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African rainforest vegetation and rumen microbes: Phenolic compounds and nutrients as correlates of digestibility

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Summary

In order to refine hypotheses concerning food selection by generalist herbivores with ruminant-like digestive systems the chemical correlates of digestibility in such a system have been studied. Samples of seeds and leaves from tree species growing in two African rainforests (Douala-Edea Forest Reserve, Cameroon, and Kibale Forest, Uganda) were assayed for phenolic content and nutrient content, and in-vitro dry matter digestibility was analysed utilizing rumen inoculum from a fistulated steer. Both forests studied carry populations of colobine monkeys with ruminant like digestive tracts. Content of condensed tannins and, to a lesser extent of total phenolics, was found to be negatively correlated with digestibility; a result that may be attributable to the inctivation of microbial enzymes by tannins. The negative association of tannin content and digestibility was stronger in material from the Cameroon site, the vegetation of which contains considerably higher concentrations of tannins and is generally less digestible than that from the Ugandan site. Gross energy content of leaves was also found to be persistently negatively correlated with digestibility. The interpretation of this result is uncertain; however, gross energy yield may well reflect variation in content of cell wall polymers, especially lignin. For the complete set of data, tannins presented the strongest observed correlation with digestibility, but when only mature leaves were considered the relationship with gross energy appeared stronger. No strong association was noted between high nutrient content and high digestibility. This was attributed to the fact that the assay measured the extent of digestion under standardised and very favourable conditions of nutrient supply. The results obtained are discussed in relation to observations of leaf and seed selection preferences of Colobus spp. in these two forests.

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References

  • Aerts JV, De Brabander DL, Cottyn BG, Butsse FX, Carlier LA, Moermans RJ (1978) Some remarks on the analytical procedure of van Soest for the prediction of forage digestibility. Animal Feed Sci Technol 3:309–322

    Google Scholar 

  • Allen SE (1974) Chemical Analysis of Ecological Materials. Blackwell, Scientific Publications Oxford

    Google Scholar 

  • Barnes RF (1973) Laboratory methods of evaluating feeding value of herbage. In: Butler GW, Bailey RW (eds) Chemistry and biochemistry of herbage, vol 1. Academic Press, London, pp 179–214

    Google Scholar 

  • Barnes RF, Mott GO, Packett LB, Plumlee MP (1964) Comparison of in vitro fermentation methods. J Anim Sci 23:1061–1065

    Google Scholar 

  • Bauchop T (1971) Stomach microbiology of primates. Annu Rev Microbiol 25:429–436

    Google Scholar 

  • Bauchop T, Martucci RW (1968) Ruminant-like digestion in the langur monkey. Science 161:698–700

    Google Scholar 

  • Baumgardt BR, Cason JL, Taylor MW (1962) Evaluation of forages in the laboratory. I. Comparative accuracy of several methods. J Dairy Sci 45:59–61

    Google Scholar 

  • Baumgardt BR, Oh HK (1964) Evaluation of forages in the laboratory. IV. Within and among trial variability of the Wisconsin artificial rumen process. J Dairy Sci 47:263–266

    Google Scholar 

  • Bernays EA (1978) Tannins: an alternative viewpoint. Entomol Exp Appl 24:244–253

    Google Scholar 

  • Bigelow D, Heflin D (1972) A procedure for in vitro dry matter digestibility. Colorado, Fort Collins, Natural Resource Ecology Lab Mimeo

  • Black JL, Sharkey MJ (1970) Reticular groove (sulcis reticuli): an obligatory adaptation in ruminant-like herbivores? Mammalia 34:294–302

    Google Scholar 

  • Boling JA, Bush LP, Buckner RC, Pendlum LC, Burns PB, Yates SG, Rogovin SP, Tookey HL (1975) Nutrient digestibility and metabolism in lambs fed added perloline. J Anim Sci 40:972

    Google Scholar 

  • Bowden DM, Church DC (1962) Artificial rumen investigations. II. Correlations between in vitro and in vivo measures of digestibility and chemical components of forages. J Dairy Sci 45:980–985

