Tannins in tropical tree fodders fed to small ruminants: A friendly foe?

Small Ruminant Research

Volumn 89, Issue 2-3, 2010, Pages 164-173

  Alonso Diaz M A ^a,b   Torres Acosta, J F J ^a   Sandoval Castro, C A ^a   Hoste, H ^c,d  

^a UNIVERSIDAD AUTÓNOMA DE YUCATÁN   (Mexico)

^b Centro de Enseñanza Investigación y Extensión en Ganadería Tropical   (Mexico)

^c IHAP   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Adaptive mechanisms; Goats; Nematodes; Preference; Saliva; Sheep; Tannins

Indexed keywords

ANIMALIA; BOVIDAE; CAPRA HIRCUS; NEMATODA; OVIS ARIES;

EID: 77950517410     PISSN: 09214488     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smallrumres.2009.12.040     Document Type: Article

References (81)

1. Ademola I.O., Akanbi A.I., and Idowu S.O. Comparative nematodicidal activity of chromatographic fractions of Leucaena leucocephala seed against gastrointestinal sheep nematodes. Pharm. Biol. 43 (2005) 599-604
2. Ademola I.O., and Idowu S.O. Anthelmintic activity of Leucaena leucocephala seed extract on Haemonchus contortus-infective larvae. Vet. Rec. 158 (2006) 485-486
3. Akkari H., Ben Salem H., Gharbi M., Abidi S., and Darghouth M.A. Feeding Acacia cyanophylla Lindl. foliage to Barbarine lambs with or without PEG: effect on the excretion of gastro-intestinal nematode eggs. Anim. Feed Sci. Technol. 147 (2008) 182-192
4. Akkari H., Darghouth M.A., and Ben Salem H. Preliminary investigations of the anti-nematode activity of Acacia cyanophylla Lindl.: excretion of gastrointestinal nematode eggs in lambs browsing A. cyanophylla with and without PEG or grazing native grass. Small Rumin. Res. 74 (2008) 78-83
5. Alonso-Díaz M.A., Torres-Acosta J.F.J., Sandoval-Castro C.A., Hoste H., Aguilar-Caballero A.J., and Capetillo-Leal C.M. Is goats' preference of forage trees affected by their tannin or fiber content when offered in cafeteria experiments?. Anim. Feed Sci. Technol. 141 (2008) 36-48
6. Alonso-Díaz M.A., Torres-Acosta J.F.J., Sandoval-Castro C.A., Aguilar-Caballero A.J., and Hoste H. In vitro larval migration and kinetics of exsheathment of Haemonchus contortus exposed to four tropical tanniniferous plants. Vet. Parasitol. 153 (2008) 313-319
7. Alonso-Díaz M.A., Torres-Acosta J.F.J., Sandoval-Castro C.A., Capetillo-Leal C., Brunet S., and Hoste H. Effects of four tropical tanniniferous plants on the inhibition of larval migration and the exsheathment process of Trichostrongylus colubriformis infective stage. Vet. Parasitol. 153 (2008) 187-192
8. Alonso-Díaz M.A., Torres-Acosta J.F.J., Sandoval-Castro C.A., Hoste H., Aguilar-Caballero A.J., and Capetillo-Leal C.M. Preference of tanniniferous tree fodder offered to sheep and its relationship with in vitro gas production and digestibility. Anim. Feed Sci. Technol. 151 (2009) 75-85
9. Alonso-Díaz M.A., Torres-Acosta J.F.J., Sandoval-Castro C., Canul-Ku L., and Hoste H. Intake of tropical tanniniferous plants by goats and sheep when offered as a sole feed. Trop. Subtrop. Agroecosyst. 11 (2009) 255-258
10. Asano K., Shinagawa K., and Hashimoto N. Characterization of haze forming proteins of beer and their roles in chill haze formation. J. Am. Soc. Brew. Chem. 40 (1982) 147-154
11. Athanasiadou S., Githiori J., and Kyriazakis I. Medicinal plants for helminth parasite control: facts and fiction. Animal 1 (2007) 1392-1400
12. Austin P.J., Suchar L.A., Robbins C.T., and Hagerman A.E. Tannin binding proteins in the saliva of deer and their absence in the saliva of sheep and cattle. J. Chem. Ecol. 15 (1989) 1335-1347
13. Ayala-Burgos A., Cetina-Góngora R., Capetillo-Leal C., Zapata-Campos C., and Sandoval-Castro C. Composición química-nutricional de árboles forrajeros. Compilación de análisis del laboratorio de nutrición animal. UADY-FMVZ. Yucatán, México (2006)
14. Baraza E., Villalba J.J., and Provenza F.D. Nutritional context influences preferences of lambs for foods with plant secondary metabolites. Appl. Anim. Behav. Sci. 92 (2005) 293-305
