Abstract
Estimating the nutritional value of a herbivore’s diet is difficult because it requires knowing what the animal eats, the relative quality of each component and how these components interact in relation to animal physiology. Current methods are cumbersome and rely on many assumptions that are hard to evaluate. We describe a new method for estimating relative diet quality directly from faeces that avoids the problems inherent in other methods. We combine this method with near infrared reflectance spectroscopy (NIRS) to analyse many samples and thus provide a technique with immense value in ecological studies. The method stems from the correlation between the concentrations of dietary and faecal nitrogen in herbivores eating a tannin-free diet, but a weaker relationship in browsers that ingest substantial amounts of tannins, which form complexes with proteins. These complexes reduce the availability of nitrogen and may increase faecal nitrogen concentrations. Using the tannin-binding compound, polyethylene glycol, we showed that tannin-bound nitrogen is a significant and variable part of faecal nitrogen in wild common brushtail possums (Trichosurus vulpecula). We developed a technique to measure faecal available nitrogen and found that it predicted the reproductive success of female brushtail possums in northern Australia. Faecal available nitrogen combined with NIRS provides a powerful tool for estimating the relative nutritional value of the diets of browsing herbivores in many ecological systems. It is a better indicator of diet quality than other commonly used single-nutrient measures such as faecal nitrogen and foliage analysis paired with observed feeding behaviour.
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References
American Society for Testing and Materials (1995) Standard practices for infrared, multivariate, quantitative analysis (Designation: E1655-94). American Society for Testing and Materials, West Conshohocken, PA
Ayres MP, Clausen TP, McLean SFJ, Redman AM, Reichard PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712
Bilgener M (1988) Chemical components of howler monkey (Alouatta palliata) food choice and kinetics of tannin binding with natural polymers. PhD dissertation, Boston University, Boston
Braithwaite LW, Turner J, Kelly J (1984) Studies on the arboreal marsupial fauna of eucalypt forests being harvested for pulpwood 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
Braithwaite LW, Binns DL, Nowlan RD (1988) The distribution of arboreal marsupials in relation to eucalypt forest types in the Eden (N.S.W.) woodchip concession area. Aust Wildl Res 15:363–373
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
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
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 Manag 85:163–175
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
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 90:711–719
Fashing PJ, Dierenfeld ES, Mowry CB (2007) Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. Int J Primatol 28:673–703
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. Oecologia 116:293–305
Hagerman AE, Robbins CT, Weerasuriya Y, Wilson TC, McArthur C (1992) Tannin chemistry in relation to digestion. J Range Manag 45:57–62
Hobbs NT (1987) Fecal indices to dietary quality—a critique. J Wildl Manag 51:317–320
Hodgeman TP, Davitt BB, Nelson JR (1996) Monitoring mule deer diet quality and intake with fecal indices. J Range Manag 49:215–222
How RA, Hillcox SJ (2000) Brushtail possum, Trichosurus vulpecula, populations in south-western Australia: demography, diet and conservation status. Wildl Res 27:81–89
Johnson CN, Clinchy M, Taylor AC, Krebs CJ, Jarman PJ, Payne A, Ritchie EG (2001) Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum. Proc R Soc Lond B 268:2001–2005
Kamler J, Homolka M (2005) Faecal nitrogen: a potential indicator of red and roe deer diet quality in forest habitats. Folia Zool 54:89–98
Kohn MH, Wayne RK (1997) Facts from faeces revisited. Tr Ecol Evol 12:223–227
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
Kucera TE (1997) Fecal indicators, diet and population parameters in mule deer. J Wildl Manag 61:550–560
Leslie DM, Starkey EE (1987) Fecal indices to dietary quality: a reply. J Wildl Manag 51:321–325
Leslie DM, Bowyer RT, Jenks JA (2008) Facts from faeces: nitrogen still measures up as a nutritional index for mammalian herbivores. J Wildl Manag 72:1420–1433
Makkar HPS (2003) Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Ruminant Res 49:241–256
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
Mason VC (1969) Some observations on the distribution and origin of nitrogen in sheep faeces. J Agric Sci 73:99–111
McArt SH, Spalinger DE, Collins WB, Schoen ER, Stevenson T, Bucho M (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology 90:1400–1411
Milton K, Van Soest PJ, Robertson JB (1980) Digestive efficiencies of wild howler monkeys. Physiol Zool 53:402–409
Moore BD, Wallis IR, Wood JT, Foley WJ (2004) Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol Monogr 74:553–568
Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, Dasilva GL, Mole S (1990) Determinants of variation in tropical forest primate biomass—new evidence from West-Africa. Ecology 71:328–343
Provenza FD, Pfister JA, Cheny CD (1992) Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. J Range Manag 45:36–45
Provenza FD, Villalba JJ, Cheney CD, Werner SJ (1998) Self-organization of foraging behaviour: from simplicity to complexity without goals. Nutr Res Rev 11:199–222
Provenza FD, Kimball BA, Villalba JJ (2000) Roles of odor, taste, and toxicity in the food preferences of lambs: implications for mimicry in plants. Oikos 88:424–432
Putman RJ (1984) Facts from faeces. Mammal Rev 14:79–97
Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987) Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:1606–1615
Schwarm A, Schweigert M, Ortmann S, Hummel J, Janssens G, Streich W, Clauss M (2008) No easy solution for the fractionation of faecal nitrogen in captive wild herbivores: results of a pilot study. J Anim Physiol Anim Nutr 93:596–605
Shrestha R, Wegge P (2006) Determining the composition of herbivore diets in the trans-Himalayan rangelands: a comparison of field methods. Rangel Ecol Manag 59:512–518
Verheyden H, Aubry L, Merlet J, Petibon P, Chauveau-Duriot B, Guillon N, Duncan P (2011) Faecal nitrogen, an index of diet quality in roe deer Capreolus capreolus? Wildl Biol 17:166–175
Wallis IR, Watson ML, Foley WJ (2002) Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Aust J Zool 50:507–519
Wasserman MD, Chapman CA (2003) Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. J Anim Ecol 72:650–659
White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin
Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126
Acknowledgments
We thank R. and E. Fryer, Australian Wildlife Conservancy, and other land owners for permission to use their land. We thank Elesha Curran for assistance with field and laboratory work. Funding was provided by grants from the Australian Research Council to C.N. Johnson and W.J. Foley and the Ecological Society of Australia and Royal Zoological Society of N.S.W. to J.L. DeGabriel.
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The authors declare that they have no conflict of interest.
Ethical standards
The procedures were approved by the Animal Experimentation Ethics Committee of the Australian National University and conform to the Guiding Principles in the Care and Use of Animals. Experiments comply with the current laws of Australia.
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Communicated by Joanna Lambert.
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Windley, H.R., Wallis, I.R., DeGabriel, J.L. et al. A faecal index of diet quality that predicts reproductive success in a marsupial folivore. Oecologia 173, 203–212 (2013). https://doi.org/10.1007/s00442-013-2616-9
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DOI: https://doi.org/10.1007/s00442-013-2616-9