Abstract
Predators attack and plants defend, so herbivores face the dilemma of how to eat enough without being eaten. But do differences in the personality of herbivores affect the foraging choices of individuals? We explored the ecological impact of personality in a generalist herbivore, the brushtail possum (Trichosurus vulpecula). After quantifying personality traits in wild individuals brought temporarily into captivity, we tested how these traits altered foraging by individuals when free-ranging in their natural habitat. To measure their responses to the dual costs of predation risk and plant toxin, we varied the toxin concentration of food in safe foraging patches against paired, non-toxic risky patches, and used a novel synthesis of a manipulative Giving-Up-Density (GUD) experiment and video behavioural analysis. At the population level, the cost of safe patches pivoted around that of risky patches depending on food toxin concentration. At the individual level, boldness affected foraging at risky high-quality food patches (as behavioural differences between bold and shy), and at safe patches only when food toxin concentration was low (as differences in foraging outcome). Our results ecologically validate the personality trait of boldness, in brushtail possums. They also reveal, for the first time, a nuanced link between personality and the way in which individuals balance the costs of food and fear. Importantly, they suggest that high plant defence effectively attenuates differences in foraging behaviour arising from variation in personality, but poorly defended plants in safe areas should be differentially subject to herbivory depending on the personality of the herbivore.
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References
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. doi:10.1890/05-1858
Banks PB, Hughes N, Rose T (2003) Do native Australian small mammals avoid faeces of domestic dogs? Responses of Rattus fuscipes and Antechinus stuartii. Aust Zool 32:406–409
Banks PB, Bytheway JP, Carthey AJR, Hughes NK, Price CJ (2014) Olfaction and predator-prey interactions amongst mammals in Australia. In: Glen AS, Dickman CR (eds) Carnivores of Australia. CSIRO (in press)
Bergvall UA, Schäpers A, Kjellander P, Weiss A (2011) Personality and foraging decisions in fallow deer, Dama dama. Anim Behav 8:101–112. doi:10.1016/j.anbehav.2010.09.018
Biggins JG, Overstreet DH (1978) Aggressive and nonaggressive interactions among captive populations of the brush-tail possum, Trichosurus vulpecula (Marsupialia: Phalangeridae). J Mammal 59:149–159. doi:10.2307/1379884
Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–67
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368. doi:10.1016/j.tree.2008.04.003
Blumstein DT, Daniel JC (2007) Quantifying behaviour the JWatcher way. Sinauer, Sunderland
Boyle R, McLean S (2004) Constraint of feeding by chronic ingestion of 1,8-cineole in the brushtail possum (Trichosurus vulpecula). J Chem Ecol 30:757–775. doi:10.1023/b:joec.0000028430.92739.83
Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47. doi:10.1007/BF00395696
Cole EF, Quinn JL (2012) Personality and problem-solving performance explain competitive ability in the wild. Proc R Soc Lond B 279:1168–1175. doi:10.1098/rspb.2011.1539
Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201. doi:10.1016/j.tree.2007.12.004
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. doi:10.1016/j.anbehav.2012.08.014
David M, Auclair Y, Cézilly F (2011) Personality predicts social dominance in female zebra finches, Taeniopygia guttata, in a feeding context. Anim Behav 81:219–224. doi:10.1016/j.anbehav.2010.10.008
Day TD, O’Connor CE (2000) Behavioural adaptation of brushtail possums (Trichosurus vulpecula) to captivity. Anim Welf 9:413–420
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. doi:10.1890/08-0940.1
Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54. doi:10.1111/1365-2656.12013
Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747. doi:10.1098/rspb.2002.2300
Dingemanse NJ, Dochtermann N, Wright J (2010) A method for exploring the structure of behavioural syndromes to allow formal comparison within and between data sets. Anim Behav 79:439–450. doi:10.1016/j.anbehav.2009.11.024
