Skip to main content
Log in

A simple, integrative assay to quantify nutritional quality of browses for herbivores

  • PLANT-ANIMAL INTERACTIONS - METHODS
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Many regard the concentrations of nitrogen (N), tannins and plant cell wall constituents (fibre) as key indicators of food quality and habitat suitability for browsing herbivores; yet there is no method for measuring their combined effects. We have developed a simple in vitro assay for measuring the effects of tannins and fibre on N availability in browse. We determined the effects of tannins by measuring the polyethylene glycol (PEG)-binding capacity (PEG-BC) of Eucalyptus leaf samples, followed by a two-stage in vitro digestion with pepsin and cellulase to determine the digestibility of dry matter and N. There was a significant relationship between concentrations of digestible N and the PEG-BC of the leaves. Furthermore, adding PEG significantly improved the digestibility of N. Our results concur with in vivo observations from several mammalian species. This suggests that our method is effective for measuring the nutritional quality of browse and the benefits of adding PEG, providing some index of the detrimental effects of tannins. We further simplified the assay by removing the PEG step, allowing us to quickly analyse samples in bulk. Nevertheless, this simplified method is still not practical for analysing the many samples necessary to compare the nutritional values of different tracts of forest. We used near-infrared reflectance spectroscopy to produce calibration equations and predicted total and digestible N in 322 trees at eleven sites. Both within and between sites, we found a wide variation in concentrations of digestible N but a much lower variation in total N, with either no relationship or poor relationships between the two measures. This confirms the variability in the nutritional quality of eucalypt forests, which may explain the distribution and abundance of mammalian herbivores. Thus, our assay provides a useful tool for understanding how food resources influence herbivore populations at different scales.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • ASTM (1995) Standard practices for infrared multivariate quantitative analysis (designation E1655-94). American Society for Testing and Materials (ASTM), Washington

  • Barnes RJ, Dhanoa MS, Lister SJ (1989) Standard normal variate transformation and detrending of near infra-red reflectance spectra. Appl Spectrosc 43:772–777

    Article  CAS  Google Scholar 

  • Batzli GO (1986) Nutritional ecology of the California vole—effects of food quality on reproduction. Ecology 67:406–412

    Article  Google Scholar 

  • Braithwaite LW, Turner J, Kelly J (1984) Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden N.S.W. III. Relationships between faunal densities, eucalypt occurrence and foliage nutrients, and soil parent materials. Aust Wildl Res 11:41–48

    Article  Google Scholar 

  • Choo GM, Waterman PG, McKey DB, Gartlan JS (1981) A simple enzyme assay for dry matter digestibility and its value in studying food selection by generalist herbivores. Oecologia 49:170–178

    Article  Google Scholar 

  • Cork SJ, Catling PC (1996) Modelling distributions of arboreal and ground-dwelling mammals in relation to climate, nutrients, plant chemical defences and vegetation structure in the eucalypt forests of southeastern Australia. For Ecol Manage 85:163–175

    Article  Google Scholar 

  • Dalla Pozza SA (1993) The use of mangroves by brushtail possums Trichosurus vulpecula, and the subsequent effects on the water and sodium turnover rates. B.Sc. (Hons.) thesis. Department of Zoology, James Cook University, Townsville

  • Decandia M, Sitzia M, Cabiddu A, Kababya D, Molle G (2000) The use of polyethylene glycol to reduce the anti-nutritional effects of tannins in goats fed woody species. Small Rumin Res 38:157–164

    Article  Google Scholar 

  • Degen AA, Becker K, Makkar HPS, Borowy N (1995) Acacia saligna as a fodder tree for desert livestock and the interaction of its tannins with fiber fractions. J Sci Food Agric 68:65–71

    Article  CAS  Google Scholar 

  • Eschler BM, Pass DM, Willis R, Foley WJ (2000) Distribution of foliar formylated phloroglucinol derivatives amongst Eucalyptus species. Biochem Syst Ecol 28:813–824

    Article  PubMed  CAS  Google Scholar 

  • Falster DS, Warton DI, Wright IJ (2006) SMATR: standardised major axis tests and routines, version 2.0. http://www.bio.mq.edu.au/ecology/SMATR/. Accessed 1 February 2008

  • Foley WJ, Hume ID (1987) Digestion and metabolism of high-tannin Eucalyptus foliage by the brushtail possum (Trichosurus vulpecula) (Marsupialia: Phalangeridae). J Comp Physiol B Biochem Syst Environ Physiol 157:67–76

