Nutritional correlates of koala persistence in a low-density population

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Stalenberg, Eleanor ^a   Wallis, Ian R ^a   Cunningham, Ross B ^b   Allen, Chris ^c   Foley, William J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c NSW National Parks and Wildlife Service   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; PHENOL DERIVATIVE; SIDEROXYLONAL DERIVATIVE; TOXIN; UNCLASSIFIED DRUG;

ANIMAL FOOD; ARTICLE; AUSTRALIA; CONTROLLED STUDY; EUCALYPTUS; FECES ANALYSIS; FOOD PREFERENCE; FORAGING BEHAVIOR; HERBIVORE; KOALA; NEAR INFRARED REFLECTANCE SPECTROSCOPY; NONHUMAN; NUTRIENT AVAILABILITY; NUTRIENT LIMITATION; NUTRITIONAL VALUE; PHENOTYPIC VARIATION; PHYTOCHEMISTRY; PLANT LEAF; POPULATION DENSITY; TAXONOMY; ANIMAL; CHEMISTRY; CLASSIFICATION; ECOSYSTEM; FECES; HERBIVORY; PHYSIOLOGY; THEORETICAL MODEL; TREE;

PHASCOLARCTIDAE;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ECOSYSTEM; EUCALYPTUS; FECES; HERBIVORY; MODELS, THEORETICAL; NEW SOUTH WALES; PHASCOLARCTIDAE; PLANT LEAVES; POPULATION DENSITY; TREES;

EID: 84916208236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113930     Document Type: Article

References (104)

1. Hunter MD, Price PW (1992) Playing chutes and ladders - heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 724-732.
2. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94: 421-425.
3. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54: 165-187.
4. Iason G, Villalba JJ (2006) Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. J Chem Ecol 32: 1115-1132.
5. Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36: 169-189.
6. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68: 1299-1311.
7. Moore BD, Lawler IR, Wallis IR, Beale CM, Foley WJ (2010) Palatability mapping: a koala's eye view of spatial variation in habitat quality. Ecology 91: 3165-3176.
8. 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.
9. Braithwaite LW, Turner J, Kelly J (1984) Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden, NSW 3. Relationships between faunal densities, eucalypt occurrence and foliage nutrients, and soil parent materials. Aust Wildl Res 11: 41-48.
10. Garber PA (1989) Role of spatial memory in primate foraging patterns - Saguinus mystax and Saguinus fuscicollis. Am J Primatol 19: 203-216.
11. Laca EA, Sokolow S, Galli JR, Cangiano CA (2010) Allometry and spatial scales of foraging in mammalian herbivores. Ecol Lett 13: 311-320.
12. Searle KR, Hobbs NT, Gordon IJ (2007) It's the "foodscape", not the landscape: Using foraging behavior to make functional assessments of landscape condition. Isr J Ecol Evol 53: 297-316.
13. Prins H, van Langeveld F (2008) Assembling a diet from different places. In: Prins H, van Langeveld F, editors. Resource ecology: spatial and temporal dynamics of foraging. Dordrecht: Springer. pp. 129-155.
14. Schoener T (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2: 369-404.
15. Stephens D, Krebs J (1986) Foraging theory. Princeton: Princeton University Press.
16. Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Func Ecol 23: 4-16.
17. Simpson SJ, Raubenheimer D (1995) The geometric analysis of feeding and nutrition - a users guide. J Insect Physiol 41: 545-553.
18. Provenza FD (1996) Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J Anim Sci 74: 2010-2020.
19. Marsh KJ, Wallis IR, Foley WJ (2007) Behavioural contributions to the regulated intake of plant secondary metabolites in koalas. Oecologia 154: 283-290.
20. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals - role of plant secondary compounds. Am Nat 108: 269-289.
21. Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, et al. (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68: 98-107.
22. Wallis IR, Edwards MJ, Windley H, Krockenberger AK, Felton A, et al. (2012) Food for folivores: nutritional explanations linking diets to population density. Oecologia 169: 281-291.
23. 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.
24. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, et al. (2009) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20: 685-690.
25. DeGabriel J, Moore B, Foley W, Johnson C (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90: 711-719.
26. Simpson SJ, Raubenheimer D, Charleston MA, Clissold FJ (2010) Modelling nutritional interactions: from individuals to communities. Trends Ecol Evol 25: 53-60.
27. Marsh KJ, Foley WJ, Cowling A, Wallis IR (2003) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 173: 69-78.
28. Foley W, Lawler I, Moore B, Marsh K, Wallis I (2004) Diet selection in marsupial folivores of Eucalyptus: the role of plant secondary metabolites. In: Goldingay R, Jackson S, editors. The Biology of Australian Possums and Gliders. Chipping Norton: Surrey Beatty and Sons. pp. 207-221.
29. Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86: 2946-2954.
30. Wiggins NL, Marsh KJ, Wallis IR, Foley WJ, McArthur C (2006) Sideroxylonal in Eucalyptus foliage influences foraging behaviour of an arboreal folivore. Oecologia 147: 272-279.
31. 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.
32. Moore BD, Foley WJ, Wallis IR, Cowling A, Handasyde KA (2005) Eucalyptus foliar chemistry explains selective feeding by koalas. Biol Lett 1: 64-67.
33. Eschler BM, Pass DM, Willis R, Foley WJ (2000) Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem Syst Ecol 28: 813-824.
34. Moore B, Wallis I, Marsh K, Foley W (2004) The role of nutrition in the conservation of the marsupial folivores of eucalypt forests. In: Lunney D, editor. Conservation of Australia's Forest Fauna. 2 ed. Mosman, NSW: Royal Zoological Society of New South Wales. pp. 549-575.
35. Alm Bergvall U, Leimar O (2005) Plant secondary compounds and the frequency of food types affect food choice by mammalian herbivores. Ecology 86: 2450-2460.
36. Marsh KJ, Wallis IR, Foley WJ (2003) The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula). Aust J Zool 51: 31-42.
37. 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.
38. DeGabriel JL, Moore BD, Ganzhorn JU, Stolter C, Wallis IR, et al. (2014) Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browser. Oikos 123: 298-308.
39. Melzer A, Lamb D (1994) Low density populations of the koala (Phascolarctos cinereus) in central Queensland. Proc R Soc Queensland 104: 89-93.
40. Sullivan BJ, Norris WM, Baxter GS (2003) Low-density koala (Phascolarctos cinereus) populations in the mulgalands of south-west Queensland. II. Distribution and diet. Wildl Res 30: 331-338.
41. Lunney D, Crowther MS, Shannon I, Bryant JV (2009) Combining a map-based public survey with an estimation of site occupancy to determine the recent and changing distribution of the koala in New South Wales. Wildl Res 36: 262-273.
42. Lunney D, Stalenberg E, Santika T, Rhodes JR (2014) Extinction in Eden: identifying the role of climate change in the decline of the koala in south-eastern NSW. Wildl Res 41: 22-34.
43. Masters P, Duka T, Berris S, Moss G (2004) Koalas on Kangaroo Island: from introduction to pest status in less than a century. Wildl Res 31: 267-272.
44. Menkhorst P (2006) Hunted, marooned, re-introduced, contracepted: a history of Koala management in Victoria. In: Lunney D, Munn A, Meikle W, editors. Too Close for Comfort: Contentious Issues in Human- Wildlife Encounters. Mosman: Royal Zoological Society of New South Wales. pp. 73-92.
45. Phillips S (2000) Population trends and the koala conservation debate. Conserv Biol 14: 650-659.
46. Callaghan J, McAlpine C, Thompson J, Mitchell D, Bowen M, et al. (2011) Ranking and mapping koala habitat quality for conservation planning on the basis of indirect evidence of tree-species use: a case study of Noosa Shire, south-eastern Queensland. Wildl Res 38: 89-102.
47. Reed PC, Lunney D (1990) Habitat loss, the key problem for the long-term survival of koalas in New South Wales. In: Lunney D, Urquhart CA, Reed P, editors. Koala Summit: Managing Koalas in New South Wales. Sydney: NSW National Parks and Wildlife Service. pp. 9-31.
48. Foley WJ, McIlwee A, Lawler I, Aragones L, Woolnough AP, et al. (1998) Ecological applications of near infrared reflectance spectroscopy - A tool for rapid, cost-effective prediction of the composition of plant and animal tissues and aspects of animal performance. Oecologia 116: 293-305.
49. Rhodes JR, McAlpine CA, Zuur AF, Smith GM, Ieno EN (2009) GLMM applied on the spatial distribution of koalas in a fragmented landscape. In: Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, editors. Mixed effects models and extensions in ecology with R. New York: Springer pp. 469-492.
50. Rhodes JR, Callaghan JG, McAlpine CA, De Jong C, Bowen ME, et al. (2008) Regional variation in habitat-occupancy thresholds: a warning for conservation planning. J Appl Ecol 45: 549-557.
51. Ellis WAH, Melzer A, Carrick FN, Hasegawa M (2002) Tree use, diet and home range of the koala (Phascolarctos cinereus) at Blair Athol, central Queensland. Wildl Res 29: 303-311.
52. Van Horne B (1983) Density as a misleading indicator of habitat quality. J Wildl Manag 47: 893-901.
53. Gaillard JM, Hebblewhite M, Loison A, Fuller M, Powell R, et al. (2010) Habitat-performance relationships: finding the right metric at a given spatial scale. Philos Trans R Soc B-Biol Sci 365: 2255-2265.
