The dilemma of foraging herbivores: dealing with food and fear

Oecologia

Volumn 176, Issue 3, 2014, Pages 677-689

  McArthur, Clare ^a   Banks, Peter B ^a   Boonstra, Rudy ^b   Forbey, Jennifer Sorensen ^c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF TORONTO   (Canada)

^c BOISE STATE UNIVERSITY   (United States)

Author keywords

Detoxification; Personality; Plant toxin; Predation risk; Stress physiology

Indexed keywords

DETOXIFICATION; ECOPHYSIOLOGY; FOOD QUALITY; FORAGING BEHAVIOR; HERBIVORY; MAMMAL; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; PREDATOR-PREY INTERACTION; TOXIN;

ANIMALIA; MAMMALIA;

ANIMAL; BIOLOGICAL MODEL; FEAR; FOOD CHAIN; HERBIVORY; PHYSIOLOGY; VERTEBRATE;

ANIMALS; FEAR; FOOD CHAIN; HERBIVORY; MODELS, BIOLOGICAL; VERTEBRATES;

EID: 84919337529     PISSN: 00298549     EISSN: 14321939     Source Type: Journal    
DOI: 10.1007/s00442-014-3076-6     Document Type: Article

References (113)

1. Andrew RL, Peakall R, Wallis IR, Foley WJ (2007) Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88:716–728
2. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144
3. Au J, Marsh KJ, Wallis IR, Foley WJ (2013) Whole-body protein turnover reveals the cost of detoxification of secondary metabolites in a vertebrate browser. J Comp Physiol B 183:993–1003
4. Bakker ES, Reiffers RC, Olff H, Gleichman JM (2005) Experimental manipulation of predation risk and food quality: effect on grazing behaviour in a central-place foraging herbivore. Oecologia 146:157–167
5. Banks PB (2001) Predation-sensitive grouping and habitat use by eastern grey kangaroos: a field experiment. Anim Behav 61:1013–1021
6. Banks PB, Hume ID, Crowe O (1999) Behavioural, morphological and dietary response of rabbits to predation risk from foxes. Oikos 85:247–256
7. Bedoya-Perez M, Carthey AJR, Mella VSA, McArthur C, Banks PB (2013) A practical guide to avoid giving up on giving-up-densities. Behav Ecol Sociobiol 67:1541–1553
8. Bedoya-Perez M, Issa D, Banks PB, McArthur C (2014) Quantifying the response of free-ranging mammalian herbivores to the interplay between plant defence and nutrient concentrations. Oecologia 175(4):1167–1177
9. Berger-Tal O, Mukherjee S, Kotler BP, Brown JS (2010) Complex state-dependent games between owls and gerbils. Ecol Lett 13:302–310
10. Bergvall UA, Schapers A, Kjellander P, Weiss A (2011) Personality and foraging decisions in fallow deer, Dama dama. Anim Behav 81:101–112
11. Boonstra R (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Funct Ecol 27:11–23
12. Boonstra R, Boutin S, Byrom A, Karels TJ, Hubbs AH, Stuart-Smith K, Blower M, Antpoehler S (2001) The role of red squirrels and arctic ground squirrels. In: Krebs CJ, Boutin S, Boonstra R (eds) Ecosystem dynamics of the boreal forest: the kluane project. Oxford University Press, New York, pp 179–501
13. Boyle R, McLean S, Foley WJ, Davies NW (1999) Comparative metabolism of dietary terpene, p-cymene, in generalist and specialist folivorous marsupials. J Chem Ecol 25:2109–2126
14. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47
15. Brown JS, Kotler B (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014
16. Brown JS, Laundre JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399
17. Bryant JP, Kuropat PJ (1980) Selection of winter forage by sub-arctic browsing vertebrates: the role of plant chemistry. Annu Rev Ecol Evol Syst 11:261–285
18. Bytheway JP, Carthey AJR, Banks PB (2013) Risk vs. reward: how predators and prey respond to aging olfactory cues. Behav Ecol Sociobiol 67:715–725
19. Carthey AJR, Bytheway JP, Banks PB (2011) Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues. J Anim Ecol 80:742–752
20. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201
21. Creel S, Winnie JA, Christianson D (2009) Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proc Natl Acad Sci USA 106:12388–12393
22. Dallman MF, Bhatnagar S (2001) Chronic stress and energy balance: role of the hypothalamo-pituitary-adrenal axis. In: McEwen BS (ed) Coping with the environment: neural and endocrine mechanisms. Oxford University Press, New York, pp 179–210
23. Dammhahn M, Almeling L (2012) Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim Behav 84:1131–1139
