Abstract
The diets of individual animals within populations can differ, but few studies determine whether this is due to fundamental differences in preferences or capacities to eat specific foods, or to external influences such as dominance hierarchies or spatial variation in food availability. The distinction is important because different drivers of dietary specialisation are likely to have different impacts on the way in which animal populations respond to, for example, habitat modification. We used a captive feeding study to investigate the mechanisms driving individual dietary specialisation in a population of wild koalas (Phascolarctos cinereus) in which individuals predominantly ate either Eucalyptus viminalis or Eucalyptus obliqua foliage. All six koalas that primarily ate E. viminalis in the wild avoided eating E. obliqua for more than 1 month in captivity. In contrast, all seven koalas that primarily ate E. obliqua could be maintained exclusively on this species in captivity, although they ate less from individual trees with higher foliar concentrations of unsubstituted B-ring flavanones (UBFs). Our results show that fundamental differences between individual animals allow some to exploit food resources that are less suitable for others. This could reduce competition for food, increase habitat carrying capacity, and is also likely to buffer the population against extinction in the face of habitat modification. The occurrence of fundamental individual specialisation within animal populations could also affect the perceived conservation value of different habitats, translocation or reintroduction success, and population dynamics. It should therefore be further investigated in other mammalian herbivore species.
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References
Araujo MS, Bolnick DI, Layman CA (2011) The ecological causes of individual specialisation. Ecol Lett 14:948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
Au J, Clark RG, Allen C, Marsh KJ, Foley WJ, Youngentob KN (2019) A nutritional mechanism underpinning folivore occurrence in disturbed forests. For Ecol Manag 453:1–8
Baraza E, Villalba JJ, Provenza FD (2005) Nutritional context influences preferences of lambs for foods with plant secondary metabolites. Appl Anim Behav Sci 92:293–305. https://doi.org/10.1016/j.applanim.2004.11.010
Bisanz JE, Spanogiannopoulos P, Pieper LM, Bustion AE, Turnbaugh PJ (2018) How to determine the role of the microbiome in drug disposition. Drug Metab Dispos 46:1588–1595. https://doi.org/10.1124/dmd.118.083402
Blyton MDJ, Soo RM, Whisson DA, Marsh KJ, Pascoe J, Le Pla M, Foley WJ, Hugenholtz P, Moore BD (2019) Faecal inoculations alter the gastrointestinal microbiome and allow dietary expansion in a wild specialist herbivore, the koala. Anim Microbiome. https://doi.org/10.1186/s42523-019-0008-0
Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: Incidence and implications of individual specialization. Am Nat 161:1–28. https://doi.org/10.1086/343878
Brice KL, Trivedi P, Jeffries TC, Blyton MDJ, Mitchell C, Singh BK, Moore BD (2019) The Koala (Phascolarctos cinereus) faecal microbiome differs with diet in a wild population. PeerJ 7:e6534. https://doi.org/10.7717/peerj.6534
Burritt EA, Provenza FD (1996) Amount of experience and prior illness affect the acquisition and persistence of conditioned food aversions in lambs. Appl Anim Behav Sci 48:73–80. https://doi.org/10.1016/0168-1591(95)01004-1
Cork SJ (1986) Foliage of Eucalyptus punctata and the maintenance nitrogen requirements of koalas, Phascolarctos cinereus. Aust J Zool 34:17–23. https://doi.org/10.1071/zo9860017
DeGabriel JL, Wallis IR, Moore BD, Foley WJ (2008) A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156:107–116. https://doi.org/10.1007/s00442-008-0960-y
DeGabriel JL, Moore BD, Shipley LA, Krockenberger AK, Wallis IR, Johnson CN, Foley WJ (2009) Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites. Oecologia 161:539–548. https://doi.org/10.1007/s00442-009-1407-9
Duncan AJ, Frutos P, Young SA (2000) The effect of rumen adaptation to oxalic acid on selection of oxalic-acid-rich plants by goats. Br J Nutr 83:59–65. https://doi.org/10.1017/S000711450000009X
Durell SEA (2000) Individual feeding specialisation in shorebirds: population consequences and conservation implications. Biol Rev 75:503–518
Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155. https://doi.org/10.1046/j.1365-2656.2003.00690.x