Dingemanse N, Dochtermann N, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548. doi:10.1007/s00265-012-1416-2
Dochtermann NA, Jenkins SH (2011) Multivariate methods and small sample sizes. Ethology 117:95–101. doi:10.1111/j.1439-0310.2010.01846.x
Dunnet GM (1964) A field study of local populations of the brush-tailed possum Trichosurus vulpecula in eastern Australia. Proc Zool Soc Lond 142:665–695. doi:10.1111/j.1469-7998.1964.tb04634.x
Fedriani JM, Boulay R (2006) Foraging by fearful frugivores: combined effect of fruit ripening and predation risk. Funct Ecol 20:1070–1079. doi:10.1111/j.1365-2435.2006.01199.x
Freeland WJ, Winter JW (1975) Evolutionary consequences of eating: Trichosurus vulpecula (marsupialia) and the genus Eucalyptus. J Chem Ecol 1:439–455. doi:10.1007/BF00988585
Guillette LM, Reddon AR, Hoeschele M, Sturdy CB (2011) Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task. Proc R Soc Lond B 278:767–773. doi:10.1098/rspb.2010.1669
Herborn KA, Macleod R, Miles WTS, Schofield ANB, Alexander L, Arnold KE (2010) Personality in captivity reflects personality in the wild. Anim Behav 79:835–843. doi:10.1016/j.anbehav.2009.12.026
Hernández L, Laundré JW (2009) 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. doi:10.2981/0909-6396(2005)11[215:FITLOF]2.0.CO;2
Hochman V, Kotler BP (2006) Effects of food quality, diet preference and water on patch use by Nubian ibex. Oikos 112:547–554. doi:10.1111/j.0030-1299.2006.14214.x
Kavanagh RP (2003) Conserving owls in Sydney’s urban bushland: current status and requirements. In: Lunney D, Burgin S (eds) Urban wildlife. Royal Zoological Society of New South Wales, Mosman, pp 93–108
Kerle JA, How RA (2008) Common brushtail possum. In: Van Dyck S, Strahan R (eds) The Mammals of Australia. Reed New Holland, Sydney, pp 274–276
Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658. doi:10.1016/j.tree.2013.05.005
Kirmani S, Banks P, McArthur C (2010) Integrating the costs of plant toxins and predation risk in foraging decisions of a mammalian herbivore. Oecologia 164:349–356. doi:10.1007/s00442-010-1717-y
Koolhaas JM et al (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. doi:10.1016/S0149-7634(99)00026-3
Korhonen HT, Jauhiainen L, Rekilä T (2002) Effect of temperament and behavioural reactions to the presence of a human during the pre-mating period on reproductive performance in farmed mink (Mustela vison). Can J Anim Sci 82:275–282. doi:10.4141/A01-088
Kovacs E, Crowther M, Webb J, Dickman C (2012) Population and behavioural responses of native prey to alien predation. Oecologia 168:947–957. doi:10.1007/s00442-011-2168-9
Krause J (1994) The influence of food competition and predation risk on size-assortative shoaling in juvenile chub (Leuciscus cephalus). Ethology 96:105–116. doi:10.1111/j.1439-0310.1994.tb00886.x
Kurvers RHJM, Prins HHT, van Wieren SE, van Oers K, Nolet BA, Ydenberg RC (2010) The effect of personality on social foraging: shy barnacle geese scrounge more. Proc R Soc Lond B 277:601–608. doi:10.1098/rspb.2009.1474
Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool 79:1401–1409. doi:10.1139/z01-094
Lawler IR, Foley WJ, Pass GJ, Eschler BM (1998) Administration of a 5HT3 receptor antagonist increases the intake of diets containing Eucalyptus secondary metabolites by marsupials. J Comp Physiol B 168:611–618. doi:10.1007/s003600050183
Lawler IR, Foley WJ, Eschler BM (2000) Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81:1327–1338. doi:10.2307/177211
Le Mar K, McArthur C (2005a) Comparison of habitat selection by two sympatric macropods, Thylogale billardierii and Macropus rufogriseus rufogriseus, in a patchy eucalypt-forestry environment. Austral Ecol 30:674–683
Le Mar K, McArthur C (2005b) Habitat selection by common brushtail possums in a patchy eucalypt-forestry environment. Aust Mammal 27:119–127. doi:10.1071/AM05119
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi:10.1139/z90-092
Marchetti C, Drent PJ (2000) Individual differences in the use of social information in foraging by captive great tits. Anim Behav 60:131–140. doi:10.1006/anbe.2000.1443
Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86:2946–2954. doi:10.1890/05-0303
Marsh K, Wallis I, Andrew R, Foley W (2006a) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32:1247–1266
