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Rapid Assessment of the Nutritional Value of Foods Eaten by Mountain Gorillas: Applying Near-Infrared Reflectance Spectroscopy to Primatology

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Abstract

The increasing recognition of the considerable intraspecific spatial and temporal variability in the nutritional contents of primate foods has necessitated development of fast and cost-effective analytical methods. Used widely for agricultural products, near-infrared reflectance spectroscopy (NIRS) is a quick, inexpensive means of assessing nutritional chemistry. The general principle of NIRS is that when the sample is irradiated with near-infrared light, the reflectance spectrum is characteristic of the mixture of chemical bonds present in the sample. These spectra, when calibrated against reference values—determined via traditional nutritional analysis—to develop regression equations, can be used to estimate nutritional values of similar samples without doing traditional nutritional analysis. We validated the use of NIRS for estimating the nutritional attributes of African herbs and trees, which were foods eaten by mountain gorillas (Gorilla beringei) collected as part of a larger study on gorilla nutritional ecology. We determined the near-infrared spectra (1100–2400 nm) of 241 dried samples of 13 species of tropical herbs and trees that formed the staple diet of the gorillas. We used modified partial least-squares regression to develop calibration equations that could predict nutritional attributes of gorilla foods, and we performed an independent validation of the calibrations. The equations had robust predictive power similar to those used in agricultural and ecology, and we found no differences between samples measured via NIRS and traditional nutritional analysis. Our analysis indicates that NIRS offers a rapid and cost-effective means of analysis of tropical leaves and herbs, and has the potential to transform primate feeding ecology studies by allowing us to evaluate the importance of intraspecific variation in nutritional value.

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References

  • Baranga, D. (1983). Changes in chemical composition of food parts in the diet of colobus monkeys. Ecology, 64, 668–673.

    Article  CAS  Google Scholar 

  • Batten, G. D. (1998). Plant analysis using near infrared reflectance spectroscopy: the potential and the limitations. Australian Journal of Experimental Agriculture, 38, 697–706.

    Article  Google Scholar 

  • Butz, P., Hofmann, C., & Tauscher, B. (2005). Recent developments in noninvasive techniques for fresh fruit and vegetable internal quality analysis. Journal of Food Science, 70, R131–R141.

    CAS  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002). Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Rode, K. D., Hauck, E. M., & McDowell, L. R. (2003). Variation in the nutritional value of primate foods: among trees, time periods, and areas. International Journal of Primatology, 24, 317–333.

    Article  Google Scholar 

  • Coates, D. B. (2002). “Is near infrared spectroscopy only as good as the laboratory reference values?” An empirical approach. Spectroscopy Europe, 14, 24–26.

    CAS  Google Scholar 

  • Conklin-Brittain, N. L., Dierenfeld, E. S., Wrangham, R. W., Norconk, M., & Silver, S. C. (1999). Chemical protein analysis: a comparison of Kjeldahl crude protein and total ninhydrin protein from wild, tropical vegetation. Journal of Chemical Ecology, 25, 2601–2622.

    Article  CAS  Google Scholar 

  • da Costa, P. A., & Volery, P. (2005). Broad-based versus specific NIRS calibration: determination of total solids in fresh cheese. Analytica Chimica Acta, 544, 82–88.

    Article  CAS  Google Scholar 

  • DeGabriel, J. L., Wallis, I. R., Moore, B. D., & Foley, W. J. (2008). A simple, integrative assay to quantify nutritional quality of browses for herbivores. Oecologia, 156, 107–116.

    Article  PubMed  Google Scholar 

  • DeGabriel, J. L., Moore, B. D., Foley, W. J., & Johnson, C. N. (2009). The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology, 90, 711–719.

    Article  PubMed  Google Scholar 

  • Dury, S., Turner, B., Foley, B., & Wallis, I. R. (2001). Use of high spectral resolution remote sensing to determine leaf palatability of eucalypt trees for folivorous marsupials. International Journal of Applied Earth Observation and Geoinformation, 3, 328–336.

    Article  Google Scholar 

  • Ezenwa, V. O. (2004). Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology, 34, 535–542.

    Article  PubMed  Google Scholar 

  • Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., Wood, J. T., et al. (2009). Protein contents of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology 20, 685–690.

    Article  Google Scholar 

  • Foley, W. J., McIlwee, A., Lawler, I., Aragones, L., Woolnough, A. P., & 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.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1995). Low level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084–2096.

    Article  Google Scholar 

  • Ganzhorn, J. U. (2002). Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia, 131, 427–435.

    Article  Google Scholar 

  • Glander, K. E. (1982). The impact of plant secondary compounds on primate feeding behavior. Yearbook of Physical Anthropology, 25, 1–18.