Forbey JS, Dearing MD, Gross EM, Orians CM, Sotka EE, Foley WJ (2013) A pharm-ecological perspective of terrestrial and aquatic plant-herbivore interactions. J Chem Ecol 39:465–480. https://doi.org/10.1007/s10886-013-0267-2
Fox GA (2005) Extinction risk of heterogeneous populations. Ecology 86:1191–1198. https://doi.org/10.1890/04-0594
Haage M, Angerbjorn A, Elmhagen B, Maran T (2017) An experimental approach to the formation of diet preferences and individual specialisation in European mink. Eur J Wildlife Res 63:34. https://doi.org/10.1007/s10344-017-1091-8
He Y, Chevillet JR, Liu G, Kim TK, Wang K (2015) The effects of microRNA on the absorption, distribution, metabolism and excretion of drugs. Br J Pharmacol 172:2733–2747. https://doi.org/10.1111/bph.12968
Hindell MA, Lee AK (1987) Habitat use and tree preferences of koalas in a mixed eucalypt forest. Aust Wildl Res 14:349–360. https://doi.org/10.1071/Wr9870349
Jensen LM, Wallis IR, Marsh KJ, Moore BD, Wiggins NL, Foley WJ (2014) Four species of arboreal folivore show differential tolerance to a secondary metabolite. Oecologia 176:251–258. https://doi.org/10.1007/s00442-014-2997-4
Jones RJ, Megarrity RG (1986) Successful transfer of DHP-degrading bacteria from Hawaiian goats to Australian ruminants to overcome the toxicity of Leucaena. Aust Vet J 63:259–262. https://doi.org/10.1111/j.1751-0813.1986.tb02990.x
Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD (2014) Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17:1238–1246. https://doi.org/10.1111/ele.12329
Kongara K (2018) Pharmacogenetics of opioid analgesics in dogs. J Vet Pharma Therap 41:195–204. https://doi.org/10.1111/jvp.12452
Launchbaugh KL, Provenza FD, Werkmeister MJ (1997) Overcoming food neophobia in domestic ruminants through addition of a familiar flavor and repeated exposure to novel foods. Appl Anim Behav Sci 54:327–334. https://doi.org/10.1016/s0168-1591(96)01194-x
Mangione AM, Dearing MD, Karasov WH (2000) Interpopulation differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology 81:2067–2076. https://doi.org/10.1890/0012-9658(2000)081[2067:Idittc]2.0.Co;2
Marsh KJ, Moore BD, Wallis IR, Foley WJ (2013) Continuous monitoring of feeding by koalas highlights diurnal differences in tree preferences. Wildl Res 40:639–646. https://doi.org/10.1071/WR13104
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. https://doi.org/10.1007/s00442-013-2808-3
Marsh KJ, Yin BF, Singh IP, Saraf I, Choudhary A, Au J, Tucker DJ, Foley WJ (2015) From leaf metabolome to in vivo testing: identifying antifeedant compounds for ecological studies of marsupial diets. J Chem Ecol 41:513–519. https://doi.org/10.1007/s10886-015-0589-3
Marsh KJ, Saraf I, Hocart CH, Youngentob KN, Singh IP, Foley WJ (2019) Occurrence and distribution of unsubstituted B-ring flavanones in Eucalyptus foliage. Phytochemistry 160:31–39. https://doi.org/10.1016/j.phytochem.2019.01.005
Martin RW (1985) Overbrowsing, and decline of a population of the koala, Phascolarctos cinereus, in Victoria. 1. Food preference and food tree defoliation. Aust Wildl Res 12:355–365
McEachern MB, Eagles-Smith CA, Efferson CM, Van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes. Oikos 113:440–448
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. https://doi.org/10.1007/s10886-006-9081-4
Melzer A, Carrick F, Menkhorst P, Lunney D, St. John B (2000) Overview, critical assessment, and conservation implications of koala distribution and abundance. Conserv Biol 14:619–628
Mirza SN, Provenza FD (1992) Effects of age and conditions of exposure on maternally mediated food selection by lambs. Appl Anim Behav Sci 33:35–42. https://doi.org/10.1016/S0168-1591(05)80082-6
Moore BD, DeGabriel JL (2012) Integrating the effects of PSMs on vertebrate herbivores across spatial and temporal scales. In: Iason GR, Dicke M, Hartley SE (eds) The Ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 226–246
Moore BD, Foley WJ (2000) A review of feeding and diet selection in koalas (Phascolarctos cinereus). Aust J Zool 48:317–333. https://doi.org/10.1071/Zo99034
Moore BD, Wallis IR, Marsh KJ, Foley WJ (2004a) The role of nutrition in the conservation of the marsupial folivores of eucalypt forests. In: Lunney D (ed) Conservation of Australia’s Forest Fauna, 2nd edn. Royal Zoological Society of New South Wales, Mossman, pp 549–575
Moore BD, Wallis IR, Pala-Paul J, Brophy JJ, Willis RH, Foley WJ (2004b) Antiherbivore chemistry of Eucalyptus: cues and deterrents for marsupial folivores. J Chem Ecol 30:1743–1769. https://doi.org/10.1023/B:Joec.0000042399.06553.C6