Marsh KJ, Wallis IR, McLean S, Sorensen JS, Foley WJ (2006b) Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets. Ecology 87:2103–2112. doi:10.1890/0012-9658(2006)87[2103:CDODPI]2.0.CO;2
Martin JGA, Réale D (2008a) Animal temperament and human disturbance: implications for the response of wildlife to tourism. Behav Process 77:66–72. doi:10.1016/j.beproc.2007.06.004
Martin JGA, Réale D (2008b) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318. doi:10.1016/j.anbehav.2007.05.026
McArthur C, Banks PB, Boonstra R, Forbey J (2014) The dilemma of foraging herbivores: dealing with food and fear. Oecologia. doi:10.1007/s00442-014-3076-6
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
McArthur C, Robbins CT, Hagerman AE, Hanley TA (1993) Diet selection by a ruminant generalist browser in relation to plant chemistry. Can J Zool 71:2236–2243. doi:10.1139/z93-314
McArthur C, Orlando P, Banks PB, Brown JS (2012) The foraging tightrope between predation risk and plant toxins: a matter of concentration. Funct Ecol 26:74–83. doi:10.1111/j.1365-2435.2011.01930.x
Mella VSA, Cooper CE, Davies SJJF (2010) Ventilatory frequency as a measure of the response of tammar wallabies (Macropus eugenii) to the odour of potential predators. Aust J Zool 58:16–23. doi:10.1071/ZO09083
Mella VSA, Cooper CE, Davies SJJF (2014a) Behavioural responses of free-ranging western grey kangaroos (Macropus fuliginosus) to olfactory cues of historical and recently introduced predators. Austral Ecol 39:115–121. doi:10.1111/aec.12050
Mella VSA, Banks PB, McArthur C (2014b) Negotiating multiple cues of predation risk in a landscape of fear: what scares free-ranging brushtail possums? J Zool (Lond) 294:22–30. doi:10.1111/jzo.12146
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. doi:10.1093/beheco/arn126
Minderman J et al (2010) Novel environment exploration and home range size in starlings Sturnus vulgaris. Behav Ecol 21:1321–1329. doi:10.1093/beheco/arq151
Moore BD, Wallis IR, Palá-Paúl J, Brophy JJ, Willis RH, Foley WJ (2004) Antiherbivore chemistry of Eucalyptus–cues and deterrents for marsupial folivores. J Chem Ecol 30:1743–1769. doi:10.1023/B:JOEC.0000042399.06553.c6
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. doi:10.1111/j.1365-2656.2011.01822.x
Nersesian C, Banks P, McArthur C (2012) Behavioural responses to indirect and direct predator cues by a mammalian herbivore, the common brushtail possum. Behav Ecol Sociobiol 66:47–55. doi:10.1007/s00265-011-1250-y
Niemelä PT, Dingemanse NJ (2014) Artificial environments and the study of ‘adaptive’ personalities. Trends Ecol Evol 29:245–247. doi:10.1016/j.tree.2014.02.007
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. doi:10.1111/j.0269-8463.2004.00887.x
Pellegrini AA, Wisenden B, Sorensen P (2010) Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk. Behav Ecol Sociobiol 64:381–387. doi:10.1007/s00265-009-0854-y
Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT (2013) Development of boldness and docility in yellow-bellied marmots. Anim Behav 86:1147–1154. doi:10.1016/j.anbehav.2013.09.016
Petit S, Waudby HP (2012) Standard operating procedures for aluminium box, wire cage, and pitfall trapping, handling, and temporary housing of small wild rodents and marsupials. Aust J Zool 60:392–401. doi:10.1071/ZO12102
Pietrzykowski E, McArthur C, Fitzgerald H, Goodwin AN (2003) Influence of patch characteristics on browsing of tree seedlings by mammalian herbivores. J Appl Ecol 40:458–469. doi:10.1046/j.1365-2664.2003.00809.x
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509. doi:10.1890/04-0719
Provenza FD, Malechek JC (1984) Diet selection by domestic goats in relation to blackbrush twig chemistry. J Appl Ecol 21:831–841. doi:10.2307/2405050
Ratkowsky DA, Evans MA, Alldredge JR (1993) Cross-over experiments. Design, analysis, and application. Marcel Dekker, New York
Réale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597. doi:10.1006/anbe.2000.1530
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev Camb Philos Soc 82:291–318. doi:10.1111/j.1469-185X.2007.00010.x
Rekilä T, Harri M, Ahola L (1997) Validation of the feeding test as an index of fear in farmed blue (Alopex lagopus) and silver foxes (Vulpes vulpes). Physiol Behav 62:805–810. doi:10.1016/S0031-9384(97)00241-2