    Article  Google Scholar 

  • Glasser, T., Landau, S., Ungar, E. D., Perevolotsky, A., Dvash, L., Muklada, H., et al. (2008). A fecal near-infrared reflectance spectroscopy-aided methodology to determine goat dietary composition in a Mediterranean shrubland. Journal of Animal Science, 86, 1345–1356.

    Article  PubMed  CAS  Google Scholar 

  • Goering, H. K., & Van Soest, P. J. (1970). Forage fiber analysis (pp. 1–20). Washington, DC: U.S. Department of Agriculture.

    Google Scholar 

  • Hruschka, W. R. (2001). Data analysis: Wavelength selection methods. In P. C. Williams & K. Norris (Eds.), Near-infrared technology in the agricultural and food industries (pp. 39–58). St. Paul, MN: American Association of Cereal Chemists.

    Google Scholar 

  • Kidane, N. F., Stuth, J. W., & Tolleson, D. R. (2008). Predicting diet quality of donkeys via fecal-NIRS calibrations. Rangeland Ecology & Management, 61, 232–239.

    Article  Google Scholar 

  • Koenig, A., Beise, J., Chalise, M. K., & Ganzhorn, J. U. (1998). When females should contest for food-testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behavioral Ecology and Sociobiology, 42, 225–237.

    Article  Google Scholar 

  • Kong, X., Xie, J., Wu, X., Huang, Y., & Bao, J. (2005). Rapid prediction of acid detergent fiber, neutral detergent fiber, and acid detergent lignin of rice materials by near-infrared spectroscopy. Journal of Agricultural and Food Chemistry, 53, 2843–2848.

    Article  PubMed  CAS  Google Scholar 

  • Landau, S., Nitzan, R., Barkai, D., & Dvash, L. (2006). Excretal near infrared reflectance spectrometry to monitor the nutrient content of diets of grazing young ostriches (Struthio camelus). South African Journal of Animal Science, 36, 248–256.

    Google Scholar 

  • Lawler, I. R., Foley, W. J., Eschler, B. M., Pass, D. M., & Handasyde, K. (1998). Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia, 116, 160–169.

    Article  Google Scholar 

  • Lawler, I. R., Foley, W. J., & Eschler, B. M. (2000). Foliar concentration of a single toxin creates habitat patchiness for a marsupial folivore. Ecology, 81, 1327–1338.

    Google Scholar 

  • Lawler, I. R., Aragones, L., Berding, N., Marsh, H., & Foley, W. J. (2006). Near-infrared reflectance spectroscopy is a rapid, cost-effective predictor of seagrass nutrients. Journal of Chemical Ecology, 32, 1353–1365.

    Article  PubMed  CAS  Google Scholar 

  • Locher, F., Heuwinkel, H., Gutser, R., & Schmidhalter, U. (2005). Development of near infrared reflectance spectroscopy calibrations to estimate legume content of multispecies legume-grass mixtures. Agronomy Journal, 97, 11–17.

    Article  Google Scholar 

  • Lyons, R. K., & Stuth, J. W. (1992). Fecal NIRS equations for predicting diet quality of free-ranging cattle. Journal of Range Management, 45, 238–244.

    Article  Google Scholar 

  • Mark, H. (2001). Qualitative near-infrared analysis. In P. C. Williams & K. Norris (Eds.), Near-infrared technology in the agricultural and food industries (pp. 233–238). St. Paul, MN: American Association of Cereal Chemists.

    Google Scholar 

  • McIlwee, A. M., Lawler, I. R., Cork, S. J., & Foley, W. J. (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 

  • Mertl-Millhollen, A. S., Moret, E. S., Felantosoa, D., Rasamimanana, H., Blumenfeld-Jones, K. C., & Jolly, A. (2003). Ring-tailed lemur home ranges correlate with food abundance and nutritional content at a time of environmental stress. International Journal of Primatology, 24, 965–985.

    Article  Google Scholar 

  • Milton, K. (1979). Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. American Naturalist, 114, 362–378.

    Article  CAS  Google Scholar 

  • Milton, K., & Dintzis, F. (1981). Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica, 12, 177–181.

    Article  Google Scholar 

  • Moore, B. D., & Foley, W. J. (2005). Tree use by koalas in a chemically complex landscape. Nature, 435, 488–490.

    Article  PubMed  CAS  Google Scholar 

  • Moore, B. D., Wallis, I. R., Wood, J. T., & Foley, W. J. (2004). Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecological Monographs, 74, 553–568.

    Article  Google Scholar 

  • Nkurunungi, J. B., Ganas, J., Robbins, M. M., & Stanford, C. B. (2004). A comparison of two mountain gorilla habitats in Bwindi Impenetrable National Park, Uganda. African Journal of Ecology, 42, 289–297.

