Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE (Open Access)

The nutritional quality of post-fire eucalypt regrowth and its consumption by koalas in the New South Wales Southern Tablelands

Murraya R. Lane https://orcid.org/0009-0000-1181-135X A * , Kara N. Youngentob B , Robert G. Clark C and Karen J. Marsh A
+ Author Affiliations
- Author Affiliations

A Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.

B Fenner School of Environment and Society, The Australian National University, Canberra, ACT 2601, Australia.

C Research School of Finance, Actuarial Studies and Statistics, The Australian National University, Canberra, ACT 2601, Australia.

* Correspondence to: murraya.lane@anu.edu.au

Handling Editor: Paul Cooper

Australian Journal of Zoology 71, ZO23024 https://doi.org/10.1071/ZO23024
Submitted: 28 June 2023  Accepted: 5 February 2024  Published: 4 March 2024

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)

Abstract

Most forests and woodlands of south-eastern Australia are fire prone. These landscapes are typically dominated by tree species of the genus Eucalyptus, and many of these are proficient epicormic resprouters after fire. Several marsupial folivores rely on Eucalyptus foliage, including the koala. Little is known about the nutritional composition of epicormic leaves and whether folivores can utilise them. Following the 2019–20 megafires, we offered koalas epicormic leaves from eight eucalypt species that occur in the New South Wales Southern Tablelands and measured concentrations of foliar chemical constituents known to influence koala feeding (total and available nitrogen, formylated phloroglucinol compounds (FPCs), and unsubstituted B-ring flavanones (UBFs)). Captive koalas ate epicormic leaves from the four eucalypt species belonging to the subgenus Symphyomyrtus but ate relatively little from the species of the subgenus Eucalyptus. Available nitrogen was significantly higher in symphyomyrtle epicormic regrowth than in monocalypts and differed between species. Concentrations of FPCs and UBFs also differed between eucalypt species. Our results suggest that post-fire epicormic regrowth from symphyomyrtle species may be more readily browsed than that of monocalypts by koalas in the NSW Southern Tablelands. Therefore, some burnt areas are likely to be better quality habitat for koalas than others.

Keywords: browse quality, bushfire, dry matter intake, epicormic leaves, herbivory, marsupial folivores, nitrogen, plant secondary metabolites.

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(3), 716-728.
| Crossref | Google Scholar | PubMed |

Attiwill PM, Adams MA (2013) Mega-fires, inquiries and politics in the eucalypt forests of Victoria, south-eastern Australia. Forest Ecology and Management 294, 45-53.
| Crossref | Google Scholar |

Au J (2018) Multi-scale effects of nutrition on an arboreal folivore. PhD thesis, Australian National University, Canberra.

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. Journal of Comparative Physiology B 183(7), 993-1003.
| Crossref | Google Scholar |

Au J, Clark RG, Allen C, Marsh KJ, Foley WJ, Youngentob KN (2019) A nutritional mechanism underpinning folivore occurrence in disturbed forests. Forest Ecology and Management 453(8), 117585.
| Crossref | Google Scholar |

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1), 1-48.
| Crossref | Google Scholar |

Beale PK, Foley WJ, Saraf I, Singh IP, Marsh KJ (2022) Common ringtail possums (Pseudocheirus peregrinus) tolerate high concentrations of unsubstituted B-ring flavanones in their diet. Australian Mammalogy 44(3), 347-351.
| Crossref | Google Scholar |

Bowman DM, Murphy BP (2010) Fire and biodiversity. In ‘Conservation biology for all.’ (Eds NS Sodhi, PR Ehrlich) pp. 163–180. (Oxford University Press: New York, NY, USA)

Bradstock RA, Williams RJ, Gill AM (2012) ‘Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world.’ (CSIRO publishing: Melbourne, Victoria, Australia)

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.
| Crossref | Google Scholar | PubMed |

Burrows G (2002) Epicormic strand structure in Angophora, Eucalyptus and Lophostemon (Myrtaceae): implications for fire resistance and recovery. New Phytologist 153(1), 111-131.
| Crossref | Google Scholar |

Burrows GE (2008a) Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire-resistant epicormic structures. Australian Journal of Botany 56(3), 254-264.
| Crossref | Google Scholar |

Burrows N (2008b) Linking fire ecology and fire management in south-west Australian forest landscapes. Forest Ecology and Management 255(7), 2394-2406.
| Crossref | Google Scholar |

Burrows G (2013) Buds, bushfires and resprouting in the eucalypts. Australian Journal of Botany 61(5), 331-349.
| Crossref | Google Scholar |

Burrows N, Stephens C, Wills A, Densmore V (2021) Fire mosaics in south-west Australian forest landscapes. International Journal of Wildland Fire 30(12), 933-945.
| Crossref | Google Scholar |

Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, Enright NJ, Knox KJE (2013) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytologist 197(1), 19-35.
| Crossref | Google Scholar | PubMed |