Schmidt KA (2000) Interaction between food chemistry and predation risk in fox squirrels. Ecology 81:2077–2085. doi:10.2307/177097
Shipley L, Davila T, Thines N, Elias B (2006) Nutritional requirements and diet choices of the pygmy rabbit (Brachylagus idahoensis): a sagebrush specialist. J Chem Ecol 32:2455–2474. doi:10.1007/s10886-006-9156-2
Shipley L, Davis E, Felicetti L, McLean S, Forbey J (2012) Mechanisms for eliminating monoterpenes of sagebrush by specialist and generalist rabbits. J Chem Ecol 38:1178–1189. doi:10.1007/s10886-012-0192-9
Shrader AM, Brown JS, Kerley GIH, Kotler BP (2008) Do free-ranging domestic goats show ‘landscapes of fear’? Patch use in response to habitat features and predator cues. J Arid Environ 72:1811–1819. doi:10.1016/j.jaridenv.2008.05.004
Sih A, Del Giudice M (2012) Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc Lond B 367:2762–2772. doi:10.1098/rstb.2012.0216
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. doi:10.1016/j.tree.2004.04.009
Sinn DL, Cawthen L, Jones SM, Pukk C, Jones ME (2014) Boldness towards novelty and translocation success in captive-raised, orphaned Tasmanian devils. Zoo Biol 33:36–48. doi:10.1002/zoo.21108
Sorensen J, Heward E, Dearing M (2005) Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida). Oecologia 146:415–422. doi:10.1007/s00442-005-0236-8
van der Merwe M, Brown JS (2009) Mapping the landscape of fear of the cape ground squirrel (Xerus inauris). J Mammal 89:1162–1169. doi:10.1644/08-mamm-a-035.1
van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2004) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc Lond B 271:65–73. doi:10.1098/rspb.2003.2518
Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121. doi:10.1006/anbe.1994.1344
Vernes K, Pope LC (2006) Population density of the northern bettong Bettongia tropica in north eastern Queensland. Aust Mammal 28:87–92. doi:10.1071/AM06010
Villalba JJ, Provenza FD (2005) Foraging in chemically diverse enviroments: energy, protein, and alternative foods influence ingestion of plant secondary metabolites by lambs. J Chem Ecol 31:123–138. doi:10.1007/s10886-005-0979-z
Voisinet BD, Grandin T, Tatum JD, O’Connor SF, Struthers JJ (1997) Feedlot cattle with calm temperaments have higher average daily gains than cattle with excitable temperaments. J Anim Sci 75:892–896
Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504. doi:10.1037/0033-2909.83.3.482
Ward AJW, Thomas P, Hart PJB, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568. doi:10.1007/s00265-003-0751-8
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 29:1447–1464. doi:10.1023/A:1024221705354
Wilson ADM, McLaughlin RL (2007) Behavioural syndromes in brook charr, Salvelinus fontinalis: prey-search in the field corresponds with space use in novel laboratory situations. Anim Behav 74:689–698. doi:10.1016/j.anbehav.2007.01.009
Wilson DS, Coleman K, Clarke AB, Biederman L (1993) Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J Comp Psychol 107:250–260. doi:10.1037/0735-7036.107.3.250
Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446. doi:10.1016/0169-5347(94)90134-1
Woinarski JCZ, Milne DJ, Wanganeen G (2001) Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia. Austral Ecol 26:360–370. doi:10.1046/j.1442-9993.2001.01121.x
Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461. doi:10.1016/j.tree.2012.05.001
Wolf M, van Doorn SG, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584. doi:10.1038/nature05835
Acknowledgments
We would like to thank the staff of the Lower Hawkesbury Area, Parks and Wildlife Service, Department of Environment and Heritage. This research was funded by an Australian Research Council grant to C.McA. and P.B.B. (ARC-DP0877585) and conducted with the approval of the University of New South Wales Animal Care and Ethics Committee (ACEC) (#11/89A) and the New South Wales National Parks Wildlife Service (NPWS) Scientific Permit Number SL100443.
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Mella, V.S.A., Ward, A.J.W., Banks, P.B. et al. Personality affects the foraging response of a mammalian herbivore to the dual costs of food and fear. Oecologia 177, 293–303 (2015). https://doi.org/10.1007/s00442-014-3110-8
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DOI: https://doi.org/10.1007/s00442-014-3110-8