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No Major Role for Binding by Salivary Proteins as a Defense Against Dietary Tannins in Mediterranean Goats

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Abstract

We investigated whether Mediterranean goats use salivary tannin-binding proteins to cope with tannin-rich forages by determining the affinity of salivary or parotid gland proteins for tannic acid or quebracho tannin. Mixed saliva, sampled from the oral cavity, or parotid gland contents were compared to the intermediate affinity protein bovine serum albumin with a competitive binding assay. Goats that consume tannin-rich browse (Damascus) and goats that tend to avoid tannins (Mamber) were sequentially fed high (Pistacia lentiscus L.), low (vetch hay), or zero (wheat hay) tannin forages. Affinity of salivary proteins for tannins did not differ between goat breeds and did not respond to presence or absence of tannins in the diet. Proteins in mixed saliva had slightly higher affinity for tannins than those in parotid saliva, but neither source contained proteins with higher affinity for tannins than bovine serum albumin. Similarly, 3 months of browsing in a tannin-rich environment had little effect on the affinity of salivary proteins for tannin in adult goats of either breed. We sampled mixed saliva from young kids before they consumed forage and after 3 months of foraging in a tannin-rich environment. Before foraging, the saliva of Mamber kids had higher affinity for tannic acid (but not quebracho tannin) than the saliva of Damascus kids, but there was no difference after 3 months of exposure to tannin-rich browse, and the affinity of the proteins was always similar to the affinity of bovine serum albumin. Our results suggest there is not a major role for salivary tannin-binding proteins in goats. Different tendencies of goat breeds to consume tannin-rich browse does not appear be related to differences in salivary tannin-binding proteins.

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References

  • AUSTIN, P. J., SUCHAR, L. A., ROBBINS, C. T., and HAGERMAN, A. E. 1989. Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. J. Chem. Ecol. 15:1335–1346.

    Article  CAS  Google Scholar 

  • BENNICK, A. 2002. Interaction of plant polyphenols with salivary proteins. Crit. Rev. Oral Biol. Med. 13:184–196.

    Article  PubMed  Google Scholar 

  • CLAUSS, M., LASON, K., GEHRKE, J., LERCHNER-DOLL, M., FICKEL, J., GRUHN, T., and STREICH, W. J. 2003. Captive roe deer (Capreolus capreolus) select for low amounts of tannic acid but not quebracho: fluctuations of preferences and potential benefits. Comp. Biochem. Physiol., B 136:369–382.

    Article  Google Scholar 

  • CLAUSS, M., GEHRKE, J., HATT, J. M., DIERENFELD, E. S., FLACH, E. J., HARMES, R., CASTELL, J., STREICH, J., and FICKEL, L. 2005. Tannin-binding salivary proteins in three captive rhinoceros species. Comp. Biochem. Physiol., A 140:67–72.

    Article  Google Scholar 

  • DEARING, M. D., FOLEY, W. J., and McLEAN, S. 2005. The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu. Rev. Ecol. Evol. Systemat. 36:169–189.

    Article  Google Scholar 

  • DECANDIA, M., SITZIA, M., CABIDDU, A., KABABYA, D., and 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 

  • DISTEL, R. A., and PROVENZA, F. D. 1991. Experience early in life affects voluntary intake of blackbrush by goats. J. Chem. Ecol. 17:431–450.

    Article  Google Scholar 

  • FICKEL, J., GORITZ, F., JOEST, B. A., HILDEBRANDT, T., HOFMANN, R. R., and BREVES, G. 1998. Analysis of parotid and mixed saliva in Roe deer (Capreolus capreolus L.). J. Comp. Physiol. (B) 168:257–264.

  • FICKEL, J., PITRA, C., JOEST, B. A., and HOFMANN, R. R. 1999. A novel method to evaluate the relative tannin-binding capacities of salivary proteins. Comp. Biochem. Physiol., C 122:225–229.

    CAS  Google Scholar 

  • GHO, F., PENA-NEIRA, A., and LOPEZ-SOLIS, R. O. 2006. Induction of salivary polypeptides associated with parotid hypertrophy by gallotannins administered topically into the mouse mouth. J. Cell. Biochem. 100:487–498.