    Google Scholar 

  • Burns J (1971) Method for estimation of tannin in sorghum grain. Agron J 63:511–512

    Google Scholar 

  • Bush LP, Streeter C, Buckner RC (1970) Perloline inhibition of in vitro ruminal cellulose digestion. Crop Sci 10:108–109

    Google Scholar 

  • Cooper-Driver G, Finch S, Swain T, Bernays EA (1977) Seasonal variation in secondary plant compounds in relation to the palatability of Pteridium aquilinum. Biochem Syst Ecol 5:177–183

    Google Scholar 

  • Crichton EG, Waterman PG (1979) Manniflavanone, a novel flavanone dimer from Garcinia mannii. Phytochemistry 18:1553–1557

    Google Scholar 

  • Dalby A, Schumann AC (1978) Temperature induced errors in the colorimetric determination of tannins. Anal Biochem 85:325–327

    Google Scholar 

  • Donnelly ED, Anthony WB (1969) Relationship of tannin, dry matter digestibility, and crude protein in sericea lespedeza. Crop Sci 9:361–362

    Google Scholar 

  • Donnelly ED, Anthony WB (1970) Effects of genotype and tannin on dry matter digestibility in sericea lespedeza. Crop Sci 10:200–202

    Google Scholar 

  • Drawert F, Kuhn H-J, Rapp A (1962) Reaktions-Gaschromatographie, III. Gaschromatographische Bestimmung der niederfluchtigen Fettsäuren in Magen von Schlankaffen (Colobinae). Z Physiol Chem 329:84–89

    Google Scholar 

  • Driedger A, Hatfield EE (1972) Influence of tannins on the nutritive value of soybean meal for ruminants. J Anim Sci 34:465–468

    Google Scholar 

  • Feeny PP (1976) Plant apparency and chemical defence. In: Wallace JW, Mansell RL (eds) Recent advances in phytochemistry, vol 10. Plenum Press, New York, pp 1–40

    Google Scholar 

  • Fischer FC, Doorne H van, Lim MI, Svendsen AB (1976) Bacteriostatic activity of some coumarin derivatives. Phytochemistry 15:1078–1079

    Google Scholar 

  • Foley GF, McCarthy RE, Binns VM, Snell EE, Guirard BM, Kidder GW, Dewey VC, Thayer PC (1959) A comparative study of the use of micro-organisms in the screening of potential antitumor agents. Ann New York Acad Sci 76:413–441

    Google Scholar 

  • Ford CW, Morrison IM, Wilson JR (1979) Temperature effects on lignin, hemicellulose and cellulose in tropical and temperate grasses. Aust J Agric Res 30:621–633

    Google Scholar 

  • Fowden L, Lewis D, Tristam H (1967) Toxic amino acids: their action as antimetabolites. Adv Enzymol 29:89–163

    Google Scholar 

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

    Google Scholar 

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory in mammals: the role of plant secondary compounds. Am Nat 108:269–289

    Google Scholar 

  • Gartlan JS, McKey DB, Waterman PG (1978) Soils, forest structure and feeding behaviour of primates in a Cameroon coastal rainforest. In: Chivers DJ, Herbert J (eds) Recent advances in primatology, vol 1. Academic Press, London pp 259–267

    Google Scholar 

  • Gartlan JS, Waterman PG, McKey DB, Struhsaker TT (1980) A comparative study of the phytochemistry of two African rainforests. Biochem Syst Ecol. in press

  • Goldstein JL, Swain T (1963) Changes in tannin in ripening fruit. Phytochemistry 2:371–383

    Google Scholar 

  • Grant WD, McMurtry CM (1978) Effects of condensed tannins on the growth of micro-organisms. In: Loutit MW, Miles JAR (eds) Microbial ecology. Springer, Berlin Heidelberg New York, pp 427–430

    Google Scholar 

  • Griffiths DW, Jones DIH (1977) Cellulase inhibition by tannins in the testa of field beans (Vicia faba). J Sci Food Agric 28:983–989