    Article  Google Scholar 

  • Norris, K. H., Barnes, R. F., Moore, J. E., & Shenk, J. S. (1976). Predicting forage quality by infrared reflectance spectroscopy. Journal of Animal Science, 43, 889–897.

    CAS  Google Scholar 

  • Ortmann, S., Bradley, B. J., Stolter, C., & Ganzhorn, J. U. (2006). Estimating the quality and composition of wild animal diets: A critical survey of methods. In G. Hohmann, M. M. Robbins & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioral aspects (pp. 397–420). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Parveen, I., Moorby, J. M., Hirst, W. M., Morris, S. M., & Fraser, M. D. (2008). Profiling of plasma and faeces by FT-IR to differentiate between heathland plant diets offered to zero-grazed sheep. Animal Feed Science and Technology, 144, 65–81.

    Article  CAS  Google Scholar 

  • Redaelli, R., & Berardo, R. (2007). Prediction of fibre components in oat hulls by near infrared reflectance spectroscopy. Journal of the Science of Food and Agriculture, 87, 580–585.

    Article  CAS  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Molina, D. O., Shaw, A. V., Hintz, H. F., & Pell, A. N. (2006). Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. American Journal of Primatology, 68, 675–691.

    Article  PubMed  CAS  Google Scholar 

  • Rothman, J. M., Plumptre, A. J., Dierenfeld, E. S., & Pell, A. N. (2007). Nutritional composition of the diets of the mountain gorilla (Gorilla beringei): a comparison between two montane habitats. Journal of Tropical Ecology, 23, 673–682.

    Article  Google Scholar 

  • Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008a). Fiber-bound protein in gorilla diets: implications for estimating the intake of dietary protein by primates. American Journal of Primatology, 70, 690–694.

    Article  CAS  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Hintz, H. F., & Pell, A. N. (2008b). Nutritional quality of gorilla diets: consequences of age, sex and season. Oecologia, 155, 111–122.

    Article  Google Scholar 

  • Rothman, J. M., Dusinberre, K., & Pell, A. N. (2009). Condensed tannins in the diets of primates: a matter of methods? American Journal of Primatology, 71, 70–76.

    Article  PubMed  Google Scholar 

  • Shenk, J. S., & Westerhaus, M. O. (1991). Population definition, sample selection and calibration procedures for near-infrared reflectance spectroscopy. Crop Science, 31, 469–479.

    Google Scholar 

  • Shenk, J. S., & Westerhaus, M. O. (1994). The application of near infrared reflectance spetroscopy (NIRS) to forage analysis. In G. C. Fahey Jr. (Ed.), Forage quality, evaluation and utilization (pp. 406–449). Madison, WI: Soil Science Society of America/ American Society of Agronomy/ Crop Science Society of America.

    Google Scholar 

  • Shenk, J. S., & Westerhaus, M. O. (1996). Calibration the ISI way. In A. M. C. Davies & P. Williams (Eds.), Near infrared spectroscopy: The future waves (pp. 198–202). West Sussex, UK: NIR Publications.

    Google Scholar 

  • Shenk, J. S., Westerhaus, M. O., & Hoover, M. R. (1979). Analysis of forages by infrared reflectance. Journal of Dairy Science, 62, 807–812.

    CAS  Google Scholar 

  • Showers, S. E., Tolleson, D. R., Stuth, J. W., Kroll, J. C., & Koerth, B. H. (2006). Predicting diet quality of white-tailed deer via NIRS fecal profiling. Rangeland Ecology & Management, 59, 300–307.

    Article  Google Scholar 

  • Steen, R. W. J., Gordon, F. J., Dawson, L. E. R., Park, R. S., Mayne, C. S., Agnew, R. E., et al. (1998). Factors affecting the intake of grass silage by cattle and prediction of silage intake. Animal Science, 66, 115–127.

    Google Scholar 

  • Stolter, C., Julkunen-Tiitto, R., & Ganzhorn, J. U. (2006). Application of near infrared reflectance spectroscopy (NIRS) to assess some properties of a sub-arctic ecosystem. Basic and Applied Ecology, 7, 167–187.

    Article  Google Scholar 

  • Stuth, J., Jama, A., & Tolleson, D. (2003). Direct and indirect means of predicting forage quality through near infrared reflectance spectroscopy. Field Crops Research, 84, 45–56.

    Article  Google Scholar 

  • van Gils, J. A., Gyimesi, A., & van Lith, B. (2007). Avian herbivory: an experiment, a field test and an allometric comparison with mammals. Ecology, 88, 2926–2935.

    Article  PubMed  Google Scholar 

  • Van Soest, P. J. (1994). Nutritional ecology of the ruminant. Ithaca, NY: Cornell University Press.

