Behavioral response of naïve and non-naïve deer to wolf urine
Autoři:
Hermine Annette Lisa van Ginkel aff001; Christian Smit aff001; Dries Pieter Jan Kuijper aff002
Působiště autorů:
Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands
aff001; Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223248
Souhrn
Large carnivores are recolonizing many regions in Europe, where their ungulate prey have lived without them for >150 years. Whether the returning large carnivores will modify ungulate behavior and indirectly affect lower trophic levels, depends on the ability of ungulates to recognize risk based on past encounters and cues indicating carnivore presence. In two case studies, we tested, by means of camera trapping, the behavioral response of deer to wolf urine. The first case study was in the Netherlands where deer (still) live in absence of wolves, and the second in Poland with long-term wolf presence. As controls we used water (no scent) and all-purpose soap (unfamiliar scent). Deer vigilance level on control plots was 20% in both case studies indicating that wolf occupancy per se does not lead to a consistent difference in behavior. Placing wolf urine did not significantly affect deer behavior in either the wolf-absent or the wolf-present area. More intense cues, or a combination of cues, are likely needed to affect deer behavior. Moreover, we found an unexpected reaction of deer towards all-purpose soap of reduced foraging (and tendency for increased vigilance) in the wolf-present area, whereas it did not affect deer behavior in the wolf-absent area. We hypothesize that deer associate all-purpose soap with human presence, causing no response in human-dominated landscapes (the Netherlands), but triggering a behavioral reaction in more remote areas (Poland). This illustrates attention should be paid to controls used in scent experiments as they may be associated differently than intended.
Klíčová slova:
Behavior – Carnivory – Deer – Foraging – Predation – Urine – Wolves – Soaps
Zdroje
1. Reidsma P, Tekelenburg T, van den Berg M, Alkemade R. Impacts of land-use change on biodiversity: an assessment of agricultural biodiversity in the European Union. Agric Ecosyst Environ. 2006;114:86–102.
2. Ceaușu S, Hofmann M, Navarro LM, Carver S, Verburg PH, Pereira HM. Mapping opportunities and challenges for rewilding in Europe. Conserv Biol. 2015;29:1017–1027. doi: 10.1111/cobi.12533 25997361
3. Trouwborst A. Global large carnivore conservation and international law. Biodivers Conserv. 2015;24:1567–1588.
4. Chapron G, Kaczensky P, Linnell JDC, von Arx M, Huber D, Andrén H, et al. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science. 2014;346:1517–1519. doi: 10.1126/science.1257553 25525247
5. Latombe G, Fortin D, Parrott L. Spatio-temporal dynamics in the response of woodland caribou and moose to the passage of grey wolf. J Anim Ecol. 2014;83:185–198. doi: 10.1111/1365-2656.12108 23859231
6. Creel S, Winnie, A. J, Christianson D, Liley S. Time and space in general models of antipredator response: tests with wolves and elk. Anim Behav. 2008;76:1139–1146.
7. Kuijper DPJ, de Kleine C, Churski M, Van Hooft P, Bubnicki JW, Jędrzejewska B. Landscape of fear in Europe: Wolves affect spatial patterns of ungulate browsing in Białowieża Primeval Forest, Poland. Ecography. 2013;36:1263–1275.
8. Altendorf KB, Laundré JW, González CAL, Brown JS. Assessing effects of predation risk on foraging behavior of mule deer. J Mammal. 2001;82:430–439.
9. Lima SL, Dill LM. Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool. 1990;68:619–640.
10. Lima SL. Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav. 1995;49:11–20.
11. Creel S, Christianson D, Liley S, Winnie J. Predation risk affects reproductive physiology and demography of Elk. Science. 2007;315:960. doi: 10.1126/science.1135918 17303746
12. Ford AT, Goheen JR, Otieno TO, Bidner L, Isbell LA, Palmer TM, et al. Large carnivores make savanna tree communities less thorny. Science. 2014;346:346–349. doi: 10.1126/science.1252753 25324387
13. Kuijper DPJ, Bubnicki JW, Churski M, Mols B, Van Hooft P. Context dependence of risk effects: Wolves and tree logs create patches of fear in an old-growth forest. Behav Ecol. 2015;26:1558–1568.
