Abstract
Cistus ladanifer L. is a shrub present in Mediterranean areas without major use, but which can be incorporated into ruminant diets, improving the digestive efficiency of dietary protein and product quality. The high levels of plant secondary metabolites, including condensed tannins, may be responsible for the beneficial properties of the plant, but can also reduce palatability. In this study, C. ladanifer was incorporated into lambs’ diets, either as aerial parts or as a condensed tannin extract, reaching 1.25% and 2.5% of condensed tannins of dry matter. Saliva was collected and electrophoretic profiles of both whole saliva and saliva after in vitro incubation with C. ladanifer tannins were compared. Animals receiving the aerial parts of C. ladanifer decreased feed ingestion. Differences in salivary protein profiles were observed for animals fed with the higher levels of aerial parts of the plant (CL2.5 group). Most of the lambs’ salivary proteins were present in the precipitate formed after tannin-saliva incubation, and one of the bands increased in CL2.5 group was present in high proportion in the precipitate. None of the protein bands stained pink with Coomassie Brilliant Blue, suggesting the absence, or low amounts, of proline-rich proteins in lamb saliva. The results suggest that the aerial parts of C. ladanifer are poor in palatability and that salivary proteins from lambs, due to their affinity for this plant’s secondary metabolites, can contribute to this. Further protein identification is needed, as well as studies to access the stability of the tannin-protein complexes through the gastrointestinal tract.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alonso-Díaz MA, Torres-Acosta JFJ, Sandoval-Castro CA, Capetillo-Leal CM (2012) Amino acid profile of the protein from whole saliva of goats and sheep and its interaction with tannic acid and tannins extracted from the fodder of tropical plants. Small Rumin Res 103:69–74. https://doi.org/10.1016/j.smallrumres.2011.10.020
Austin PJ, Suchar LA, Robbins CT, Hagerman AE (1989) Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. J Chem Ecol 15:1335–1347. https://doi.org/10.1007/BF01014834
Beeley JA, Sweeney D, Lindsay JC et al (1991) Sodium dodecyl sulphate-polyacrylamide gel electrophoresis of human parotid salivary proteins. Electrophoresis 12:1032–1041. https://doi.org/10.1002/elps.1150121207
Brudzynski K, Maldonado-Alvarez L (2015) Polyphenol-protein complexes and their consequences for the redox activity, structure and function of honey. A current view and new hypothesis—a review. Polish J Food Nutr Sci 65:71–80
Clauss M, Gehrke J, Hatt JM et al (2005) Tannin-binding salivary proteins in three captive rhinoceros species. Comp Biochem Physiol A Mol Integr Physiol. https://doi.org/10.1016/j.cbpb.2004.11.005
da Costa G, Lamy E, Capela e Silva F et al (2008) Salivary amylase induction by tannin-enriched diets as a possible countermeasure against tannins. J Chem Ecol 34:376–387. https://doi.org/10.1007/s10886-007-9413-z
Dentinho MTP, Belo AT, Bessa RJB (2014) Digestion, ruminal fermentation and microbial nitrogen supply in sheep fed soybean meal treated with Cistus ladanifer L. tannins. Small Rumin Res. https://doi.org/10.1016/j.smallrumres.2014.02.012
Francisco A, Dentinho MT, Alves SP et al (2015) Growth performance, carcass and meat quality of lambs supplemented with increasing levels of a tanniferous bush (Cistus ladanifer L.) and vegetable oils. Meat Sci. https://doi.org/10.1016/j.meatsci.2014.10.014
Frazão DF, Raimundo JR, Domingues JL et al (2018) Cistus ladanifer (Cistaceae): a natural resource in Mediterranean-type ecosystems. Planta 247:289–300
Guerreiro O, Alves SP, Costa M et al (2016a) Effects of extracts obtained from Cistus ladanifer L on in vitro rumen biohydrogenation. Anim Feed Sci Technol. https://doi.org/10.1016/j.anifeedsci.2016.06.024