Moore BD, Foley WJ, Wallis IR, Cowling A, Handasyde KA (2005) Eucalyptus foliar chemistry explains selective feeding by koalas. Biol Lett 1:64–67. https://doi.org/10.1098/rsbl.2004.0255
Parent CE, Agashe D, Bolnick DI (2014) Intraspecific competition reduces niche width in experimental populations. Ecol Evol 4:3978–3990. https://doi.org/10.1002/ece3.1254
Phillips S (2011) Development of a lightweight, portable trap for capturing free-ranging Koalas Phascolarctos cinereus. Aust Zool 35:747–749
Reese KP, Connelly JW (1997) Translocations of sage grouse Centrocercus urophasianus in North America. Wildl Biol 3:235–241
Saraf I, Marsh KJ, Vir S, Foley WJ, Singh IP (2017) Quantitative analysis of various B-ring unsubstituted and substituted flavonoids in ten Australian species of Eucalyptus. Nat Prod Commun 12:1695–1699
Searle KR, Hunt LP, Gordon IJ (2010) Individualistic herds: individual variation in herbivore foraging behavior and application to rangeland management. Appl Anim Behav Sci 122:1–12. https://doi.org/10.1016/j.applanim.2009.10.005
Sorensen JS, Skopec MM, Dearing MD (2006) Application of pharmacological approaches to plant-mammal interactions. J Chem Ecol 32:1229–1246. https://doi.org/10.1007/s10886-006-9086-z
State of NSW and Office of Environment and Heritage (2018) A review of koala tree use across New South Wales, Sydney, NSW, Australia. State of NSW and Office of Environment and Heritage, Sydney
Svanback R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc Royal Soc B 274:839–844. https://doi.org/10.1098/rspb.2006.0198
Torregrossa AM, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56. https://doi.org/10.1111/j.1365-2435.2008.01523.x
Villalba JJ, Provenza FD (2000) Postingestive feedback from starch influences the ingestive behaviour of sheep consuming wheat straw. Appl Anim Behav Sci 66:49–63. https://doi.org/10.1016/S0168-1591(99)00081-7
Villalba JJ, Provenza FD (2009) Learning and dietary choice in herbivores. Rangel Ecol Manag 62:399–406. https://doi.org/10.2111/08-076.1
Wallis IR, Nicolle D, Foley WJ (2010) Available and not total nitrogen in leaves explains key chemical differences between the eucalypt subgenera. Forest Ecol Manag 260:814–821. https://doi.org/10.1016/j.foreco.2010.05.040
Whisson DA, Carlyon K (2010) Temporal variation in reproductive characteristics of an introduced and abundant island population of koalas. J Mammal 91:1160–1167. https://doi.org/10.1644/09-Mamm-a-384.1
Whisson DA, Dixon V, Taylor ML, Melzer A (2016) Failure to respond to food resource decline has catastrophic consequences for koalas in a high-density population in southern Australia. PLoS ONE. https://doi.org/10.1371/journal.pone.0144348
Wilkinson GR (2005) Drug metabolism and variability among patients in drug response. New Engl J Med 352:2211–2221. https://doi.org/10.1056/Nejmra032424
Youngentob KN, Wallis IR, Lindenmayer DB, Wood JT, Pope ML, Foley WJ (2011) Foliage chemistry influences tree choice and landscape use of a gliding marsupial folivore. J Chem Ecol 37:71–84. https://doi.org/10.1007/s10886-010-9889-9
Acknowledgements
We thank the Conservation Ecology Centre (Cape Otway) for their generous support of the project, and in particular for allowing us to use their facilities for housing koalas. Desley Whisson assisted with catching koalas, Jack Pascoe, Mark Le Pla and various interns at the Conservation Ecology Centre assisted with radio-tracking koalas, and Huiying Wu assisted with the care of captive koalas. The study was approved by the Australian National University Animal Experimentation Ethics Committee (protocol A2017/03), and was supported by a grant from the Australian Research Council to BDM and WJF (Linkage Programme LP140100751).
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All authors conceived and designed the experiments. KJM and MDJB performed the experiments. KJM and BDM analysed the data. KJM wrote the manuscript; other authors provided editorial advice.
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Communicated by Joanna E. Lambert.
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Marsh, K.J., Blyton, M.D.J., Foley, W.J. et al. Fundamental dietary specialisation explains differential use of resources within a koala population. Oecologia 196, 795–803 (2021). https://doi.org/10.1007/s00442-021-04962-3
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DOI: https://doi.org/10.1007/s00442-021-04962-3