    Article  CAS  Google Scholar 

  • Foley WJ, Moore BD (2005) Plant secondary metabolites and vertebrate herbivores—from physiological regulation to ecosystem function. Curr Opin Plant Biol 8:430–435

    Article  PubMed  CAS  Google Scholar 

  • Foley WJ, McIlwee A, Lawler I, Aragones L, Woolnough AP, Berding N (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 (review). Oecologia 116:293–305

    Article  Google Scholar 

  • Foley WJ, Iason GR, McArthur C (1999) Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Jung H-JG, Fahey GCJ (eds) Nutritional ecology of herbivores: Proc 5th Int Symp Nutrition of Herbivores. American Society of Animal Science, Savoy, IL, pp 130–209

  • Fox LR, Macauley BJ (1977) Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia 29:145–162

    Google Scholar 

  • Getachew G, Makkar HPS, Becker K (2000) Effect of polyethylene glycol on in vitro degradability of nitrogen and microbial protein synthesis from tannin-rich browse and herbaceous legumes. Br J Nutr 84:73–83

    PubMed  CAS  Google Scholar 

  • Gilboa N, Perevolotsky A, Landau S, Nitsan Z, Silanikove N (2000) Increasing productivity in goats grazing Mediterranean woodland and scrubland by supplementation of polyethylene glycol. Small Rumin Res 38:183–190

    Article  Google Scholar 

  • Hagerman AE, Butler LG (1989) Choosing appropriate methods and standards for assaying tannin. J Chem Ecol 15:1795–1810

    Article  CAS  Google Scholar 

  • Hagerman AE, Robbins CT, Weerasuriya Y, Wilson TC, McArthur C (1992) Tannin chemistry in relation to digestion. J Range Manage 45:57–62

    Article  Google Scholar 

  • Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge

  • Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc 64:123–131

    Article  PubMed  CAS  Google Scholar 

  • Jones WT, Mangan JL (1977) Complexes of the condensed tannins of sainfoin (Onobrychis vicifolia Scop.) with fraction 1 leaf protein and with submaxillay mucoprotein, and their reversal by polyethylene glycol and pH. J Sci Food Agric 28:126–136

    Article  CAS  Google Scholar 

  • Jones RJ, Palmer B (2000) In vitro digestion studies using C-14-labelled polyethylene glycol (PEG) 4000: comparison of six tanniniferous shrub legumes and the grass Panicum maximum. Anim Feed Sci Technol 85:215–221

    Article  Google Scholar 

  • Landau S, et al (2004) Determination of poly(ethylene glycol)-binding to browse foliage, as an assay of tannin, by near-infrared reflectance spectroscopy. J Agric Food Chem 52:638–642

    Article  PubMed  CAS  Google Scholar 

  • Landau S, Glasser T, Dvash L (2006) Monitoring nutrition in small ruminants with the aid of near infrared reflectance spectroscopy (NIRS) technology: a review. Small Rumin Res 61:1–11

    Article  Google Scholar 

  • Makkar HPS (2003) Quantification of tannins in tree and shrub foliage: a laboratory manual. Kluwer Academic, Dordrecht

  • Makkar HPS (2005) In vitro gas methods for evaluation of feeds containing phytochemicals. Anim Feed Sci Technol 123–124:291–302

    Article  CAS  Google Scholar 

  • Makkar HPS, Singh B (1991) Distribution of condensed tannins (proanthocyanidins) in various fibre fractions in young and mature leaves of some oak species. Anim Feed Sci Technol 32:253–260

    Article  CAS  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). J Comp Physiol B Biochem Syst Environ Physiol 173:69–78

    CAS  Google Scholar 

  • 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). Aust J Zool 51:31–42

    Article  CAS  Google Scholar 

  • Martin RW, Handasyde KA (1999) The koala: natural history, conservation and management, 2nd edn. University of New South Wales Press, Sydney

    Google Scholar 

  • McArthur C (1988) Variation in neutral detergent fibre analysis of tannin-rich foliage. J Wildl Manage 52:374–378

    Article  Google Scholar 

  • McArthur C, Sanson GD (1991) Effects of tannins on digestion in the common ringtail possum (Pseudocheirus peregrinus), a specialized marsupial folivore. J Zool 225:233–251

    Article  Google Scholar 

  • McIlwee AM, Lawler IR, Cork SJ, Foley WJ (2001) Coping with chemical complexity in mammal–plant interactions: near-infrared spectroscopy as a predictor of Eucalyptus foliar nutrients and of the feeding rates of folivorous marsupials. Oecologia 128:539–548