    Article  Google Scholar 

  • GLASSER, T. A. 2009. Maternal and breed effects on the consumption of Pistacia lentiscus by domestic goats: a fecal NIRS aided study. Ph.D. dissertation. The Hebrew University of Jerusalem.

  • GLASSER, T. A., LANDAU, S., UNGAR, E. D., PEREVOLOTSKY, A., DVASH, L., MUKLADA, H., KABABYA, D., and WALKER, J. W. 2008. A fecal near-infrared reflectance spectroscopy-aided methodology to determine goat dietary composition in a Mediterranean shrubland. J. Anim. Sci. 86:1345–1356.

    Article  CAS  PubMed  Google Scholar 

  • HAGERMAN, A. E., and ROBBINS, C. T. 1993. Specificity of tannin-binding salivary proteins relative to diet selection by mammals. Can. J. Zool. 71:628–633.

    Article  CAS  Google Scholar 

  • ICACG 1994. Israel Council on Animal Care Guidelines: Legislation on Animal Welfare (defending animal rights). Paragraph 14. Knesset Law Pub., Jerusalem, Israel (in Hebrew).

  • KABABYA, D., PEREVOLOTSKY, A., BRUCKENTAL, I., and LANDAU, S. 1998. Selection of diets by dual-purpose Mamber goats in Mediterranean woodland. J. Agric. Sci., Camb. 131:221–228.

    Article  Google Scholar 

  • LAMY, E., DA COSTA, G., SILVA, F. C. E., POTES, J., COELHO, A. V., and BAPTISTA, E. S. 2008. Comparison of electrophoretic protein profiles from sheep and goat parotid saliva. J. Chem. Ecol. 34:388–397.

    Article  CAS  PubMed  Google Scholar 

  • LANDAU, S., SILANIKOVE, N., NITSAN, Z., BARKAI, D., BARAM, H., PROVENZA, F. D., and PEREVOLOTSKY, A. 2000. Short-term changes in eating patterns explain the effects of condensed tannins in heifers. Appl. Anim. Behav. Sci. 69:199–213.

    Article  PubMed  Google Scholar 

  • LANDAU, S. Y., PEREVOLOTSKY, A., KABABYA, D., SILANIKOVE, N., NITSAN, R., BARAM, H., and PROVENZA, F. D. 2002. Polyethylene glycol affects goats’ feeding behavior in a tannin-rich environment. J. Range Manage. 55:598–603.

    Article  Google Scholar 

  • LANDAU, S., DVASH, L., DECANDIA, M., CABIDDU, A., SHAPIRO, F., MOLLE, G., and SILANIKOVE, N. 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  CAS  PubMed  Google Scholar 

  • LANDAU, S., GLASSER, T., MUKLADA, H., DVASH, L., PEREVOLOTSKY, A., UNGAR, E. D., and WALKER, J. W. 2005. Fecal NIRS prediction of dietary protein percentage and in vitro dry matter digestibility in diets ingested by goats in Mediterranean scrubland. Small Rumin. Res. 59:251–263.

    Article  Google Scholar 

  • LYMAN, T. D., PROVENZA, F. D., and VILLALBA, J. J. 2008. Sheep foraging behavior in response to interactions among alkaloids, tannins and saponins. J. Sci. Food Agric. 88:824–831.

    Article  CAS  Google Scholar 

  • MAKKAR, H. P. S., and BECKER, K. 1998. Adaptation of cattle to tannins: role of proline-rich proteins in oak-fed cattle. Anim. Sci. 67:277–281.

    CAS  Google Scholar 

  • MEHANSHO, H., HAGERMAN, A., CLEMENTS, S., BUTLER, L., ROGLER, J., and CARLSON, D. M. 1983. Modulation of proline-rich protein biosynthesis in rat parotid glands by sorghums with high tannin levels. Proc. Natl. Acad. Sci. USA 80:3948–3952.