14. Ripple WJ, Beschta RL. Linking wolves to willows via risk-sensitive foraging by ungulates in the northern Yellowstone ecosystem. For Ecol Manage. 2006;230:96–106.
15. Charnov EL. Optimal foraging, the marginal value theorem. Theor Popul Biol. 1976;9:129–136. doi: 10.1016/0040-5809(76)90040-x 1273796
16. Lima SL, Bednekoff PA. Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat. 1999;153:649–659. doi: 10.1086/303202 29585647
17. Brown JS, Laundré JW, Gurung M. The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal. 1999;80:385–399.
18. Kuijper DPJ, Verwijmeren M, Churski M, Zbyryt A, Schmidt K, Jędrzejewska B, et al. What cues do ungulates use to assess predation risk in dense temperate forests? PLoS One. 2014;9:e84607. doi: 10.1371/journal.pone.0084607 24404177
19. Wikenros C, Kuijper DPJ, Behnke R, Schmidt K. Behavioural responses of ungulates to indirect cues of an ambush predator. Behaviour. 2015;152:1019–1040.
20. Shrader AM, Brown JS, Kerley GIH, Kotler BP. Do free-ranging domestic goats show ‘landscapes of fear’? Patch use in response to habitat features and predator cues. J Arid Environ. 2008;72:1811–1819.
21. Winnie J, Creel S. Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav. 2007;73:215–225.
22. Creel S, Winnie J, Maxwell B, Hamlin K, Creel M. Elk alter habitat selection as an antipredator response to wolves. Ecology. 2005;86:3387–3397.
23. Barnier F, Valeix M, Duncan P, Chamaillé-Jammes S, Barre P, Loveridge AJ, et al. Diet quality in a wild grazer declines under the threat of an ambush predator. Proc R Soc B. 2014;281:20140446. doi: 10.1098/rspb.2014.0446 24789903
24. Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS. Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology. 2005;86:1320–1330.
25. Sand H, Wikenros C, Wabakken P, Liberg O. Cross-continental differences in patterns of predation: will naive moose in Scandinavia ever learn? Proc R Soc B. 2006;273:1421–1427. doi: 10.1098/rspb.2005.3447 16777732
26. Berger J, Swenson JE, Persson I-L. Recolonizing carnivores and naïve prey: conservation lessons from Pleistocene extinctions. Science. 2001;291:1036–1039. doi: 10.1126/science.1056466 11161215
27. Nicholson KL, Milleret C, Månsson J, Sand H. Testing the risk of predation hypothesis: The influence of recolonizing wolves on habitat use by moose. Oecologia. 2014;176:69–80. doi: 10.1007/s00442-014-3004-9 25015119
28. Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, et al. Relaxed selection in the wild. Trends Ecol Evol. 2009;24:487–496. doi: 10.1016/j.tree.2009.03.010 19500875
29. Mery F, Burns JG. Behavioural plasticity: an interaction between evolution and experience. Evol Ecol. 2010;24:571–583.
30. Laundré JW, Hernández L, Altendorf KB. Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, U.S.A. Can J Zool. 2001;79:1401–1409.
31. Frank ASK, Carthey AJR, Banks PB. Does historical coexistence with dingoes explain current avoidance of domestic dogs? Island bandicoots are naïve to dogs, unlike their mainland counterparts. PLoS One. 2016;11:e0161447. doi: 10.1371/journal.pone.0161447 27603517
32. Carthey AJR, Blumstein DT. Predicting predator recognition in a changing world. Trends Ecol Evol. 2017;33:106–115. doi: 10.1016/j.tree.2017.10.009 29132776
33. Blumstein DT. The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology. 2006;112:209–217.
34. Elmeros M, Winbladh JK, Andersen PN, Madsen AB, Christensen JT. Effectiveness of odour repellents on red deer (Cervus elaphus) and roe deer (Capreolus capreolus): a field test. Eur J Wildl Res. 2011;57:1223–1226.
