cosentino BJ, Marsh DM, Jones KS, Apodaca JJ, Bates C, Beach J, Beard KH, Becklin K, Bell JM, Crockett C, Fawson G, Fjelsted J, Forys EA, Genet KS, Grover M, Holmes J, Indeck K, Karraker NE, Kilpatrick ES, Langen TA, Mugel SG, Molina A, Vonesh JR, Weaver RJ, Willey A (2014) Citizen science reveals widespread negative effects of roads on amphibian distributions. Biol Conserv 180:31–38. doi:10.1016/j.biocon.2014.09.027

    Article  Google Scholar 

  • Courter JR, Ritchison G (2010) Alarm calls of tufted titmice convey information about predator size and threat. Behav Ecol 21:936–942. doi:10.1093/beheco/arq086

    Article  Google Scholar 

  • Cramer P, Olsson M, Gadd ME, van der Ree R, Sielecki LE (2015) Transportation and large herbivores. In: van der Ree R, Smith DJ, Grilo C (eds) Handbook of road ecology. Wiley, West Sussex, pp 344–352

    Google Scholar 

  • Cromsigt JPGM, Kuijper DPJ, Adam M, Beschta RL, Churski M, Eycott A, Kerley GIH, Mysterud A, Schmidt K, West K (2013) Hunting for fear: innovating management of human-wildlife conflicts. J Appl Ecol 50:544–549. doi:10.1111/1365-2664.12076

    Article  Google Scholar 

  • DeJong LN, Cowell SD, Nguyen TNN, Proppe DS (2015) Attracting songbirds with conspecific playback: a community approach. Behav Ecol 26:1379–1388. doi:10.1093/beheco/arv094

    Article  Google Scholar 

  • Domjan M (2010) The principles of learning and behavior. Wadsworth Publishing, Stamford

    Google Scholar 

  • Donnelly R, Marzluff JM (2006) Relative importance of habitat quantity, structure, and spatial pattern to birds in urbanizing environments. Urban Ecosystems 9:99–117. doi:10.1007/s11252-006-7904-2

    Article  Google Scholar 

  • Downing RJ, Rytwinski T, Fahrig L (2015) Positive effects of roads on small mammals: a test of the predation release hypothesis. Ecol Res 30:651–662. doi:10.1007/s11284-015-1264-4

    Article  Google Scholar 

  • Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14:21

    Article  Google Scholar 

  • Farine DR, Aplin LM, Sheldon BC, Hoppitt W (2015) Interspecific social networks promote information transmission in wild songbirds. Proc R Soc B-Biol Sci 282:20142804. doi:10.1098/rspb.2014.2804

    Article  Google Scholar 

  • Francis CD, Barber JR (2013) A framework for understanding noise impacts on wildlife: an urgent conservation priority. Front Ecol Environ 11:305–313. doi:10.1890/120183

    Article  Google Scholar 

  • Fuller RA, Warren PH, Gaston KJ (2007) Daytime noise predicts nocturnal singing in urban robins. Biol Lett 3:368–370. doi:10.1098/rsbl.2007.0134

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124. doi:10.3758/BF03342209

    Article  Google Scholar 

  • Glista DJ, DeVault TL, DeWoody JA (2009) A review of mitigation measures for reducing wildlife mortality on roadways. Landsc Urban Plan 91:1–7. doi:10.1016/j.landurbplan.2008.11.001

    Article  Google Scholar 

  • Greggor AL, Clayton NS, Phalan B, Thornton A (2014) Comparative cognition for conservationists. Trends Ecol Evol 29:489–495. doi:10.1016/j.tree.2014.06.004

    Article  PubMed  PubMed Central  Google Scholar 

  • Grilo C, Bissonette JA, Santos-Reis M (2008) Spatial-temporal patterns in Mediterranean carnivore road casualties: consequences for mitigation. Biol Conserv 142:301–313

    Article  Google Scholar 

  • Grosman PD, Jaeger JAG, Biron PM, Dussault C, Ouellet J (2009) Reducing moose-vehicle collisions through salt pool removal and displacement: an agent-based modeling approach. Ecol Soc 14:17

    Article  Google Scholar 

  • Halfwerk W, Holleman LJM, Lessells CM, Slabbekoorn H (2011) Negative impact of traffic noise on avian reproductive success. J Appl Ecol 48:210–219. doi:10.1111/j.1365-2664.2010.01914.x

    Article  Google Scholar 

  • Hammond LJ (1968) Retardation of fear acquisition by a previously inhibitory CS. J Comp Physiol Psychol 66:756–759. doi:10.1037/h0026546