Guerreiro O, Dentinho MTP, Moreira OC et al (2016b) Potential of Cistus ladanifer L. (rockrose) in small ruminant diets—effect of season and plant age on chemical composition, in vitro digestibility and antioxidant activity. Grass Forage Sci 71:437–447
Hofmann RR, Streich WJ, Fickel J et al (2008) Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species. J Morphol 269:240–257. https://doi.org/10.1002/jmor.10580
Horne J, Hayes J, Lawless HT (2002) Turbidity as a measure of salivary protein reactions with astringent substances. Chem Senses. https://doi.org/10.1093/chemse/27.7.653
Jerónimo E, Alves SP, Dentinho MTP et al (2010) Effect of grape seed extract, Cistus ladanifer L., and vegetable oil supplementation on fatty acid composition of abomasal digesta and intramuscular fat of lambs. J Agric Food Chem. https://doi.org/10.1021/jf1021626
Jerónimo E, Alfaia CMM, Alves SP et al (2012) Effect of dietary grape seed extract and Cistus ladanifer L. in combination with vegetable oil supplementation on lamb meat quality. Meat Sci. https://doi.org/10.1016/j.meatsci.2012.07.011
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0
Lamy E, da Costa G, Santos R et al (2009) Sheep and goat saliva proteome analysis: a useful tool for ingestive behavior research? Physiol Behav 98:393–401. https://doi.org/10.1016/j.physbeh.2009.07.002
Lamy E, Graça G, da Costa G et al (2010) Changes in mouse whole saliva soluble proteome induced by tannin-enriched diet. Proteome Sci 8:65. https://doi.org/10.1186/1477-5956-8-65
Lamy E, da Costa G, Santos R et al (2011) Effect of condensed tannin ingestion in sheep and goat parotid saliva proteome. J Anim Physiol Anim Nutr (Berl) 95:304–312. https://doi.org/10.1111/j.1439-0396.2010.01055.x
Naumann HD, Tedeschi LO, Zeller WE, Huntley NF (2017) The role of condensed tannins in ruminant animal production: advances, limitations and future directions. Rev Bras Zootec 46:929–949
Pech-Cervantes AA, Ventura-Cordero J, Capetillo-Leal CM et al (2016) Relationship between intake of tannin-containing tropical tree forage, PEG supplementation, and salivary haze development in hair sheep and goats. Biochem Syst Ecol. https://doi.org/10.1016/j.bse.2016.07.003
Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163. https://doi.org/10.1007/s10886-006-9077-0
Strumeyer DH, Malin MJ (1975) Condensed tannins in grain sorghum: isolation, fractionation, and characterization. J Agric Food Chem. https://doi.org/10.1021/jf60201a019
Vargas-Magaña JJ, Aguilar-Caballero AJ, Torres-Acosta JFJ et al (2013) Tropical tannin-rich fodder intake modifies saliva-binding capacity in growing sheep. Animal 7:1921–1924. https://doi.org/10.1017/S1751731113001651
Acknowledgements
This manuscript is funded by FEDER funding through the Alentejo2020 programme, with financial support for the project ‘CistusRumen—Sustainable use of Rockrose (Cistus ladanifer L.) in small ruminants—Increase of the competitiveness and reduction of the environmental impact’ (ALT20-03-0145-FEDER-000023), Operational Programme for Competitiveness Factors-COMPETE and national funding through the FCT—Foundation for Science and Technology under the project UID/AGR/00115/2013 (ICAAM—University of Évora). The authors also acknowledge the financial support from the FCT in the form of Elsa Lamy’s FCT investigator contract IF/01778/2013 and Olinda Guerreiro’s research grant (SFRH/BD/84406/2012).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lamy, E., Rodrigues, L., Guerreiro, O. et al. Changes in salivary protein composition of lambs supplemented with aerial parts and condensed tannins: extract from Cistus ladanifer L.—a preliminary study. Agroforest Syst 94, 1501–1509 (2020). https://doi.org/10.1007/s10457-019-00386-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10457-019-00386-4