Cork SJ (1986) Foliage of eucalyptus-punctata and the maintenance nitrogen requirements of koalas, Phascolarctos cinereus. Australian Journal of Zoology 34(1), 17-23.
| Crossref | Google Scholar |

DeGabriel JL, Wallis IR, Moore BD, Foley WJ (2008) A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156(1), 107-116.
| Crossref | Google Scholar | PubMed |

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(3), 711-719.
| Crossref | Google Scholar | PubMed |

Fox J, Weisberg S (2018) ‘An R companion to applied regression.’ 3rd edn. (Sage publications: Thousand Oaks, California, USA)

French WW, Dridi S, Shouse SA, Wu H, Hawley A, Lee S-O, Gu X, Baum JI (2017) A high-protein diet reduces weight gain, decreases food intake, decreases liver fat deposition, and improves markers of muscle metabolism in obese Zucker rats. Nutrients 9(6), 587.
| Crossref | Google Scholar | PubMed |

Gill AM (1994) How fires affect biodiversity. In ‘Fire and biodiversity: the effects and effectiveness of fire management.’ (Dept. of the Environment, Sport and Territories, Biodiversity Unit: Canberra, ACT, Australia)

He T (2014) Ecological divergence and evolutionary transition of resprouting types in Banksia attenuata. Ecology and Evolution 4(16), 3162-3174.
| Crossref | Google Scholar | PubMed |

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(1), 251-258.
| Crossref | Google Scholar | PubMed |

Kuznetsova A, Brockhoff PB, Christensen RH (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82(13), 1-26.
| Crossref | Google Scholar |

Landsberg J (1990) Dieback of rural eucalypts: does insect herbivory relate to dietary quality of tree foliage? Australian Journal of Ecology 15(1), 73-87.
| Crossref | Google Scholar |

Landsberg J, Wylie FR (1983) Water stress, leaf nutrients and defoliation: a model of dieback of rural eucalypts. Australian Journal of Ecology 8(1), 27-41.
| Crossref | Google Scholar |

Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998) Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116(1–2), 160-169.
| Crossref | Google Scholar | PubMed |

Lawler IR, Foley WJ, Eschler BM (2000) Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology 81(5), 1327-1338.
| Crossref | Google Scholar |

Lenth R (2023) emmeans: Estimated Marginal Means, aka Least-Square Means (Version 1.8.5). Available at https://CRAN.R-project.org/package=emmeans [accessed 10 March 2023]

Lucas C, Hennessy K, Mills G, Bathols J (2007) Bushfire Weather in Southeast Australia: Recent Trends and Projected Climate Change Impacts. Report, Melbourne, Victoria, Australia.

Lunney D, Gresser SM, Mahon PS, Matthews A (2004) Post-fire survival and reproduction of rehabilitated and unburnt koalas. Biological Conservation 120(4), 567-575.
| Crossref | Google Scholar |

Marsh KJ, Foley WJ, Cowling A, Wallis IR (2003a) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). Journal of Comparative Physiology B 173(1), 69-78.
| Crossref | Google Scholar | PubMed |

Marsh KJ, Wallis IR, Foley WJ (2003b) The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula). Australian Journal of Zoology 51(1), 31-42.
| Crossref | Google Scholar |

Marsh KJ, Wallis IR, Foley WJ (2005) Detoxification rates constrain feeding in common brushtail possums (Trichosurus vulpecula). Ecology 86(11), 2946-2954.
| Crossref | Google Scholar |

Marsh KJ, Wallis IR, Foley WJ (2007) Behavioural contributions to the regulated intake of plant secondary metabolites in koalas. Oecologia 154(2), 283-290.
| Crossref | Google Scholar | PubMed |

Marsh KJ, Moore BD, Wallis IR, Foley WJ (2014a) Feeding rates of a mammalian browser confirm the predictions of a ‘foodscape’ model of its habitat. Oecologia 174(3), 873-882.
| Crossref | Google Scholar | PubMed |

Marsh KJ, Moore BD, Wallis IR, Foley WJ (2014b) Continuous monitoring of feeding by koalas highlights diurnal differences in tree preferences. Wildlife Research 40(8), 639-646.
| Crossref | Google Scholar |

Marsh KJ, Ward J, Wallis IR, Foley WJ (2018) Intraspecific variation in nutritional composition affects the leaf age preferences of a mammalian herbivore. Journal of Chemical Ecology 44(1), 62-71.
| Crossref | Google Scholar | PubMed |

Marsh KJ, Saraf I, Hocart CH, Youngentob K, Singh I-P, Foley WJ (2019) Occurrence and distribution of unsubstituted B-ring flavanones in Eucalyptus foliage. Phytochemistry 160, 31-39.
| Crossref | Google Scholar | PubMed |

Marsh KJ, Blyton MDJ, Foley WJ, Moore BD (2021) Fundamental dietary specialisation explains differential use of resources within a koala population. Oecologia 196(3), 795-803.
| Crossref | Google Scholar | PubMed |

