Common ringtail possums (Pseudocheirus peregrinus) tolerate high concentrations of unsubstituted B-ring flavanones in their diet
Phillipa K. Beale A , William J. Foley A , Isha Saraf B , Inder Pal Singh B and Karen J. Marsh
A *
+ Author Affiliations
- Author Affiliations
A Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
B Department of Natural Products, National Institute of Pharmaceutical Education and Research, SAS Nagar, 160062 Punjab, India.
Australian Mammalogy 44(3) 347-351 https://doi.org/10.1071/AM21027
Submitted: 27 July 2021 Accepted: 25 December 2021 Published: 10 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Mammal Society.
Abstract
Plant secondary metabolites (PSMs) can influence the consumption of particular plants by herbivores. Unsubstituted B-ring flavanones (UBFs), which are compounds found in the leaves of Eucalyptus species from the Eucalyptus subgenus (common name monocalypt), deter feeding by common brushtail possums (Trichosurus vulpecula) when added to artificial diets at concentrations that reflect those found naturally in foliage. We hypothesised that common ringtail possums (Pseudocheirus peregrinus) would tolerate higher UBF concentrations, because, unlike brushtail possums, they regularly eat monocalypt foliage. This proved to be the case; ringtail possums were not deterred by two different UBFs, pinocembrin and flavanone, at concentrations up to 4.7% dry matter, which is substantially higher than the concentrations that deter brushtail possums. These results extend and refine our understanding of how variation in tolerance or susceptibility to eucalypt PSMs affects the diets of sympatric marsupial folivores, potentially reducing competition for food.
Keywords: common ringtail possum (Pseudocheirus peregrinus), dietary niche, eucalypt, folivore, herbivory, monocalypt, plant secondary metabolites, unsubstituted B-ring flavanones (UBFs).
References
Au, J., Clark, R. G., Allen, C., Marsh, K. J., Foley, W. J., and Youngentob, K. N. (2019). A nutritional mechanism underpinning folivore occurrence in disturbed forests. Forest Ecology and Management 453, 117585.| A nutritional mechanism underpinning folivore occurrence in disturbed forests.Crossref | GoogleScholarGoogle Scholar |
Austin, M. P., Cunningham, R. B., and Wood, J. T. (1983). The subgeneric composition of eucalypt forest stands in a region of south-eastern Australia. Australian Journal of Botany 31, 63–71.
| The subgeneric composition of eucalypt forest stands in a region of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Eschler, B. M., Pass, D. M., Willis, R., and Foley, W. J. (2000). Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochemical Systematics and Ecology 28, 813–824.
| Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species.Crossref | GoogleScholarGoogle Scholar | 10913843PubMed |
Goodger, J. Q. D., Senaratne, S. L., Nicolle, D., and Woodrow, I. E. (2016). Foliar essential oil glands of Eucalyptus subgenus Eucalyptus (Myrtaceae) are a rich source of flavonoids and related non-volatile constituents. PLoS One 11, e0151432.
| Foliar essential oil glands of Eucalyptus subgenus Eucalyptus (Myrtaceae) are a rich source of flavonoids and related non-volatile constituents.Crossref | GoogleScholarGoogle Scholar |
Hoffman, R. (1989). Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443–457.
| Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system.Crossref | GoogleScholarGoogle Scholar |
Iason, G. R., and Palo, R. T. (1991). Effects of birch phenolics on a grazing and a browsing mammal – a comparison of hares. Journal of Chemical Ecology 17, 1733–1743.
| Effects of birch phenolics on a grazing and a browsing mammal – a comparison of hares.Crossref | GoogleScholarGoogle Scholar | 24257917PubMed |
Jensen, L. M., Wallis, I. R., Marsh, K. J., Moore, B. D., Wiggins, N. L., and Foley, W. J. (2014). Four species of arboreal folivore show differential tolerance to a secondary metabolite. Oecologia 176, 251–258.
| Four species of arboreal folivore show differential tolerance to a secondary metabolite.Crossref | GoogleScholarGoogle Scholar | 24974269PubMed |
Jensen, L. M., Wallis, I. R., and Foley, W. J. (2015). Relative concentrations of nutrients and toxins dictate feeding by a vertebrate browser, the greater glider Petauroides volans. PLoS One 10, e0121584.
| Relative concentrations of nutrients and toxins dictate feeding by a vertebrate browser, the greater glider Petauroides volans.Crossref | GoogleScholarGoogle Scholar | 25938422PubMed |
Lawler, I. R., Foley, W. J., Eschler, B. M., Pass, D. M., and Handasyde, K. (1998). Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116, 160–169.
| Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials.Crossref | GoogleScholarGoogle Scholar | 28308521PubMed |
Marsh, K. J., Foley, W. J., Cowling, A., and Wallis, I. R. (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, 69–78.
| Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar |
Marsh, K. J., Wallis, I. R., and Foley, W. J. (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, 31–42.
| The effect of inactivating tannins on the intake of Eucalyptus foliage by a specialist Eucalyptus folivore (Pseudocheirus peregrinus) and a generalist herbivore (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar |
Marsh, K. J., Yin, B. F., Singh, I. P., Saraf, I., Choudhary, A., Au, J., Tucker, D. J., and Foley, W. J. (2015). From leaf metabolome to in vivo testing: Identifying antifeedant compounds for ecological studies of marsupial diets. Journal of Chemical Ecology 41, 513–519.
| From leaf metabolome to in vivo testing: Identifying antifeedant compounds for ecological studies of marsupial diets.Crossref | GoogleScholarGoogle Scholar | 25994224PubMed |
Marsh, K. J., Kulheim, C., Blomberg, S. P., Thornhill, A. H., Miller, J. T., Wallis, I. R., Nicolle, D., Salminen, J. P., and Foley, W. J. (2017). Genus-wide variation in foliar polyphenolics in eucalypts. Phytochemistry 144, 197–207.