    Article  CAS  PubMed  Google Scholar 

  • Hare B, Plyusnina I, Ignacio N, Schepina O, Stepika A, Wrangham R, Trut L (2005) Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 15:226–230. doi:10.1016/j.cub.2005.01.040

    Article  CAS  PubMed  Google Scholar 

  • Harrison S, Prodohl PA, Elwood RW (2004) Behavioural trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim Conserv 7:313–320. doi:10.1017/S1367943004001490

    Article  Google Scholar 

  • Hinde RA, Fisher J (1951) Further observations on the opening of milk bottles by birds. Br Birds 44:393–396

    Google Scholar 

  • Holderegger R, Di Giulio M (2010) The genetic effects of roads: a review of empirical evidence. Basic Appl Ecol 11:522–531. doi:10.1016/j.baae.2010.06.006

    Article  Google Scholar 

  • Holling CS (1978) Adaptive Environmental Management and Assessment. Wiley, Chichester

    Google Scholar 

  • Hollis KL, Pharr VL, Dumas MJ, Britton GB, Field J (1997) Classical conditioning provides paternity advantage for territorial male blue gouramis (Trichogaster trichopterus). J Comp Psychol 111:219–225. doi:10.1037/0735-7036.111.3.219

    Article  Google Scholar 

  • Hume DK (1995) Anti-predator training: an experimental approach in reintroduction biology. Dissertation, University of Canterbury

  • Jachowski DS, Slotow R, Millspaugh JJ (2014) Good virtual fences make good neighbors: opportunities for conservation. Anim Conserv 17:187–196. doi:10.1111/acv.12082

    Article  Google Scholar 

  • James MS, Stockwell MP, Clulow J, Clulow S, Mahony MJ (2015) Investigating behaviour for conservation goals: conspecific call playback can be used to alter amphibian distributions within ponds. Biol Conserv 192:287–293. doi:10.1016/j.biocon.2015.10.001

    Article  Google Scholar 

  • Jochimsen DM, Peterson CR, Andrews KM, Gibbons WJ (2004) A literature review of the effects of roads on amphibians and reptiles and the measures used to minimize those effects. Idaho Fish and Game Department and USDA Forest Service report

  • Jones CE, Riha PD, Gore AC, Monfils M (2014) Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats. Anim Cognit 17:827–834. doi:10.1007/s10071-013-0711-2

    Article  Google Scholar 

  • Kight CR, Saha MS, Swaddle JP (2012) Anthropogenic noise is associated with reductions in the productivity of breeding Eastern Bluebirds (Sialia sialis). Ecol Appl 22:1989–1996

    Article  PubMed  Google Scholar 

  • Kilgo JC, Labisky RF, Fritzen DE (1998) Influences of hunting on the behavior of white-tailed deer: implications for conservation of the Florida panther. Conserv Biol 12:1359–1364. doi:10.1046/j.1523-1739.1998.97223.x

    Article  Google Scholar 

  • Kilpatrick HJ, LaBonte AM, Seymour JT (2002) A shotgun-archery deer hunt in a residential community: evaluation of hunt strategies and effectiveness. Wildl Soc Bull 30:478–486

    Google Scholar 

  • Kloppers EL, St. Clair CC, Hurd TE (2005) Predator-resembling aversive conditioning for managing habituated wildlife. Ecol Soc 10:18–31

    Google Scholar 

  • Kociolek AV, Clevenger AP, Clair CCS, Proppe DS (2011) Effects of road networks on bird populations. Conserv Biol 25:241–249. doi:10.1111/j.1523-1739.2010.01635.x

    CAS  PubMed  Google Scholar 

  • Krutzen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB (2005) Cultural transmission of tool use in bottlenose dolphins. Proc Natl Acad Sci 102:8939–8943. doi:10.1073/pnas.0500232102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Laland KN (2004) Social learning strategies. Learn Behav 32:4–14

    Article  PubMed  Google Scholar 

  • Langen TA, Ogden KM, Schwarting LL (2009) predicting hot spots of herpetofauna road mortality along highway networks. J Wildl Manag 73:104–114. doi:10.2193/2008-017

    Article  Google Scholar 

  • Lee C, Prayaga K, Reed M, Henshall J (2007) Methods of training cattle to avoid a location using electrical cues. Appl Anim Behav Sci 108:229–238. doi:10.1016/j.applanim.2006.12.003

    Article  Google Scholar 

  • Lefebvre L (1995) The opening of milk bottles by birds: evidence for accelerating learning rates, but against the wave-of-advance model of cultural transmission. Behav Process 34:43–53. doi:10.1016/0376-6357(94)00051-H