15. Behnke, J.M., Buttle, D.J., Stepek, G., Lowe, A., Duce, I.R., 2008. Developing new anthelmintics from plant cysteine proteinases. Parasite and vectors, 1: 29, DOI: 10.1186/1756-3305r-r1-29.
16. Ben Salem H., Ben Salem I., Nefzaoui A., and Ben Saïd M.S. Effect of PEG and olive cake feed blocks supply on feed intake, digestion, and health of goats given kermes oak (Quercus coccifera L.) foliage. Anim. Feed Sci. Technol. 110 (2003) 45-59
17. Ben Salem H., Nefzaoui A., Makkar H.P.S., Hochlef H., Ben Salem I., and Ben Salem L. Effect of early experience and adaptation period on voluntary intake, digestion, and growth in Barbarine lambs given tannin-containing (Acacia cyanophylla Lindl. foliage) or tannin free (oaten hay) diets. Anim. Feed Sci. Technol. 122 (2005) 59-77
18. Brunet S., and Hoste H. Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. J. Agric. Food Chem. 54 (2006) 7481-7487
19. Brunet S., Martinez-Ortiz de Montellano C., Torres-Acosta J.F.J., Sandoval-Castro C.A., Aguilar-Caballero C.A., Capetillo-Leal C., and Hoste H. Effect of the consumption of Lysiloma latisiliquum on the larval establishment of gastrointestinal nematodes in goats. Vet. Parasitol. 157 (2008) 81-88
20. Cenci F.B., Louvandini H., McManus C.M., DelľPorto A., Costa D.M., Araújo S.C., Minho A.P., and Abdalla A.L. Effects of condensed tannin from Acacia mearnsii on sheep infected naturally with gastrointestinal helminths. Vet. Parasitol. 144 (2007) 132-137
21. Clauss M., Gehrke J., Hatt J.M., Dierenfeld E.S., Flach E.J., Hermes R., Castell J., Streich W.J., and Fickel J. Tannin-binding salivary proteins in three captive rhinoceros species. Comp. Biochem. Physiol. Physiol. 140 (2005) 67-72
22. Costa C.T.C., Morais S.M., Bevilaqua C.M.L., Souza M.M.C., and Leite F.K.A. Efeito ovicida de extratos de sementes de Mangifera indica l. sobre Haemonchus contortus. Rev. Bras. Parasitol. Vet. 11 (2002) 57-60
23. Costa G., Lamy E., Capela e Silva F., Andersen J., Sales Baptista E., and Coelho A. Salivary amylase induction by tannin-enriched diets as a possible countermeasure against tannins. J. Chem. Ecol. 34 (2008) 376-387
24. Duncan A.J., Ginane C., Gordon I.J., and Orkov E.R. Why do herbivores select mixed diets?. Proceedings of VI International Symposium on the Nutrition of Herbivores. Mérida, Yucatán, México, October 19-24, 2003 (2003)
25. El-Meccawi S., Kam M., Brosh A., and Degen A.A. Heat production and energy balance of sheep and goats fed sole diets of Acacia saligna and Medicago sativa. Small Rumin. Res. 75 (2008) 199-203
26. Flores S.J., Vermont-Ricalde M.R., and Kantún-Balam M.J. Leguminosae diversity in the Yucatan Peninsula and its importance for sheep and goats feeding. In: Sandoval-Castro C.A., Hovell F.D.De.B., Torres-Acosta J.F.J., and Ayala-Burgos A. (Eds). Herbivores: The Assessment of Intake, Digestibility and The Roles of Secondary Compounds (2006), Nottingham University Press, Nottingham 291-299
27. Food and Agriculture Organization (FAO), 2008. World Agriculture: Toward 2015/2030 (http://www.fao.org/docrep/004/y3557e/y3557e03.htm).
28. Hadjigeorgiou I.E., Gordon I.J., and Milne J.A. Comparative preference by sheep and goats for gramineae forages varying in chemical composition. Small Rumin. Res. 49 (2003) 147-156
29. Heckendorn F., Häring D.A., Maurer V., Zinsstag J., Langhans W., and Hertzberg H. Effect of sainfoin (Onobrychis viciifolia) silage and hay on established populations of Haemonchus contortus and Cooperia curticei in lambs. Vet. Parasitol. 142 (2006) 293-300
30. Hernández-Orduño G., Torres-Acosta J.F.J., Sandoval-Castro C.A., and Aguilar-Caballero A. Polyethylene glycol (PEG) did not modify preference for tanniniferous plants in cafeterial trials of sheep and goats with browsing experience. Proceedings of the 9th International Conference on Goats. Queretaro, Mexico (2008) 194
31. 3 larvae. Trop. Subtrop. Agroecosyst. 8 (2008) 191-197
32. Horne J., Hayes J., and Lawless H.T. Turbidity as a measure of salivary protein reactions with astringent substances. Chem. Senses 27 (2002) 653-659