Martin RW (1981) Age-specific fertility in three populations of the koala, Phascolarctos cinereus Goldfuss, in Victoria. Wildlife Research 8(2), 275-283.
| Crossref | Google Scholar |

Matthews A, Lunney D, Gresser S, Maitz W (2007) Tree use by koalas (Phascolarctos cinereus) after fire in remnant coastal forest. Wildlife Research 34(2), 84-93.
| Crossref | Google Scholar |

Melzer A, Carrick F, Menkhorst P, Lunney D, John BS (2000) Overview, critical assessment, and conservation implications of koala distribution and abundance. Conservation Biology 14(3), 619-628.
| Crossref | Google Scholar |

Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435(7041), 488-490.
| Crossref | Google Scholar | PubMed |

Moore BD, Wallis IR, Marsh KJ, Foley WJ (2004a) The role of nutrition in the conservation of the marsupial folivores of eucalypt forests. In ‘Conservation of Australia’s Forest Fauna.’ (Ed. D Lunney). (Royal Zoological Society of New South Wales: Sydney, New South Wales, Australia)

Moore BD, Wallis IR, Wood JT, Foley WJ (2004b) Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecological Monographs 74(4), 553-568.
| Crossref | Google Scholar |

Moore BD, Wallis IR, Palá-Paúl J, Brophy JJ, Willis RH, Foley WJ (2004c) Antiherbivore chemistry of Eucalyptus-cues and deterrents for marsupial folivores. Journal of Chemical Ecology 30(9), 1743-1769.
| Crossref | Google Scholar | PubMed |

Moore BD, Foley WJ, Wallis IR, Cowling A, Handasyde KA (2005) Eucalyptus foliar chemistry explains selective feeding by koalas. Biology Letters 1(1), 64-67.
| Crossref | Google Scholar | PubMed |

Pausas JG, Keeley JE (2017) Epicormic resprouting in fire-prone ecosystems. Trends in Plant Science 22(12), 1008-1015.
| Crossref | Google Scholar | PubMed |

Pausas JG, Pratt RB, Keeley JE, Jacobsen AL, Ramirez AR, Vilagrosa A, Paula S, Kaneakua-Pia IN, Davis SD (2016) Towards understanding resprouting at the global scale. New Phytologist 209(3), 945-954.
| Crossref | Google Scholar | PubMed |

Penman TD, Kavanagh RP, Binns DL, Melick DR (2007) Patchiness of prescribed burns in dry sclerophyll eucalypt forests in south-eastern Australia. Forest Ecology and Management 252(1–3), 24-32.
| Crossref | Google Scholar |

Phillips S, Callaghan J (2000) Tree species preferences of koalas (Phascolarctos cinereus) in the Campbelltown area south-west of Sydney, New South Wales. Wildlife Research 27(5), 509-516.
| Crossref | Google Scholar |

R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/

Russell-Smith J, Yates CP, Whitehead PJ, Smith R, Craig R, Allan GE, Thackway R, Frakes I, Cridland S, Meyer MCP, Malcolm Gill A (2007) Bushfires ‘down under’: patterns and implications of contemporary Australian landscape burning. International Journal of Wildland Fire 16(4), 361-377.
| Crossref | Google Scholar |

Stalenberg E, Wallis IR, Cunningham RB, Allen C, Foley WJ (2014) Nutritional correlates of koala persistence in a low-density population. PLoS ONE 9(12), e113930.
| Crossref | Google Scholar | PubMed |

State of NSW and Department of Planning Industry and Environment (2020) NSW Fire and the Environment 2019-20 Summary. Report, State of NSW and Department of Planning Industry and Environment, Sydney, New South Wales, Australia.

State of NSW and Office of Environment and Heritage (2018) A review of koala tree use across New South Wales. Report, State of NSW and Office of Environment and Heritage, Sydney, New South Wales, Australia.

Vernes K, Castellano M, Johnson CN (2001) Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial. Journal of Animal Ecology 70(6), 945-954.
| Crossref | Google Scholar |

Wallis IR, Nicolle D, Foley WJ (2010) Available and not total nitrogen in leaves explains key chemical differences between the eucalypt subgenera. Forest Ecology and Management 260(5), 814-821.
| Crossref | Google Scholar |

Wallis IR, Keszei A, Henery ML, Moran GF, Forrester R, Maintz J, Marsh KJ, Andrew RL, Foley WJ (2011) A chemical perspective on the evolution of variation in Eucalyptus globulus. Perspectives in Plant Ecology, Evolution and Systematics 13(4), 305-318.
| Crossref | Google Scholar |

Waters DA, Burrows GE, Harper JDI (2010) Eucalyptus regnans (Myrtaceae): a fire-sensitive eucalypt with a resprouter epicormic structure. American Journal of Botany 97(4), 545-556.
| Crossref | Google Scholar | PubMed |

Wintle BA, Legge S, Woinarski JC (2020) After the megafires: What next for Australian wildlife? Trends in Ecology & Evolution 35(9), 753-757.
| Crossref | Google Scholar | PubMed |