    Article  CAS  Google Scholar 

  • Leigh J, Chamberlain MJ (2008) Effects of aversive conditioning on behavior of nuisance Louisiana black bears. Hum Wildl Confl 2:175–182

    Google Scholar 

  • Magrath RD, Haff TM, McLachlan JR, Igic B (2015) Wild birds learn to eavesdrop on heterospecific alarm calls. Curr Biol 25:2047–2050. doi:10.1016/j.cub.2015.06.028

    Article  CAS  PubMed  Google Scholar 

  • Maier SF, Seligman ME (1976) Learned helplessness: theory and evidence. J Exp Psychol Gen 105:3–46. doi:10.1037/0096-3445.105.1.3

    Article  Google Scholar 

  • Maier SF, Seligman ME, Solomon RL (1969) Pavlovian fear conditioning and learned helplessness effects on escape and avoidance behavior of (a) the CS-US contingency and (b) the independence of the US and voluntary responding. In: Campbell BA, Church RM (eds) Punishment and aversive behavior. Appleton, New York, pp 299–342

    Google Scholar 

  • Maier SF, Tomie A, Jackson RL (1987) Potentiation, overshadowing, and prior exposure to inescapable shock. J Exp Psychol Anim Behav 13:260–270

    Article  Google Scholar 

  • Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931. doi:10.1146/annurev.neuro.24.1.897

    Article  CAS  PubMed  Google Scholar 

  • Marler P (1970) A comparative approach to vocal learning: song development in white-crowned sparrows. J Comp Physiol Psychol 71:1–25. doi:10.1037/h0029144

    Article  Google Scholar 

  • Marler P, Tamura M (1964) Culturally transmitted patterns of vocal behavior in sparrows. Science 146:1483–1486

    Article  CAS  PubMed  Google Scholar 

  • Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:729–749. doi:10.1007/s00359-010-0551-3

    Article  CAS  PubMed  Google Scholar 

  • Mastro LL, Conover MR, Frey SN (2008) Deer-vehicle collision prevention techniques. Hum Wildl Confl 2:80–92

    Google Scholar 

  • Mazur RL (2010) Does aversive conditioning reduce human-black bear conflict? J Wildl Manag 74:48–54. doi:10.2193/2008-163

    Article  Google Scholar 

  • McClure CJW, Ware HE, Carlisle J, Kaltenecker G, Barber JR (2013) An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road. Proc Roy Soc B 280:20132290. doi:10.1098/rspb.2013.2290

    Article  Google Scholar 

  • McGregor P, Horn A, Leonard M, Thomsen F (2013) Anthropogenic noise and conservation. In: Brumm H (ed) Animal communication and noise. Springer, London, pp 409–444. doi:10.1007/978-3-642-41494-7_14

    Chapter  Google Scholar 

  • McLean IG, Duncan C, Jarman PJ, Wynne CDL, Schmitt NT (2000) Learning for life: training marsupials to recognise introduced predators. Behaviour 137:1361–1376. doi:10.1163/156853900501971

    Article  Google Scholar 

  • Meillere A, Brischoux F, Ribout C, Angelier F (2015) Traffic noise exposure affects telomere length in nestling house sparrows. Biol Lett 11:20150559. doi:10.1098/rsbl.2015.0559

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mennitt D, Fristrup KM, Sherrill K, Nelson L (2013) Mapping sound pressure levels on continental scales using a geospatial sound model. Proc Inter-Noise 1–11

  • Michaels CJ, Downie JR, Campbell-Palmer R (2014) The importance of enrichment for advancing amphibian welfare and conservation goals: a review of a neglected topic. Amphib Rept Conserv 8:e77

    Google Scholar 

  • Miller GE, Chen E, Zhou ES (2007) If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol Bull 133:25–45. doi:10.1037/0033-2909.133.1.25

    Article  PubMed  Google Scholar 

  • Munro KG, Bowman J, Fahrig L (2012) Effect of paved road density on abundance of white-tailed deer. Wildl Res 39:478–487. doi:10.1071/WR11152

    Article  Google Scholar 

  • Ng JW, Nielsen C, Clair CCS (2008) Landscape and traffic factors influencing deer-vehicle collisions in an urban environment. Human-Wildl Confl 2:34–47

    Google Scholar 

  • Nijland HA, Van Kempen EEMM, Van Wee GP, Jabben J (2003) Costs and benefits of noise abatement measures. Transp Policy 10:131–140. doi:10.1016/S0967-070X(02)00064-1