33. Hoste H., Gaillard L., and Le Frileux Y. Consequences of the regular distribution of sainfoin hay on gastrointestinal parasitism with nematodes and milk production in dairy goats. Small Rumin. Res. 59 (2005) 265-271
34. Hoste H., Jackson F., Athanasiadou S., Thamsborg S.M., and Hoskin S.O. The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol. 22 (2006) 253-261
35. Hoste H., Torres-Acosta J.F., Alonso-Díaz M.A., Brunet S., Sandoval-Castro C., and Houzangbe-Adote S. Identification and validation of bioactive plants for the control of gastrointestinal nematodes in small ruminants. Trop. Biomed. 25 (2008) 56-72
36. Houzangbe-Adote S.M., Paolini V., Fouraste I., Moutairou K., and Hoste H. In vitro effects of four tropical plants on the intestinal parasitic nematode, Trichostrongylus colubriformis. J. Helminthol. 79 (2005) 29-33
37. Houzangbe-Adote S.M., Paolini V., Fouraste I., Moutairou K., and Hoste H. In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Res. Vet. Sci. 78 (2005) 155-160
38. Iason G. The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc. Nutr. Soc. 64 (2005) 123-131
39. Iason R.G., and Villalba J.J. Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. J. Chem. Ecol. 32 (2006) 1115-1132
40. Kabasa J.D., Opuda-Asibo J., and Meulen U. The effect of oral administration of polyethylene glycol on faecal helminth egg counts in pregnant grazed on browse containing condensed tannins. Trop. Anim. Health Prod. 32 (2000) 73-86
41. Kahiya C., Mukaratirwa S., and Thamsborg S.M. Effects of Acacia nilotica and Acacia karoo diets on Haemonchus contortus infection in goats. Vet. Parasitol. 115 (2003) 265-274
42. Lange K.C., Olcott D.D., Miller J.E., Mosjidis J.A., Terrill T.H., Burke J.M., and Kearney M.T. Effect of sericea lespedeza (Lespedeza cuneata) fed as hay, on natural and experimental Haemonchus contortus infections in lambs. Vet. Parasitol. 141 (2006) 273-278
43. Maciel M.V., Morais S.M., Bevilaqua C.M.L., Camurça-Vasconcelos A.L.F., Costa C.T.C., and Castro C.M.S. Ovicidal and larvicidal activity of Melia azedarach extracts on Haemonchus contortus. Vet. Parasitol. 140 (2006) 98-104
44. Makkar H.P.S. Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Rumin. Res. 49 (2003) 241-256
45. Mantz G.K., Villalba J.J., and Provenza F.D. Supplemental polyethylene glycol affects intake of and preference for sericea lespedeza by cattle. J. Anim. Sci. 87 (2009) 761-769
46. Min B.R., and Hart S.P. Tannins for suppression of internal parasites. J. Anim. Sci. 81 E. Suppl. 2 (2003) E102-E109
47. Minho A.P., Bueno I.C.S., Louvandini H., Jackson F., Gennari S.M., and Abdalla A.L. Effect of Acacia molissima tannin extract on the control of gastrointestinal parasites in sheep. Anim. Feed Sci. Technol. 147 (2007) 172-181
48. Molan A.L., Alexander R.A., Brookes I.M., and McNabb W.C. Effect of an extract from sulla (Hedysarum coronarium) containing condensed tannins on the migration of three sheep gastrointestinal nematodes in vitro. Proc. NZ Soc. An. 60 (2000) 21-25
49. Molan A.L., Warghorn G.C., and McNabb W.C. Effect of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro. Vet. Rec. 150 (2002) 65-69
50. Mote T.E., Villalba J.J., and Provenza F.D. Relative availability of tannin- and terpene-containing foods affects food intake and preference by lambs. J. Chem. Ecol. 33 (2007) 1197-1206
51. Mueller-Harvey I. Unravelling the conundrum of tannins in animal nutrition and health. J. Sci. Food Agric. 86 (2006) 2010-2037
52. Niezen J.H., Robertson H.A., and Waghorn G.C. Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Vet. Parasitol. 80 (1998) 15-27
53. Osoro K., Mateos-Sanz A., Frutos P., García U., Ortega-Mora L.M., Ferreira L.M.M., Celaya R., and Ferre I. Anthelmintic and nutritional effects of heather supplementation on Cashmere goats grazing prennial ryegrass-white clover pastures. J. Anim. Sci. 85 (2007) 861-870
54. Paolini V., Dorchies P., and Hoste H. Effect of sainfoin hay on gastrointestinal nematode infections in goats. Vet. Rec. 152 (2003) 600-601
55. Paolini V., Fouraste I., and Hoste H. In vitro effects of three woody plant and sainfoin extracts on 3rd-stage larvae and adult worms of three gastrointestinal nematodes. Parasitology 129 (2004) 69-77