    Google Scholar 

  • Harris HB, Cummins DG, Burns RE (1970) Tannin content and digestibility of sorghum grain as influenced by bagging. Agron J 62:633–635

    Google Scholar 

  • Henis Y, Tagari H, Volcani R (1964) Effect of water extracts of carob pods, tannic acid, and their derivatives on the morphology and growth of micro-organisms. Appl Microbiol 12:204–209

    Google Scholar 

  • Henry TA (1949) The alkaloids 4th edn. J and A Churchill, London

    Google Scholar 

  • Hladik CM, Gueguen L (1974) Geophagie et nutrition minerale chez les primates sauvages. C R Acad Sci Ser D: 279:1393–1396

    Google Scholar 

  • Horowitz W (ed) (1970) Official methods of analysis of the Association of Official Analyticla Chemists, 11th edn. AOAC, Washington DC

    Google Scholar 

  • Hungate RE (1966) The rumen and its microbes. Academic Press, New York

    Google Scholar 

  • Hungate RE (1975) The rumen microbial system. Annu Rev Ecol Syst 6:39–66

    Google Scholar 

  • Ivie GW, Witzel DA, Herz W, Kannan R, Norman JO, Rushing DD, Rowe LD, Veech JA (1975) Hymenovin. Major toxic constituent of western bitterweed (Hymenoxys odorata DC). J Agric Food Chem 23:841–845

    Google Scholar 

  • Janis C (1976) The evolutionary strategy of the Equidae and the origins of rumen and caecal digestion. Evolution 30:757–774

    Google Scholar 

  • Johnson RR, Dehority BA, Conrad HR, Davis RR (1962) Relationship of in vitro cellulose digestibility of undried and dried mixed forages to their in vivo dry matter digestibility. J Dairy Sci 45:250–252

    Google Scholar 

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

    Google Scholar 

  • Kay RNB, Hoppe P, Maloiy GMO (1976) Fermentative digestion of food by the colobus monkey, Colobus polykomos. Experentia 32:485–486

    Google Scholar 

  • Kuhn H-J (1964) Zur Kenntnis von Bau und Funktion des Magens der Schlankaffen (Colobinae). Folia Primatol 2:193–221

    Google Scholar 

  • Lanigan GW, Smith LW (1970) Metabolism of pyrrolizidine alkaloids in ovine rumen. I. Formation of 7-α-hydroxy-α-methyl-8-α-pyrrolizidine from heliotropina and basiocarpine. Aust J Agric Res 21:493–500

    Google Scholar 

  • Leroy F, Zelter SZ, Francois A (1967) Protection des proteines alimentaires contre la desamination bacterienne en milieu de rumen. Proc 7th Int Congr Nutr 5:113–117

    Google Scholar 

  • Longhurst WM, Oh HK, Jones MB, Kepner RE (1968) A basis for the palatability of deer forage plants. Trans North Am Wildl Nat Resour Conf 33:181–189

    Google Scholar 

  • Loomis WD, Battaile J (1966) Plant phenolic compounds and the isolation of plant enzymes. Phytochemistry 5:423–428

    Google Scholar 

  • Lyford SJ, Smart WWG, Bell TA (1967) Inhibition of rumen cellulose digestion by extracts of sericea lespedeza. J Anim Sci 26:632–637

    Google Scholar 

  • Mandels M, Reese ET (1965) Inhibition of cellulases. Annu Rev Phytopathol 3:85–102

    Google Scholar 

  • Maner JH, Gomez G (1973) Implications of cyanide toxicity in animal feeding studies using high cassava rations. In: Nestels B, MacIntyre R (eds) Chronic cassava toxicity: Proceedings of an International Workshop. Int Development Research Center Monograph, Ottawa, pp 113–120

  • Marquardt RR, McKirdy JA, Ward AT (1978) Comparative cell wall constituent levels of tannin-free and tannin-containing cultivars of faba beans (Vicia faba L.) Can J Anim Sci 58:775–781