54. Lunney D, Esson C, Moon C, Ellis M, Matthews A (1997) A community-based survey of the koala, Phascolarctos cinereus, in the Eden region of South-eastern New South Wales. Wildl Res 24: 111-128.
55. Lunney D, Leary T (1988) The impact on native mammals of land-use changes and exotic species in the Bega district, New-South-Wales, since settlement. Aust J Ecol 13: 67-92.
56. Phillips SJ, Callaghan J (2011) The Spot Assessment Technique: a tool for determining localised levels of habitat use by Koalas Phascolarctos cinereus. Aust Zool 35: 774-780.
57. Wallis IR, Foley WJ (2005) The rapid determination of sideroxylonals in Eucalyptus foliage by extraction with sonication followed by HPLC. Phytochem Anal 16: 49-54.
58. DeGabriel JL, Moore BD, Marsh KJ, Foley WJ (2010) The effect of plant secondary metabolites on the interplay between the internal and external environments of marsupial folivores. Chemoecology 20: 97-108.
59. Anon (1995) Standard practices for infrared multivariate quantitative analysis (Designation E1655-94). Washington DC: American Society for Testing and Materials.
60. Moore BD, Wallis IR, Pala-Paul J, Brophy JJ, Willis RH, et al. (2004) Antiherbivore chemistry of Eucalyptus - Cues and deterrents for marsupial folivores. J Chem Ecol 30: 1743-1769.
61. Smyth GK, Verbyla AP (1996) A conditional likelihood approach to REML in generalized linear model. J R Stat Soc Series B Stat Methodol 58: 565-572.
62. Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435: 488-490.
63. Foley WJ, Cork SJ (1992) Use of fibrous diets by small herbivores - How far can the rules be bent? Trends Ecol Evol 7: 159-162.
64. Cork SJ, Hume ID, Dawson TJ (1983) Digestion and metabolism of a natural foliar diet (Eucalyptus punctata) by an arboreal marsupial, the koala (Phascolarctos cinereus). J Comp Physiol 153: 181-190.
65. Cork SJ, Sanson GD (1991) Digestion and nutrition in the koala: a review. In: Lee AK, Handasyde, K.A and Sanson, G.D, editor. Biology of the koala. pp. 129-144.
66. Moore B (2004) Chemical determinants of diet and habitat quality in the koala (Phascolactos cinereus) Goldfuss [PhD]. Canberra: Australian National University.
67. 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.
68. Marsh KJ,Wallis IR, Andrew RL, Foley WJ (2006) The detoxification limitation hypothesis: Where did it come from and where is it going? J Chem Ecol 32: 1247-1266.
69. Au J, Wallis IR, Ford KJ, Foley WJ (2013) Whole body protein turnover as an estimate of costs of detoxification of secondary metabolites in a browsing mammal. J Comp Physiol B 183: 993-1003.
70. Searle KR, Stokes CJ, Gordon IJ (2008) When foraging and fear meet: using foraging hierarchies to inform assessments of landscapes of fear. Behav Ecol 19: 475-482.
71. Lunney D, Gresser S, O'Neill LE, Matthews A, Rhodes JR (2007) The impact of fire and dogs on koalas at Port Stephens, New South Wales, using population viability analysis. Pac Conserv Biol 13: 189-201.
72. Wiggins NL, McArthur C, Davies NW (2006) Diet switching in a generalist mammalian folivore: fundamental to maximising intake. Oecologia 147: 650-657.
73. Wiggins NL, McArthur C, Davies NW, McLean S (2006) Spatial scale of the patchiness of plant poisons: A critical influence on foraging efficiency. Ecology 87: 2236-2243.
74. Jones PD, Demarais S, Strickland BK, Edwards SL (2008) Soil region effects on white-tailed deer forage protein content. Southeast Nat 7: 595-606.
75. Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR (2004) Predicting folivorous primate abundance: Validation of a nutritional model. Am J Primatol 62: 55-69.
76. McArt SH, Spalinger DE, Collins WB, Schoen ER, Stevenson T, et al. (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology 90: 1400-1411.
77. Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA (2002) Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. Int J Primatol 23: 283-310.
78. Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests - test of a hypothesis. Oecologia 91: 540-547.
79. Simmen B, Tarnaud L, Hladik A (2012) Leaf nutritional quality as a predictor of primate biomass: further evidence of an ecological anomaly within prosimian communities in Madagascar. J Trop Ecol 28: 141-151.
80. Felton AM, Felton A, Lindenmayer DB, Foley WJ (2009) Nutritional goals of wild primates. Func Ecol 23: 70-78.
81. Krockenberger A (2003) Meeting the energy demands of reproduction in female koalas, Phascolarctos cinereus: evidence for energetic compensation. J Comp Physiol B 173: 531-540.
82. Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc BBiol Sci 363: 375-398.
83. Hengeveld G, van Langeveld F, Groen T, de Knegt H (2009) Optimal foraging for multiple resources in several food species. Am Nat 174: 102-110.
84. Lunney D, O'Neill L, Matthews A, Sherwin WB (2002) Modelling mammalian extinction and forecasting recovery: koalas at Iluka (NSW, Australia). Biol Conserv 106: 101-113.
85. Reed PC, Lunney D, Walker P (1990) A 1986-1987 survey of the koala Phascolarctos cinereus (Goldfuss) in New SouthWales and an ecological interpretation of its distribution. In: Lee AK, Handasyde KA, Sanson GD, editors. Biology of the Koala. Sydney: Surrey Beatty & Sons. pp. 55-74.
86. Lunney D, Matthews A (2002) Ecological changes to forests in the Eden region of New South Wales. In: Dargavel J, Gaughwin D, Libbis B, editors. Australia's Ever-Changing Forests V: Proceedings of the Fifth National Conference on Australian Forest History. Canberra: Centre for Resource and Environmental Studies, Australian National University. pp. 289-310.
87. Lunney D, Moon C (1988) An ecological view of the history of logging and fire in Mumbulla State Forest on the South Coast of New South Wales. In: Frawley KJ, Semple NM, editors. Australia's Ever Changing Forests: Proceedings of the First National Conference on Australian Forest History. Canberra: Department of Geography and Oceanography, Australian Defence Force Academy. pp. 23-61.
88. Putman RJ (1984) Facts from feces. Mamm Rev 14: 79-97.
89. Wilson GJ, Delahay RJ (2001) A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation. Wildl Res 28: 151-164.
90. Ahrestani FS, Heitkonig IMA, Prins HHT (2012) Diet and habitat-niche relationships within an assemblage of large herbivores in a seasonal tropical forest. J Trop Ecol 28: 385-394.
91. Mansson J, Andren H, Sand H (2011) Can pellet counts be used to accurately describe winter habitat selection by moose Alces alces? Eur J Wildl Res 57: 1017-1023.
92. Hegland SJ, Lilleeng MS, Moe SR (2013) Old-growth forest floor richness increases with red deer herbivory intensity. For Ecol Manage 310: 267-274.
93. McGregor DC, Kerr SE, Krockenberger AK (2013) The distribution and abundance of an island population of koalas (Phascolarctos cinereus) in the far north of their geographic range. PLoS One 8: e59713.
94. Sullivan BJ, Baxter GS, Lisle AT (2002) Low-density koala (Phascolarctos cinereus) populations in the mulgalands of south-west Queensland. I. Faecal pellet sampling protocol. Wildl Res 29: 455-462.
95. Ellis WAH, Melzer A, Bercovitch FB (2009) Spatiotemporal dynamics of habitat use by koalas: the checkerboard model. Behav Ecol Sociobiol 63: 1181-1188.
96. Phillips S, Callaghan J (2000) Tree species preferences of koalas (Phascolarctos cinereus) in the Campbelltown area south-west of Sydney, New South Wales. Wildl Res 27: 509-516.
97. Sullivan BJ, Baxter GS, Lisle AT (2003) Low-density koala (Phascolarctos cinereus) populations in the mulgalands of south-west Queensland. III. Broad-scale patterns of habitat use. Wildl Res 30: 583-591.
98. Ellis W, FitzGibbon S, Melzer A, Wilson R, Johnston S, et al. (2013) Koala habitat use and population density: using field data to test the assumptions of ecological models. Aust Mammal 35: 160-165.
99. Crowther MS, Lunney D, Lemon J, Stalenberg E, Wheeler R, et al. (2013) Climate-mediated habitat selection in an arboreal folivore. Ecography 37: 336-343.
100. Briscoe NJ, Handasyde KA, Griffiths SR, Porter WP, Krockenberger A, et al. (2014) Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals. Biol Lett 10: 20140235.
101. Mitchell P (1990) The home ranges and social activity of koalas - a quantitative analysis. In: Lee AK, Handasyde KA, Sanson GD, editors. Biology of the koala. Sydney: Surrey Beatty & Sons. pp. 171-187.
102. Nagy KA, Martin RW (1985) Field metabolic-rate, water flux, food-consumption and time budget of koalas, Phascolarctos cinereus (Marsupialia, Phascolarctidae) in Victoria. Aust J Zool 33: 655-665.
103. Ellis WAH, Sullivan BJ, Lisle AT, Carrick FN (1998) The spatial and temporal distribution of koala faecal pellets. Wildl Res 25: 663-668.
104. Matthews A, Lunney D, Gresser S, Maitz W (2007) Tree use by koalas (Phascolarctos cinereus) after fire in remnant coastal forest. Wildl Res 34: 84-93.