35. Swihart RK, Pignatello JJ, Mattina MJI. Aversive responses of white-tailed deer, Odocoileus virginianus, to predator urines. J Chem Ecol. 1991;17:767–777. doi: 10.1007/BF00994199 24258921
36. Christensen JW, Rundgren M. Predator odour per se does not frighten domestic horses. Appl Anim Behav Sci. 2008;112:136–145.
37. Kluever BM, Howery LD, Breck SW, Bergman DL. Predator and heterospecific stimuli alter behaviour in cattle. Behav Processes. 2009;81:85–91. doi: 10.1016/j.beproc.2009.02.004 19429201
38. Li C, Yang X, Ding Y, Zhang L, Fang H, Tang S, et al. Do Père David’s deer lose memories of their ancestral predators? PLoS One. 2011;6:e23623. doi: 10.1371/journal.pone.0023623 21887286
39. Chamaillé-Jammes S, Malcuit H, Le Saout S, Martin J-L. Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence. Oecologia. 2014;174:1151–1158. doi: 10.1007/s00442-013-2843-0 24288079
40. Dalerum F, Belton L. African ungulates recognize a locally extinct native predator. Behav Ecol. 2015;26:215–222.
41. Sahlén E, Noell S, DePerno CS, Kindberg J, Spong G, Cromsigt JPGM. Phantoms of the forest: legacy risk effects of a regionally extinct large carnivore. Ecol Evol. 2016;6:791–799. doi: 10.1002/ece3.1866 26865966
42. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, et al. Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos. 2010;119:610–621.
43. Jędrzejewska B, Jędrzejewski W, Bunevich AN, Miłkowski L, Okarma H. Population dynamics of wolves Canis lupus in Białowieża primeval forest (Poland and Belarus) in relation to hunting by humans, 1847–1993. Mamm Rev. 1996;26:103–126.
44. Jędrzejewska B, Jędrzejewski W, Bunevich AN, Milkowski L, Krasinski ZA. Factors shaping population densities and increase rates of ungulates in Bialowieza Primeval Forest (Poland and Belarus) in the 19th and 20th centuries. Acta Theriol. 1997;42:399–451.
45. Schmidt K, Jȩdrzejewski W, Okarma H, Kowalczyk R. Spatial interactions between grey wolves and Eurasian lynx in Białowieża Primeval Forest, Poland. Ecol Res. 2009;24:207–214.
46. Okarma H. The trophic ecology of wolves and their predatory role in ungulate communities of forest ecosystems in Europe. Acta Theriol. 1995;40:335–386.
47. Okarma H, Jędrzejewska B, Jędrzejewski W, Krasiński ZA, Miłkowski L. The roles of predation, snow cover, acorn crop, and man-related factors on ungulate mortality in Białowieża Primeval Forest, Poland. Acta Theriol. 1995;40:197–217.
48. Kuijper DPJ, Cromsigt JPGM, Churski M, Adam B, Jędrzejewska B, Jędrzejewski W. Do ungulates preferentially feed in forest gaps in European temperate forest? For Ecol Manage. 2009;258:1528–1535.
49. Banks PB, Daly A, Bytheway JP. Predator odours attract other predators, creating an olfactory web of information. Biol Lett. 2016;12:20151053. doi: 10.1098/rsbl.2015.1053 27194283
50. Kay M, Wobbrock JO. ARTool: Aligned rank transform for nonparametric factorial ANOVAs. 2019.
51. Blanchard P, Fritz H. Induced or routine vigilance while foraging. Oikos. 2007;116:1603–1608.
52. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev. 2005;29:1123–1144. doi: 10.1016/j.neubiorev.2005.05.005 16085312