    Article  Google Scholar 

  • Min BR, McNabb WC, Barry TN, Kemp PD, Waghorn GC, McDonald MF (1999) The effect of condensed tannins in Lotus corniculatus upon reproductive efficiency and wool production in sheep during late summer and autumn. J Agric Sci 132:323–334

    Article  CAS  Google Scholar 

  • Mlambo V, Makkar HPS (2005) Calibration and validation of the C-14-labelled polyethylene glycol-binding assay for tannins in tropical browse. Anim Feed Sci Technol 122:29–40

    Article  CAS  Google Scholar 

  • Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435:488–490

    Article  PubMed  CAS  Google Scholar 

  • 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 (eds) Conservation of Australia’s forest fauna, 2nd edn. Royal Zoological Society of New South Wales, Mosman, pp 549–575

    Google Scholar 

  • Moore BD, Wallis IR, Wood J, Foley WJ (2004b) Foliar nutrition, site quality and temperature affect foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol Monogr 74:553–568

    Article  Google Scholar 

  • Mueller-Harvey I (2006) Unravelling the conundrum of tannins in animal nutrition and health. J Sci Food Agric 86:2010–2037

    Article  CAS  Google Scholar 

  • Palmer B, Jones RJ (2000) The effect of PEG addition in vitro on dry matter and nitrogen digestibility of Calliandra calothyrsus and Leucaena leucocephala leaf. Anim Feed Sci Technol 85:259–268

    Article  CAS  Google Scholar 

  • Pettorelli N, Gaillard JM, Duncan P, Ouellet JP, Van Laere G (2001) Population density and small-scale variation in habitat quality affect phenotypic quality in roe deer. Oecologia 128:400–405

    Article  Google Scholar 

  • Robbins CT, et al (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107

    Article  CAS  Google Scholar 

  • Shenk JS, Westerhaus MO (1991) Population definition, sample selection and calibration procedures for near infrared reflectance spectroscopy. Crop Sci 31:469–474

    Article  Google Scholar 

  • Shimada T, Saitoh T (2003) Negative effects of acorns on the wood mouse Apodemus speciosus. Popul Ecol 45:7–17

    Google Scholar 

  • Silanikove N, Nitsan Z, Perevolotsky A (1994) Effect of a daily supplementation of polyethylene glycol on intake and digestion of tannin-containing leaves (Ceratonia siliqua) by sheep. J Agric Food Chem 42:2844–2847

    Article  CAS  Google Scholar 

  • Silanikove N, Gilboa N, Nir I, Perevolotsky A, Nitsan Z (1996a) Effect of a daily supplementation of polyethylene glycol on intake and digestion of tannin-containing leaves (Quercus calliprinos, Pistacia lentiscus, and Ceratonia siliqua) by goats. J Agric Food Chem 44:199–205

    Article  CAS  Google Scholar 

  • Silanikove N, Shinder D, Gilboa N, Eyal M, Nitsan Z (1996b) Binding of poly(ethylene glycol) to samples of forage plants as an assay of tannins and their negative effects on ruminal degradation. J Agric Food Chem 44:3230–3234

    Article  CAS  Google Scholar 

  • Silanikove N, Perevolotsky A, Provenza FD (2001) Use of tannin-binding chemicals to assay for tannins and their negative postingestive effects in ruminants. Anim Feed Sci Technol 91:69–81

    Article  CAS  Google Scholar 

  • Van Soest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Comstock, Ithaca, NY

  • Vogel KP, Pedersen JF, Masterson SD, Toy JJ (1999) Evaluation of a filter bag system for NDF, ADF, and IVDMD forage analysis. Crop Sci 39:276–279

    Article  Google Scholar 

  • White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin

    Google Scholar 

Download references

Acknowledgements

We are grateful to Euan Ritchie and Lewis Anderson for help with collecting leaf samples and Frances Marsh and Elesha Curran for assistance in the laboratory. We thank Raymond Jones for valuable advice and discussions and Glenn Iason and two anonymous reviewers for helpful comments on an earlier version of the manuscript. Ray and Betty Fryer, Brian Furber and the Australian Wildlife Conservancy kindly allowed us access to their land. Leaf samples were collected under Queensland EPA permit number—WISP03374205. Funding was provided by grants from the Australian Research Council to WJF and the Australia-Pacific Science Foundation to BDM. JLD was supported by an Australian National University Graduate School Scholarship and thanks Chris Johnson for advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jane L. DeGabriel.

Additional information

Communicated by Jörg Ganzhorn.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 25 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

DeGabriel, J.L., Wallis, I.R., Moore, B.D. et al. A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia 156, 107–116 (2008). https://doi.org/10.1007/s00442-008-0960-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-0960-y

Keywords

Navigation