    Google Scholar 

  • Van Soest, P. J., Robertson, J. B., & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.

    Article  PubMed  Google Scholar 

  • Ventura, M., de Jager, A., & de Putter, H. (1998). Non-destructive determination of soluble solids in apple fruit by near infrared spectroscopy (NIRS). Postharvest Biology and Technology, 14, 21–27.

    Article  Google Scholar 

  • Veraart, A. J., Nolet, B. A., Rosell, F., & de Vries, P. P. (2006). Stimulations winter browsing may lead to induced susceptibility of willows to beavers in spring. Canadian Journal of Zoology, 84, 1733–1742.

    Article  Google Scholar 

  • Wallis, I. R., Watson, M. L., & Foley, W. J. (2002). Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum. Australian Journal of Zoology, 50, 507–519.

    Article  Google Scholar 

  • Watts, D. P. (1998). Long-term habitat use by mountain gorillas (Gorilla gorilla beringei). 2. Reuse of foraging areas in relation to resource abundance, quality, and depletion. International Journal of Primatology, 19, 681–702.

    Article  Google Scholar 

  • Williams, P. C., & Norris, K. (2001). Variables affecting near-infrared spectroscopic analysis. In P. C. Williams & K. Norris (Eds.), Near-infrared technology in the agricultural and food industries (pp. 171–189). St. Paul, MN: American Association of Cereal Chemists.

    Google Scholar 

  • Woolnough, A. P., & du Toit, J. T. (2001). Vertical zonation of browse quality in tree canopies exposed to a size-structured guild of African browsing ungulates. Oecologia, 129, 585–590.

    Google Scholar 

  • Woolnough, A. P., & Foley, W. J. (2002). Rapid evaluation of pasture quality for a critically endangered mammal, the Northern hairy-nosed wombat (Lasiorhinus krefftii). Wildlife Research, 29, 91–100.

    Article  Google Scholar 

  • Worman, C. O., & Chapman, C. A. (2005). Seasonal variation in the quality of tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology, 21, 689–697.

    Article  Google Scholar 

  • Worman, C. O., & Chapman, C. A. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. International Journal of Primatology, 27, 203–225.

    Article  Google Scholar 

  • Yamashita, N. (2008). Chemical properties of the diets of two lemur species in Southwestern Madagascar. International Journal of Primatology, 29, 339–364.

    Article  Google Scholar 

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Acknowledgments

We thank Kathy Dusinberre and Jamie Crawford for laboratory assistance. The plant collections would not have been possible without the hard work of the field assistants at the Institute of Tropical Forest Conservation in Uganda. Alastair McNeilage, William Olupot, Joseph Okori, Dennis Babaasa, Robert Bitariho, John Makombo, and Aventino Kasangaki provided logistical support in the field. Jane Engel and the Robert G. Engel Family Foundation, the Department of Animal Science at Cornell University, Mario Einaudi Center, Cornell University Graduate School, and the Institute of African Development provided funding for this research, and the Canada Research Chairs program (awarded to C. A. Chapman) provided funding to J. M. Rothman during NIRS analysis and write-up. Joanna Setchell and 2 anonymous reviewers provided excellent suggestions, which improved the manuscript. All research conducted during this study complied with the regulations of the Government of Uganda and was conducted with the permission of the Uganda Wildlife Authority and the Uganda National Council for Science and Technology.

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Authors and Affiliations

  1. Department of Anthropology, Hunter College of the City University of New York, New York, NY, 10065, USA

    Jessica M. Rothman

  2. New York Consortium of Evolutionary Primatology, New York, NY, 10065, USA

    Jessica M. Rothman

  3. McGill School of Environment, McGill University, Montreal, QC, H3A 2T7, Canada

    Jessica M. Rothman

  4. Department of Animal Science, Cornell University, Ithaca, NY, 14853, USA

    Jessica M. Rothman, Debbie J. R. Cherney & Alice N. Pell

  5. McGill School of Environment and Department of Anthropology, McGill University, Montreal, QC, H3A 2T7, Canada

    Colin A. Chapman

  6. Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY, 10460, USA

    Colin A. Chapman

  7. Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY, 14853, USA

    Julie L. Hansen

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  1. Jessica M. Rothman
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  2. Colin A. Chapman
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  3. Julie L. Hansen
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  5. Alice N. Pell
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Correspondence to Jessica M. Rothman.

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Rothman, J.M., Chapman, C.A., Hansen, J.L. et al. Rapid Assessment of the Nutritional Value of Foods Eaten by Mountain Gorillas: Applying Near-Infrared Reflectance Spectroscopy to Primatology. Int J Primatol 30, 729–742 (2009). https://doi.org/10.1007/s10764-009-9372-z

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