    Article  CAS  PubMed  Google Scholar 

  • MOTE, T. E., VILLALBA, J. J., and PROVENZA, F. D. 2008. Sequence of food presentation influences intake of foods containing tannins and terpenes. Appl. Anim. Behav. Sci. 113:57–68.

    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 

  • ODENYO, A. A., McSWEENEY, C. S., PALMER, B., NEGGASA, D., and OSUJI, P. O. 1999. In vitro screening of rumen fluid samples from indigenous African ruminants provides evidence for rumen fluid with superior capacities to digest tannin-rich fodders. Aust. J. Agric. Res. 50:1147–1157.

    Article  CAS  Google Scholar 

  • RAUTIO, P., BERGVALL, U. A., KARONEN, M., and SALMINEN, J. P. 2007. Bitter problems in ecological feeding experiments: Commercial tannin preparations and common methods for tannin quantifications. Biochem. Syst. Ecol. 35: 257–262.

    Article  CAS  Google Scholar 

  • ROMANI, A., PINELLI, P., GALARDI, C., MULINACCI, N., and TATTINI, M. 2002. Identification and quantification of galloyl derivatives, flavonoid glycosides and anthocyanins in leaves of Pistacia lentiscus L. Phytochem. Anal. 13:79–86.

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute Inc. 1989. SAS/STAT Guide. Release 6.12. SAS Inst, Cary.

    Google Scholar 

  • SHIMADA, T. 2006. Salivary proteins as a defense against dietary tannins. J. Chem. Ecol. 32:1149–1163.

    Article  CAS  PubMed  Google Scholar 

  • SILANIKOVE, N., GILBOA, N., PEREVOLOTSKY, A., and NITSAN, Z. 1996a. Goats fed tannin-containing leaves do not exhibit toxic syndromes. Small Rumin. Res. 21:195–201.

    Article  Google Scholar 

  • SILANIKOVE, N., GILBOA, N., NIR, I., PEREVOLOTSKY, A., and NITZAN, Z. 1996b. 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 

  • SMITH, P. K., KROHN, R. I., HERMANSON, G. T., MALLIA, A. K., GARTNER, F. H., PROVENZANO, M. D., FUJIMOTO, E. K., GOEKE, N. M., OLSON, B. J., and KLENK, D. C. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76–85.

    Article  CAS  PubMed  Google Scholar 

  • TITUS, C. H., PROVENZA, F. D., PEREVOLOTSKY, A., and SILANIKOVE, N. 2000. Preferences for foods varying in macronutrients and tannins by lambs supplemented with polyethylene glycol. J. Anim. Sci. 78:1443–1449.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by Research Grant No. IS-3555-04 from BARD, the United States—Israel Binational Agricultural Research and Development Fund. ARO Publication no. 107/10.

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Authors and Affiliations

  1. Department of Agronomy and Natural Resources, Institute of Plant Sciences, Agricultural Research Organization, P.O. Box 6, Bet Dagan, 50250, Israel

    Michal Hanovice-Ziony, Serge Yan Landau, Eugene David Ungar, Hussein Muklada, Tzach Aharon Glasser & Avi Perevolotsky

  2. Department of Food Sciences, Institute of Technology and Storage of Agricultural Products, Agricultural Research Organization, P.O. Box 6, Bet Dagan, 50250, Israel

    Nathan Gollop

  3. Texas A&M University Agricultural Research and Extension Center, 7887 U.S. Hwy. 87 N., San Angelo, TX, 76901, USA

    John Withers Walker

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  1. Michal Hanovice-Ziony
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  2. Nathan Gollop
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  3. Serge Yan Landau
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  4. Eugene David Ungar
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  5. Hussein Muklada
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Correspondence to Serge Yan Landau.

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Hanovice-Ziony, M., Gollop, N., Landau, S.Y. et al. No Major Role for Binding by Salivary Proteins as a Defense Against Dietary Tannins in Mediterranean Goats. J Chem Ecol 36, 736–743 (2010). https://doi.org/10.1007/s10886-010-9809-z

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  • DOI: https://doi.org/10.1007/s10886-010-9809-z

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