    Article  Google Scholar 

  • Nogueira SSC, Abreu SA, Peregrino H, Nogueira-Filho SLG (2014) The effects of feeding unpredictability and classical conditioning on pre-release training of white-lipped peccary (Mammalia, Tayassuidae). PLoS One 9:e86080. doi:10.1371/journal.pone.0086080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Northrup JM, Pitt J, Muhly TB, Stenhouse GB, Musiani M, Boyce MS (2012) Vehicle traffic shapes grizzly bear behaviour on a multiple-use landscape. J Appl Ecol 49:1159–1167. doi:10.1111/j.1365-2664.2012.02180.x

    Article  Google Scholar 

  • Novaro AJ, Funes MC, Walker RS (2005) An empirical test of source-sink dynamics induced by hunting. J Appl Ecol 42:910–920. doi:10.1111/j.1365-2664.2005.01067.x

    Article  Google Scholar 

  • Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Oxford University Press, Milford

    Google Scholar 

  • Pearce JM, Dickinson A (1975) Pavlovian counterconditioning: changing the suppressive properties of shock by association with food. J Exp Psychol Anim Behav 1:170–177

    Article  CAS  PubMed  Google Scholar 

  • Price-Rees SJ, Webb JK, Shine R (2011) School for Skinks: can conditioned taste aversion enable bluetongue lizards (Tiliqua scincoides) to avoid toxic cane toads (Rhinella marina) as prey? Ethology 117:749–757. doi:10.1111/j.1439-0310.2011.01935.x

    Article  Google Scholar 

  • Price-Rees SJ, Webb JK, Shine R (2013) Reducing the impact of a toxic invader by inducing taste aversion in an imperilled native reptile predator. Anim Conserv 16:386–394. doi:10.1111/acv.12004

    Article  Google Scholar 

  • Quinn JL, Whittingham MJ, Butler SJ, Cresswell W (2006) Noise, predation risk compensation and vigilance in the chaffinch fringilla coelebs. J Avian Biol 37:601–608

    Article  Google Scholar 

  • Reijnen R, Foppen R (2006) Impact of road traffic on breeding bird populations. In: Davenport J, Davenport JL (eds) The ecology of transportation: managing mobility for the environment. Springer, Heidelberg, pp 255–274

    Chapter  Google Scholar 

  • Rendell L, Fogarty L, Hoppitt WJE, Morgan TJH, Webster MM, Laland KN (2011) Cognitive culture: theoretical and empirical insights into social learning strategies. Trends Cognit Sci (Regul Ed) 15:68–76. doi:10.1016/j.tics.2010.12.002

    Article  Google Scholar 

  • Rescorla RA (1969) Pavlovian conditioned inhibition. Psychol Bull 72:77–94. doi:10.1037/h0027760

    Article  Google Scholar 

  • Rossler ST, Gehring TM, Schultz RN, Rossler MT, Wydeven AP, Hawley JE (2012) Shock collars as a site-aversive conditioning tool for wolves. Wildl Soc Bull 36:176–184. doi:10.1002/wsb.93

    Article  Google Scholar 

  • Row JR, Blouin-Demers G, Weatherhead PJ (2007) Demographic effects of road mortality in black rat snakes (Elaphe obsolete). Biol Conserv 137:117–124

    Article  Google Scholar 

  • Samia DSM, Nakagawa S, Nomura F, Rangel TF, Blumstein DT (2015) Increased tolerance to humans among disturbed wildlife. Nat Commun 6:8877. doi:10.1038/ncomms9877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schakner ZA, Lunsford C, Straley J, Eguchi T, Mesnick SL (2014) Using models of social transmission to examine the spread of longline depredation behavior among sperm whales in the Gulf of Alaska. PLoS One 9:e109079. doi:10.1371/journal.pone.0109079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schiff R, Smith N, Prochaska J (1972) Extinction of avoidance in rats as a function of duration and number of blocked trials. J Comp Physiol Psychol 81:356–359. doi:10.1037/h0033540

    Article  CAS  PubMed  Google Scholar 

  • Seligman MEP, Maier SF, Solomon RL (1971) Unpredictable and uncontrollable aversive events. In: Brush RF (ed) Aversive conditioning and learning. Academic Press Inc., New York, pp 347–400

    Chapter  Google Scholar 

  • Shepard DB, Kuhns AR, Dreslik MJ, Phillips CA (2008) Roads as barriers to animal movement in fragmented landscapes. Anim Conserv 11:288–296. doi:10.1111/j.1469-1795.2008.00183.x

    Article  Google Scholar 

  • Sherry DF, Galef BG (1984) Cultural transmission without imitation: milk bottle opening by birds. Anim Behav 32:937–938. doi:10.1016/S0003-3472(84)80185-2