53. Verdolin JL. Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol. 2006;60:457–464.
54. Carthey AJR, Banks PB. Naïveté in novel ecological interactions: Lessons from theory and experimental evidence. Biol Rev. 2014;89:932–949. doi: 10.1111/brv.12087 25319946
55. Banks PB, Dickman CR. Alien predation and the effects of multiple levels of prey naivete. Trends Ecol Evol. 2007;22:229–230. doi: 10.1016/j.tree.2007.02.006 17300855
56. Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, et al. Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci. 2011;108:11235–11240. doi: 10.1073/pnas.1103317108 21690383
57. Arnould C, Malosse C, Signoret J-P, Descoins C. Which chemical constituents from dog feces are involved in its food repellent effect in sheep? J Chem Ecol. 1998;24:559–576.
58. Carthey AJR, Bucknall MP, Wierucka K, Banks PB. Novel predators emit novel cues: A mechanism for prey naivety towards alien predators. Sci Rep. 2017;7:1–9. doi: 10.1038/s41598-016-0028-x
59. Carthey AJR, Banks PB. Naiveté is not forever: responses of a vulnerable native rodent to its long term alien predators. Oikos. 2016;125:918–926.
60. Parsons AW, Bland C, Forrester T, Baker-Whatton MC, Schuttler SG, McShea WJ, et al. The ecological impact of humans and dogs on wildlife in protected areas in eastern North America. Biol Conserv. 2016;203:75–88.
61. Jȩdrzejewski W, Schmidt K, Theuerkauf J, Jȩdrzejewska B, Selva N, Zub K, et al. Kill rates and predation by wolves on ungulate populations in Białowieża Primeval Forest (Poland). Ecology. 2002;83:1341–56.
62. Parsons MH, Blumstein DT. Familiarity breeds contempt: kangaroos persistently avoid areas with experimentally deployed dingo scents. PLoS One. 2010;5:e10403. doi: 10.1371/journal.pone.0010403 20463952
63. Eccard JA, Meißner JK, Heurich M. European roe deer increase vigilance when faced with immediate predation risk by Eurasian lynx. Ethology. 2015;121:1–11.
64. Rouco C, Villafuerte R, Castro F, Ferreras P. Responses of naive and experienced European rabbits to predator odour. Eur J Wildl Res. 2011;57:395–398.
65. Peters RP, Mech LD. Scent-marking in wolves: radio-tracking of wolf packs has provided definite evidence that olfactory sign is used for territory maintenance and may serve for other forms of communication within the pack as well. Am Sci. 1975;63:628–637. 1200478
66. Sullivan TP, Nordstrom LO, Sullivan DS. Use of predator odors as repellents to reduce feeding damage by herbivores II. Black-tailed deer (Odocoileus hemionus columbianus). J Chem Ecol. 1985;11:921–935. doi: 10.1007/BF01012078 24310276
67. Osada K, Miyazono S, Kashiwayanagi M. Pyrazine analogs are active components of wolf urine that induce avoidance and fear-related behaviors in deer. Front Behav Neurosci. 2014;8:276. doi: 10.3389/fnbeh.2014.00276 25177281
68. Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY. Fear of large carnivores causes a trophic cascade. Nat Commun. 2016;7:10698. doi: 10.1038/ncomms10698 26906881
69. Liley S, Creel S. What best explains vigilance in elk: characteristics of prey, predators, or the environment? Behav Ecol. 2008;19:245–54.
70. Zub K, Theuerkauf J, Jędrzejewski W, Jędrzejewska B, Schmidt K, Kowalczyk R. Wolf pack territory marking in the Białowieża Primeval Forest (Poland). Behaviour. 2003;140:635–48.
71. Mella VSA, Banks PB, McArthur C. Negotiating multiple cues of predation risk in a landscape of fear: what scares free-ranging brushtail possums? J Zool. 2014;294:22–30.