    Google Scholar 

  • McKey DB (1978) Plant chemical defenses and the feeding and ranging behavior of Colobus monkeys in African rainforests. PhD Dissertation, University of Michigan (University Microfilms International)

  • McKey DB, Waterman PG, Mbi CN, Gartlan JS, Struhsaker TT (1978) Phenolic content of vegetation in two African rainforests: ecological implications. Science 202:61–64

    Google Scholar 

  • McLeod MN, Minson DJ (1976) The analytical and biological accuracy of estimating dry matter digestibility of different legume species. Anim Feed Sci Technol 1:61–72

    Google Scholar 

  • Moir RJ (1968) Ruminant digestion and evolution. In: Handbook of physiology, vol 5. Am Physiol Soc, Washington DC, pp 2673–2694

    Google Scholar 

  • Nagy JG, Steinhoff HW, Ward GM (1964) Effects of essential oils of sagebrush on deer rumen microbial function. J Wild Manage 28:785–790

    Google Scholar 

  • Nagy JG, Tengerdy RP (1968) Antibacterial action of essential oils of Artemisia as an ecological factor. II. Antibacterial action of the volatile oils of Artemisia tridentata (big sagebrush) on bacteria from the rumen of mule deer. Appl Microbiol 16:441–444

    Google Scholar 

  • Oates JF (1977) The guereza and its food. In: Clutton-Brock TH (ed) Primate ecology. Academic Press, London, pp 275–321

    Google Scholar 

  • Oates JF (1978) Water-plant and soil consumption of guereza monkeys (Colobus guereza): a relationship with minerals and toxins in the diet? Biotropica 10:241–253

    Google Scholar 

  • Oates JF, Swain T, Zantovska J (1977) Secondary compounds and food selection by colobus monkeys. Biochem Syst Ecol 5:317–321

    Google Scholar 

  • Oates JF, Waterman PG, Choo GM (1980) Food selection by the south Indian leaf-monkey, Presbytis johnii, in relation to leaf chemistry. Oecologia (Berl) 45:45–56

    Google Scholar 

  • Oh HK, Jones MB, Longhurst WM (1968) Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species. Appl Microbiol 16:39–44

    Google Scholar 

  • Oh HK, Sakai T, Jones MB, Longhurst WM (1967) Effects of various essential oils isolated from Douglas Fir needles upon sheep and deer rumen microbial activity. Appl Microbiol 15:777–784

    Google Scholar 

  • Osbourn DF (1978) Principles governing the use of chemical methods for assessing the nutritive value of forages: a review. Anim Feed Sci Technol 3:265–275

    Google Scholar 

  • Price ML, Butler LG (1977) Rapid visual estimation and spectrophotometric determination of tannin content in sorghum grain. J Agric Food Chem 25:1268–1273

    Google Scholar 

  • Reiser R, Fu HC (1962) The mechanism of gossypol detoxification in ruminant animals. J Nutr 76:215–218

    Google Scholar 

  • Rhoades DF (1977) The antiherbivore chemistry of Larrea. In: Mabry TJ, Hunziker JH, DiFeo DF (eds) Creosote bush. Biology and chemistry of Larrea in New World Deserts. Dowden, Hutchinson and Ross, Inc. Stroudsberg, p 135–175

    Google Scholar 

  • Rhoades DF, Cates RG (1976) Toward a general theory of plant anti-herbivore chemistry. In: Wallace JW, Mansell RW (eds) Recent advances in phytochemistry, vol 10. Plenum Press, New York, p 168–213

    Google Scholar 

  • Ribereau-Gayon P (1972) Plant phenolics. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Rosenthal G, Janzen DH (eds) (1979) Interrelationships of secondary plant constituents and herbivores. Academic Press, New York

    Google Scholar 

  • Russell GR, Smith RM (1968) Reduction of heliotrine by a rumen micro-organism. Aust J Biol Sci 21:1277–1290