| Genus-wide variation in foliar polyphenolics in eucalypts.Crossref | GoogleScholarGoogle Scholar | 28957714PubMed |
Marsh, K. J., Saraf, I., Hocart, C. H., Youngentob, K. N., Singh, I. P., and Foley, W. J. (2019). Occurrence and distribution of unsubstituted B-ring flavanones in Eucalyptus foliage. Phytochemistry 160, 31–39.
| Occurrence and distribution of unsubstituted B-ring flavanones in Eucalyptus foliage.Crossref | GoogleScholarGoogle Scholar | 30682682PubMed |
Marsh, K. J., Wallis, I. R., Kulheim, C., Clark, R., Nicolle, D., Foley, W. J., and Salminen, J. P. (2020). New approaches to tannin analysis of leaves can be used to explain in vitro biological activities associated with herbivore defence. New Phytologist 225, 488–498.
| New approaches to tannin analysis of leaves can be used to explain in vitro biological activities associated with herbivore defence.Crossref | GoogleScholarGoogle Scholar |
Marsh, K. J., Blyton, M. D. J., Foley, W. J., and Moore, B. D. (2021). Fundamental dietary specialisation explains differential use of resources within a koala population. Oecologia 196, 795–803.
| Fundamental dietary specialisation explains differential use of resources within a koala population.Crossref | GoogleScholarGoogle Scholar | 34142232PubMed |
Moore, B. D., Wallis, I. R., Marsh, K. J., and Foley, W. J. (2004). The role of nutrition in the conservation of the marsupial folivores of eucalypt forests. In ‘Conservation of Australia’s Forest Fauna’. 2nd edn. (Ed. D. Lunney) pp. 549–575. (Royal Zoological Society of New South Wales: Mossman, NSW.)
Moore, B. D., Foley, W. J., Wallis, I. R., Cowling, A., and Handasyde, K. A. (2005). Eucalyptus foliar chemistry explains selective feeding by koalas. Biology Letters 1, 64–67.
| Eucalyptus foliar chemistry explains selective feeding by koalas.Crossref | GoogleScholarGoogle Scholar | 17148129PubMed |
Noble, I. R. (1989). Ecological traits of the Eucalyptus Lherit subgenera Monocalyptus and Symphyomyrtus. Australian Journal of Botany 37, 207–224.
| Ecological traits of the Eucalyptus Lherit subgenera Monocalyptus and Symphyomyrtus.Crossref | GoogleScholarGoogle Scholar |
Pryor, L. (1959). Species distribution and association in Eucalyptus. In ‘Biogeography and ecology in Australia’. (Eds. A. Keast, R. Crocker, and C. Christian) pp. 461–471. (Junk: The Hague.)
Rios, J. M., Mangione, A. M., and Marone, L. (2012). Tolerance to dietary phenolics and diet breadth in three seed-eating birds: implications for graminivory. Journal of Experimental Zoology Part A - Ecological Genetics and Physiology 317A, 425–433.
| Tolerance to dietary phenolics and diet breadth in three seed-eating birds: implications for graminivory.Crossref | GoogleScholarGoogle Scholar |
Saraf, I., Choudhary, A., Sharma, R. J., Dandi, K., Marsh, K. J., Foley, W. J., and Singh, I. P. (2015). Extraction of pinocembrin from leaves of different species of Eucalyptus and its quantitative analysis by qNMR and HPTLC. Natural Product Communications 10, 379–382.
| Extraction of pinocembrin from leaves of different species of Eucalyptus and its quantitative analysis by qNMR and HPTLC.Crossref | GoogleScholarGoogle Scholar |
Saraf, I., Marsh, K. J., Vir, S., Foley, W. J., and Singh, I. P. (2017). Quantitative analysis of various B-ring unsubstituted and substituted flavonoids in ten Australian species of Eucalyptus. Natural Product Communications 12, 1695–1699.
| Quantitative analysis of various B-ring unsubstituted and substituted flavonoids in ten Australian species of Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Smith, A. P., and Ganzhorn, J. U. (1996). Convergence in community structure and dietary adaptation in Australian possums and gliders and Malagasy lemurs. Australian Journal of Ecology 21, 31–46.
| Convergence in community structure and dietary adaptation in Australian possums and gliders and Malagasy lemurs.Crossref | GoogleScholarGoogle Scholar |
Tucker, D. J., Wallis, I. R., Bolton, J. M., Marsh, K. J., Rosser, A. A., Brereton, I. M., Nicolle, D., and Foley, W. J. (2010). A metabolomic approach to identifying chemical mediators of mammal–plant interactions. Journal of Chemical Ecology 36, 727–735.
| A metabolomic approach to identifying chemical mediators of mammal–plant interactions.Crossref | GoogleScholarGoogle Scholar | 20556637PubMed |
Wollenweber, E., and Kohorst, G. (1981). Epicuticular leaf flavonoids from Eucalyptus species and from Kalmia latifolia. Zeitschrift fur Naturforschung C 36, 913–915.
| Epicuticular leaf flavonoids from Eucalyptus species and from Kalmia latifolia.Crossref | GoogleScholarGoogle Scholar |
Youngentob, K. N., Wallis, I. R., Lindenmayer, D. B., Wood, J. T., Pope, M. L., and Foley, W. J. (2011). Foliage chemistry influences tree choice and landscape use of a gliding marsupial folivore. Journal of Chemical Ecology 37, 71–84.
| Foliage chemistry influences tree choice and landscape use of a gliding marsupial folivore.Crossref | GoogleScholarGoogle Scholar | 21161340PubMed |