    Article  Google Scholar 

  • Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088. doi:10.1016/j.anbehav.2013.02.017

    Article  Google Scholar 

  • Slabbekoorn H, Peet M (2003) Birds sing at a higher pitch in urban noise—Great tits hit the high notes to ensure that their mating calls are heard above the city’s din. Nature 424:267

    Article  CAS  PubMed  Google Scholar 

  • Somaweera R, Webb JK, Brown GP, Shine R (2011) Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads. Behaviour 148:501–517. doi:10.1163/000579511X565763

    Article  Google Scholar 

  • St Clair CC (2003) Comparative permeability of roads, rivers, and meadows to songbirds in Banff National Park. Conserv Biol 17:1151–1160

    Article  Google Scholar 

  • Stamps JA (2001) Habitat selection by dispersers: integrating proximate and ultimate approaches. In: Clobert E, Danchin C, Dhondt A, Nichols A (eds) Dispersal. Oxford University Press, New York, pp 230–242

    Google Scholar 

  • Sturdy CB, Proppe DS (2015) Hearing is believing: birds learn fear. Learn Behav. doi:10.3758/s13420-015-0207-9

    Google Scholar 

  • Sudharsan K, Riley SJ, Winterstein SR (2006) Relationship of autumn hunting season to the frequency of deer-vehicle collisions in Michigan. J Wildl Manag 70:1161–1164. doi:10.2193/0022-541X(2006)70[1161:ROAHST]2.0.CO;2

    Article  Google Scholar 

  • Swaddle JP, Francis CD, Barber JR, Cooper CB, Kyba CCM, Dominoni DM, Shannon G, Aschehoug E, Goodwin SE, Kawahara AY, Luther D, Spoelstra K, Voss M, Longcore T (2015) A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol Evol 30:550–560. doi:10.1016/j.tree.2015.06.009

    Article  PubMed  Google Scholar 

  • Swaisgood RR (2010) The conservation-welfare nexus in reintroduction programmes: a role for sensory ecology. Anim Welf 19:125–137

    CAS  Google Scholar 

  • Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1937. doi:10.1126/science.1108841

    Article  CAS  PubMed  Google Scholar 

  • Urbanek RP, Fondow LEA, Zimorski SE, Wellington MA, Nipper MA (2010) Winter release and management of reintroduced migratory Whooping Cranes Grus americana. Bird Conserv Int 20:43–54. doi:10.1017/S0959270909990153

    Article  Google Scholar 

  • Walters C, Hilborn R (1978) Ecological optimization and adaptive management. Annu Rev Ecol Syst 9:157–188. doi:10.1146/annurev.es.09.110178.001105

    Article  Google Scholar 

  • Ward M, Schlossberg S (2004) Conspecific attraction and the conservation of territorial songbirds. Conserv Biol 18:519–525. doi:10.1111/j.1523-1739.2004.00494.x

    Article  Google Scholar 

  • Ward-Fear G, Pearson DJ, Brown GP, Rangers B, Shine R (2016) Ecological immunization: in situ training of free-ranging predatory lizards reduces their vulnerability to invasive toxic prey. Biol Lett 12:20150863. doi:10.1098/rsbl.2015.0863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ware HE, McClure CJ, Carlisle JD, Barber JR (2015) A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. Proc Natl Acad Sci USA 112:12105–12109. doi:10.1073/pnas.1504710112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webb JK, Brown GP, Child T, Greenlees MJ, Phillips BL, Shine R (2008) A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Austral Ecol 33:821–829. doi:10.1111/j.1442-9993.2008.01847.x

    Article  Google Scholar 

  • Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CE, Wrangham RW, Boesch C (1999) Cultures in chimpanzees. Nature 399:682–685. doi:10.1038/21415

    Article  CAS  PubMed  Google Scholar 

  • Williams SC, DeNicola AJ, Ortega IM (2008) Behavioral responses of white-tailed deer subjected to lethal management. Can J Zool 86:1358–1366. doi:10.1139/Z08-126

    Article  Google Scholar 

  • Woodley SK (2010) Pheromonal communication in amphibians. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:713–727. doi:10.1007/s00359-010-0540-6

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Special thanks to T Bugnyar and D Blumstien for their helpful comments on the manuscript.

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Correspondence to D. S. Proppe.

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This article is part of the Special Issue Animal cognition in a human-dominated world.

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Proppe, D.S., McMillan, N., Congdon, J.V. et al. Mitigating road impacts on animals through learning principles. Anim Cogn 20, 19–31 (2017). https://doi.org/10.1007/s10071-016-0989-y

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  • DOI: https://doi.org/10.1007/s10071-016-0989-y

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