72. Zöttl M, Lienert R, Clutton-Brock T, Millesi E, Manser MB. The effects of recruitment to direct predator cues on predator responses in meerkats. Behav Ecol. 2013;24:198–204.
73. Jayakody S, Sibbald AM, Gordon IJ, Lambin X. Red deer Cervus elephus vigilance behaviour differs with habitat and type of human disturbance. Wildlife Biol. 2008;14:81–91.
74. Clair CCS, Forrest A. Impacts of vehicle traffic on the distribution and behaviour of rutting elk, Cervus elaphus. Behaviour. 2009;146:393–413.
75. Sibbald AM, Hooper RJ, McLeod JE, Gordon IJ. Responses of red deer (Cervus elaphus) to regular disturbance by hill walkers. Eur J Wildl Res. 2011;57:817–825.
76. Le Saout S, Padié S, Chamaillé-Jammes S, Chollet S, Côté S, Morellet N, et al. Short-term effects of hunting on naive black-tailed deer (Odocoileus hemionus sitkensis): behavioural response and consequences on vegetation growth. Can J Zool. 2014;92:915–925.
77. Ciuti S, Northrup JM, Muhly TB, Simi S, Musiani M, Pitt JA, et al. Effects of humans on behaviour of wildlife exceed those of natural predators in a landscape of fear. PLoS One. 2012;7:e50611. doi: 10.1371/journal.pone.0050611 23226330
78. Worm B. A most unusual (super)predator. Science. 2015;349:784–785. doi: 10.1126/science.aac8697 26293936
79. Clinchy M, Zanette LY, Roberts D, Suraci JP, Buesching CD, Newman C, et al. Fear of the human “super predator” far exceeds the fear of large carnivores in a model mesocarnivore. Behav Ecol. 2016 Jul 19;27:1826–1832.
80. Smith JA, Suraci JP, Clinchy M, Crawford A, Roberts D, Zanette LY, et al. Fear of the human ‘super predator’ reduces feeding time in large carnivores. Proc R Soc B. 2017;284:20170433. doi: 10.1098/rspb.2017.0433 28637855
81. Gervasi V, Sand H, Zimmermann B, Mattisson J, Linnell JDC. Decomposing risk: landscape structure and wolf behavior generate different predation patterns in two sympatric ungulates. Ecol Appl. 2013;23:1722–1734. doi: 10.1890/12-1615.1 24261051
82. Darimont CT, Fox CH, Bryan HM, Reimchen TE. The unique ecology of human predators. Science. 2015;349:858–860. doi: 10.1126/science.aac4249 26293961
83. Karl T, Striednig M, Graus M, Hammerle A, Wohlfahrt G. Urban flux measurements reveal a large pool of oxygenated volatile organic compound emissions. Proc Natl Acad Sci. 2018;115:1186–1191. doi: 10.1073/pnas.1714715115 29358383
84. Lowry H, Lill A, Wong BBM. Behavioural responses of wildlife to urban environments. Biol Rev. 2013;88:537–549. doi: 10.1111/brv.12012 23279382
85. Stillfried M, Gras P, Börner K, Göritz F, Painer J, Röllig K, et al. Secrets of success in a landscape of fear: urban wild boar adjust risk perception and tolerate disturbance. Front Ecol Evol. 2017;5:157.
86. Cromsigt JPGM Kuijper DPJ, Adam M Beschta RL, Churski M, Eycott A, et al. Hunting for fear: innovating management of human-wildlife conflicts. J Appl Ecol. 2013;50:544–549.
87. Lone K, Loe LE, Gobakken T, Linnell JDC, Odden J, Remmen J, et al. Living and dying in a multi-predator landscape of fear: roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans. Oikos. 2014;123:641–651.
88. Kuijper DPJ, Sahlén E, Elmhagen B, Chamaillé-Jammes S, Sand H, Lone K, et al. Paws without claws? Ecological effects of large carnivores in anthropogenic landscapes. Proc R Soc B. 2016;283:20161625. doi: 10.1098/rspb.2016.1625 27798302
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