24. Dearing MD (1996) Disparate determinants of summer and winter diet selection of a generalist herbivore, Ochotona princeps. Oecologia 108:467–478
25. Dearing MD, Cork S (1999) Role of detoxification of plant secondary compounds on diet breadth in a mammalian herbivore, Trichosurus vulpecula. J Chem Ecol 25:1205–1219
26. DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711–719
27. Degabriele R, Dawson TJ (1979) Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol 134:293–301
28. Embar K, Kotler BP, Mukherjee S (2011) Risk management in optimal foragers: the effect of sightlines and predator type on patch use, time allocation, and vigilance in gerbils. Oikos 120:1657–1666
29. Embar K, Raveh A, Hoffmann I, Kotler BP (2014) Predator facilitation or interference: a game of vipers and owls. Oecologia 174:1301–1309
30. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soule ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–306
31. Fedriani JM, Boulay R (2006) Foraging by fearful frugivores: combined effect of fruit ripening and predation risk. Funct Ecol 20:1070–1079
32. Feng ZL, Liu RS, DeAngelis DL (2008) Plant–herbivore interactions mediated by plant toxicity. Theor Popul Biol 73:449–459
33. Foley WJ (1992) Nitrogen and energy retention and acid-base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals. Zoology 65:403–421
34. Foley WJ, Iason GR, McArthur C (1999) Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Jung H-JG, Fahey GC (eds) Nutritional ecology of herbivores: proceedings of the Vth International Symposium on the Nutrition of Herbivores. American Society of Animal Science, Savoy, pp 130–209
35. Forbey JS, Pu X, Xu D, Kielland K, Bryant JP (2011) Inhibition of snowshoe hare succinate dehydrogenase activity as a mechanism of deterrance for papyriferic acid in birch. J Chem Ecol 37:1285–1293
36. Forbey JS, Dearing MD, Gross E, Orians C, Sotka E, Foley WJ (2013) Vertebrate herbivores in terrestrial and aquatic systems: a pharm-ecological perspective. J Chem Ecol 39:465–480
37. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: role of plant secondary compounds. Am Nat 108:269–289
38. Frye GG, Connelly JW, Musil DD, Forbey JS (2013) Phytochemistry predicts habitat selection by an avian herbivore at multiple spatial scales. Ecology 94:308–314
39. Gagne D, Pons M, Philibert D (1985) RU-38486: a potent antiglucocorticoid in vitro and in vivo. J Steroid Biochem Mol Biol 23:247–251
40. Harris SB, Gunion MW, Rosenthal MJ, Walford RL (1994) Serum glucose, glucose-tolerance, corticosterone and free fatty-acids during aging in energy restricted mice. Mech Ageing Dev 73:209–221
41. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180
42. Hernandez L, Laundre JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildl Biol 11:215–220
43. Hochman V, Kotler BP (2006) Effects of food quality, diet preference and water on patch use by Nubian ibex. Oikos 112:547–554
44. Hughes NK, Kelley JL, Banks PB (2012) Dangerous liaisons: the predation risks of receiving social signals. Ecol Lett 15:1326–1339
45. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago
46. Kirmani SN, Banks PB, McArthur C (2010) Integrating the costs of plant toxins and predation risk in foraging decisions of a mammalian herbivore. Oecologia 164:349–356
47. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321
48. Kotler BP (1997) Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 78:274–282
49. Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A (2010) Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc R Soc B 277:1469–1474
50. Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, Dale MRT, Martin K, Turkington R (1995) Impact of food and predation on the snowshoe hare cycle. Science 269:1112–1115
51. Laundre JW, Hernandez L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool-Rev Can Zool 79:1401–1409
52. Laundre JW, Hernandez L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7
53. Lawler IR, Foley WJ, Pass GJ, Eschler BM (1998) Administration of a 5HT(3) receptor antagonist increases the intake of diets containing Eucalyptus secondary metabolites by marsupials. J Comp Physi B 168:611–618