    Google Scholar 

  • Sarker SK, Howarth RE (1976) Specificity of the vanillin test for flavonols. J Agric Food Chem 24:317–320

    Google Scholar 

  • Sherbrooke WC (1976) Differential acceptance of toxic jojoba seed (Simondsia chinensis) by four Sonoran Desert heteromyid rodents. Ecology 57:596–602

    Google Scholar 

  • Simkins KL, Baumgardt BR (1963) Evaluation of forages in the laboratory. III. Comparison of various methods for predicting silage digestibility. J Dairy Sci 46:338–40

    Google Scholar 

  • Simons AB, Marten GC (1971) Relationship of indole alkaloids to palatability of Phalaris arundinacea L. Agron J 63:915–919

    Google Scholar 

  • Singleton VL, Kratzer FH (1969) Toxicity and related physiological activity of phenolic substances of plant origin. J Agric Food Chem 17:497–512

    Google Scholar 

  • Singleton VL, Kratzer FH (1973) Plant phenolics. In: Toxicants occurring naturally in foods. National Academy of Sciences, Washington DC, p 309–345

    Google Scholar 

  • Smart WWG, Bell TA, Stanley NW, Cope WA (1961) Inhibition of rumen cellulase by an extract from sericea forage. J Dairy Sci 44:1945–1946

    Google Scholar 

  • Smith D, Paulsen GM, Raguse CA (1964) Extraction of total available carbohydrates from grass and legume tissue. Plant Physiol 39:960–962

    Google Scholar 

  • Soest PJ van (1964) Symposium on nutrition and forage and pastures: new chemical procedures for evaluating forages. J Anim Sci 23:838–845

    Google Scholar 

  • Struhsaker TT (1975) The red colobus. Univ Chicago Press, Chicago

    Google Scholar 

  • Sumere CF van, Albrecht J, Dodonder A, Pooter H de, Pe I (1975) Plant proteins and phenolics. In: Harborne JB (ed) Chemistry and biochemistry of plant proteins. Academic Press, London, p 211–264

    Google Scholar 

  • Swain T (1979) Tannins and lignins. In: Rosenthal G, Janzen DH (eds) Interrelationships of secondary plant constituents with herbivores. Academic Press, New York, p 657–682

    Google Scholar 

  • Tagari H, Henis Y, Tamir M, Volcani R (1965) Effect of carob pod extract on cellulolysis, proteolysis, deamination and protein biosynthesis in an artificial rumen. Appl Microbiol 13:437–442

    Google Scholar 

  • Waterman PG (1973) Alkaloids and triterpenes from the African Toddalioideae. Biochem Syst Ecol 1:153–161

    Google Scholar 

  • Waterman PG, Meshal IA, Hall JB, Swaine MD (1978) Biochemical systematics and ecology of the Toddalioideae in the central part of the west African forest zone. Biochem Syst Ecol 6:239–245

    Google Scholar 

  • Westermarck H (1959) Digitalis inactivation in vitro due to rumen microbes from the sheep. Acta et Scand 1:67–73

    Google Scholar 

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Authors and Affiliations

  1. Phytochemistry Research Laboratory, Department of Pharmaceutical Chemistry, University of Strathclyde, G1 1XW, Glasgow, Scotland, United Kingdom

    Peter G. Waterman & Christiana N. Mbi

  2. Primate Ecology Unit, Wisconsin Regional Primate Research Center, University of Wisconsin, 53706, Madison, Wisconsin, USA

    Doyle B. McKey & J. Stephen Gartlan

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  1. Peter G. Waterman
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  2. Christiana N. Mbi
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  3. Doyle B. McKey
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  4. J. Stephen Gartlan
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Publication 19-013 of the Wisconsin Regional Primate Research Center

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Waterman, P.G., Mbi, C.N., McKey, D.B. et al. African rainforest vegetation and rumen microbes: Phenolic compounds and nutrients as correlates of digestibility. Oecologia 47, 22–33 (1980). https://doi.org/10.1007/BF00541771

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