54. Lawler IR, Foley WJ, Eschler BM (2000) Foliar concentrations of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81:1327–1338
55. Le PP, Friedman JR, Schug J, Brestelli JE, Parker JB, Bochkis IM, Kaestner KH (2005) Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet 1:159–170
56. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
57. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool-Rev Can Zool 68:619–640
58. Loney PE, McArthur C, Sanson GD, Davies NW, Close DC, Jordan GJ (2006) How do soil nutrients affect within-plant patterns of herbivory in seedlings of Eucalyptus nitens? Oecologia 150:409–420
59. Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86:2946–2954
60. Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103–2112
61. Marsh KJ, Moore BD, Wallis IR, Foley WJ (2014) Feeding rates of a mammalian browser confirm the predictions of a ‘foodscape’ model of its habitat. Oecologia 174:873–882
62. McArthur C, Hagerman AE, Robbins CT (1991) Physiological strategies of mammalian herbivores against plant defenses. In: Palo RT, Robbins CT (eds) Plant defenses against mammalian herbivores. CRC, Boca Raton, pp 103–114
63. McArthur C, Loney PE, Davies N, Jordan GJ (2010) Early ontogenetic trajectories vary among defence chemicals in seedlings of a fast-growing eucalypt. Austral Ecol 35:157–166
64. McArthur C, Orlando P, Banks PB, Brown JS (2012) The foraging tight-rope between predation risk and plant toxins: a matter of concentration. Funct Ecol 26:74–83
65. McLean S, Duncan AJ (2006) Pharmacological perspectives on the detoxification of plant secondary metabolites: implications for ingestive behavior of herbivores. J Chem Ecol 32:1213–1228
66. McLean S, Boyle RR, Brandon S, Davies NW, Sorensen JS (2007) Pharmacokinetics of 1,8-cineole, a dietary toxin, in the brushtail possum (Trichosurus vulpecula): significance for feeding. Xenobiotica 37:903–922
67. McNamara JM, Houston AI (1987) Starvation and predation a factors limiting population size. Ecology 68:1515–1519
68. Mella VSA, Banks PB, McArthur C (2014) Negotiating multiple cues of predation risk in a landscape of fear: what scares free-ranging brushtail possums? J Zool. doi:10.1111/jzo.12146
69. Michelena P, Sibbald AM, Erhard HW, McLeod JE (2009) Effects of group size and personality on social foraging: the distribution of sheep across patches. Behav Ecol 20:145–152
70. Montiglio PO, Garant D, Pelletier F, Reale D (2012) Personality differences are related to long-term stress reactivity in a population of wild eastern chipmunks, Tamias striatus. Anim Behav 84:1071–1079
71. Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435:488–490
72. Muller C, Almasi B, Roulin A, Breuner CW, Jenni-Eiermann S, Jenni L (2009) Effects of corticosterone pellets on baseline and stress-induced corticosterone and corticosteroid-binding-globulin. Gen Comp Endocrinol 160:59–66
73. Nersesian CL, Banks PB, McArthur C (2011) Titrating the cost of plant toxins against predators: determining the tipping point for foraging herbivores. J Anim Ecol 80:753–760
74. Nersesian CL, Banks PB, McArthur C (2012a) Influences of plant toxins and their spatial distribution on foraging by the common brushtail possum, a generalist mammalian herbivore. J Chem Ecol 38:1544–1551
75. Nersesian CL, Banks PB, Simpson SJ, McArthur C (2012b) Mixing nutrients mitigates the intake constraints of a plant toxin in a generalist herbivore. Behav Ecol 23:879–888
76. O’Reilly-Wapstra JM, McArthur C, Potts BM (2004) Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species. Funct Ecol 18:677–684
77. Pech RP, Sinclair ARE, Newsome AE, Catling PC (1992) Limits to predator regulation of rabbits in Australia: evidence from predator to removal experiments. Oecologia 89:102–112
78. Powell F, Banks PB (2004) Do house mice modify their foraging behaviour in response to predator odours and habitat? Anim Behav 67:753–759
79. Preisser EL, Bolnick DI, Benard ME (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509
80. Price CJ, Banks PB (2012) Exploiting olfactory learning in alien rats to protect birds’ eggs. Proc Natl Acad Sci USA 109:19304–19309
81. Provenza FD, Ortega-Reyes L, Scott CB, Lynch JJ, Burritt EA (1994) Antiemetic drugs atttenuate food aversions in sheep. J Anim Sci 72:1989–1994
82. Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
83. Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484
84. Salo P, Banks PB, Dickman CR, Korpimaki E (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecol Monogr 80:531–546
85. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89
86. Schmidt KA (2000) Interactions between food chemistry and predation risk in fox squirrels. Ecology 81:2077–2085
87. Seneca N, Zoghbi SS, Shetty HU, Tuan E, Kannan P, Taku A, Innis RB, Pike VW (2010) Effects of ketoconazole on the biodistribution and metabolism of [C-11]loperamide and [C-11]N-desmethyl-loperamide in wild-type and P-gp knockout mice. Nucl Med Biol 37:335–345
88. Sheriff MJ, Krebs CJ, Boonstra R (2011) From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia 166:593–605
89. Shipley LA, Forbey JS, Moore BD (2009) Revisiting the dietary niche: when is a mammalian herbivore a specialist? Integr Comp Biol 49:274–290
90. Shipley LA, Davis EM, Felicetti LA, McLean S, Forbey JS (2012) Mechanisms for eliminating monoterpenes in sagebrush by specialist and generalist rabbits. J Chem Ecol 38:1178–1189
91. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
92. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311
93. Sinclair ARE, Mduma S, Brashares JS (2003) Patterns of predation in a diverse predator-prey system. Nature 425:288–290
94. Sorensen JS, Dearing MD (2006) Efflux transporters as a novel herbivore countermechanism to plant chemical defenses. J Chem Ecol 32:1181–1196
95. Sorensen JS, Turnbull CA, Dearing MD (2004) A specialist herbivore (Neotoma stephensi) absorbs fewer plant toxins than a generalist (Neotoma albigula). Physiol Biochem Zool 77:139–148
96. Sorensen JS, Heward E, Dearing MD (2005a) Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida). Oecologia 146:415–422
97. Sorensen JS, McLister JD, Dearing MD (2005b) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139
98. Sorensen JS, Skopec MM, Dearing MD (2006) Application of pharmacological approaches to plant–mammal interactions. J Chem Ecol 32:1229–1246
99. Torregrossa AM, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56
100. Tremmel M, Muller C (2013) Insect personality depends on environmental conditions. Behav Ecol 24:386–392
101. Ulappa A, Kelsey RG, Frye GG, Rachlow JL, Shipley LA, Bond L, Pu X, Forbey JF (2014) Plant protein and secondary metabolites influence diet selection in a mammalian specialist herbivore. J Mammal 95:834–842
102. van der Merwe M, Brown JS (2008) Mapping the landscape of fear of the Cape ground squirrel (Xerus inauris). J Mammal 89:1162–1169
103. Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464
104. Viblanc VA, Valette V, Kauffmann M, Malosse N, Groscolas R (2012) Coping with social stress: heart rate responses to agonistic interactions in king penguins. Behav Ecol 23:1178–1185
105. Wascher CAF, Scheiber IBR, Braun A, Kotrschal K (2011) Heart rate responses to induced challenge situations in greylag geese (Anser anser). J Comp Psychol 125:116–119
106. Wiggins NL, McArthur C, McLean S, Boyle R (2003) Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. J Chem Ecol 29:1423–1441
107. Wiggins NL, Marsh KJ, Wallis IR, Foley WJ, McArthur C (2006a) Sideroxylonal in Eucalyptus foliage influences foraging behaviour of an arboreal folivore. Oecologia 147:272–279
108. Wiggins NL, McArthur C, Davies NW (2006b) Diet switching in a generalist mammalian folivore: fundamental to maximising intake. Oecologia 147:650–657
109. Wiggins NL, McArthur C, Davies NW, McLean S (2006c) Spatial scale of the patchiness of plant poisons: a critical influence on foraging efficiency. Ecology 87:2236–2243
110. Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446
111. Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS (ed) Handbook of physiology. Section 7. The endocrine system. Volume 4: coping with the environment: neural and endocrine mechanisms. Oxford University Press, New York, pp 211–234
112. Wirsing AJ, Heithaus MR (2014) Accounting for individual behavioural variation in studies of habitat selection. J Anim Ecol 83:319–321
113. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461