56. Papanastasis V.P., Yiakoulaki M.D., Decandia M., and Dini-Papanastasi O. Integrating woody species into livestock feeding in the Mediterranean areas of Europe. Anim. Feed Sci. Technol. 140 (2008) 1-17
57. Provenza F.D. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. J. Range Manage. 48 (1995) 2-17
58. Provenza F.D. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74 (1996) 2010-2020
59. Provenza F.D. Behavioral mechanisms influencing use of plants with secondary metabolitos by herbivores. In: Sandoval-Castro C.A., Hovell F.D.De.B., Torres-Acosta J.F.J., and Ayala-Burgos A. (Eds). Herbivores: The Assessment of Intake, Digestibility and The Roles of Secondary Compounds (2006), Nottingham University Press, Nottingham 183-195
60. Provenza F.D., Villalba J.J., Dziba L.E., Atwood S.B., and Banner R.E. Linking herbivore experience, varied diets, and plant biochemical diversity. Small Rumin. Res. 49 (2003) 257-274
61. Provenza F.D., Villalba J.J., Wiedmeier R.W., Lyman T., Owens J., Lisonbee L., Clemensen A., Welch K., Gardner D., and Lee S. Value of plant diversity for diet mixing and sequencing in herbivores. Rangelands 31 (2009) 45-49
62. Ramírez-Restrepo C.A., Barry T.N., Pomroy W.E., López-Villalobos N., McNabb W.C., and Kemp P.D. Use of Lotus corniculatus containing condensed tannins to increase summer lamb growth under commercial dry land farming conditions with minimal anthelmintic drench input. Anim. Feed Sci. Technol. 122 (2005) 197-217
63. Revaud, M.H.R., 2007. Impact des tannins condenses sur la consommation de plantes par les chevres au Yucatan (Mexique) (Thése pour le grade de Doctor Vétérinaire). Toulouse, France. Ecole Nationale Vétérinaire de Toulouse.
64. Rios G., and Riley J.A. Estudios preliminares sobre la producción caprina con dietas a base de ramoneo en monte bajo en la zona henequenera de Yucatán. I. Selección y valor nutritivo de plantas nativas. Trop. Anim. Prod. 10 (1985) 1-11
65. Rogosic J., Estell R.E., Skobic D., Martinovic A., and Maric S. Role of species diversity and secondary compound complemetarity on diet selection of Mediterranean shrubs by goats. J. Chem. Ecol. 32 (2006) 1279-1287
66. Rogosic J., Estell R.E., Ivankovic S., Kezic J., and Razov J. Potential mechanisms to increase shrub intake and performance of small ruminants in Mediterranean shrubby ecosystems. Small Rumin. Res. 74 (2008) 1-15
67. Rojas D.K., López J., Tejada I., Vásquez V., Shimada A., Sánchez D., and Ibarra F. Impact of condensed tannins from tropical forages on Haemonchus contortus burdens in Mongolian gerbils (Meriones unguiculatus) and Pelibuey lambs. Anim. Feed Sci. Technol. 128 (2006) 218-228
68. Sandoval-Castro C.A., Lizarraga-Sánchez H.L., and Solorio-Sánchez F.J. Assessment of tree fodder preference by cattle using chemical composition, in vitro gas production and in situ degradability. Anim. Feed Sci. Technol. 123-124 (2005) 277-289
69. Shimada T. Salivary proteins as a defence against dietary tannins. J. Chem. Ecol. 32 (2006) 1149-1163
70. Silanikove N., Landau S., Or D., Kababya D., Bruckental I., and Nitsan Z. Analytical approach and effects of condensed tannins in carob pods (Ceratonia siliqua) on feed intake, digestive and metabolic responses of kids. Livest. Sci. 99 (2006) 29-38
71. Skopec M.M., Hagerman A.E., and Karasov W.H. Do salivary proline-rich proteins counteract dietary hydrolysable tannin in laboratory rats?. J. Chem. Ecol. 30 (2004) 1679-1692
72. Sorensen S.J., McLister D.J., and Dearing M.D. Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology 86 (2005) 140-154
73. 14C-labelled condensed tannins in the gastrointestinal tract of sheep. Br. J. Nutr. 72 (1994) 467-477
74. Terrill T.H., Mosjidis J.A., Moore D.A., Shaik S.A., Miller J.E., Burke J.M., Muir J.P., and Wolfe R. Effect of pelleting on efficacy of Sericea lespedeza hay as a natural dewormer in goats. Vet. Parasitol. 146 (2007) 117-122
75. Terrill T.H., Dykes G.S., Shaik S.A., Miller J.E., Kouakou B., Kannan G., Burke J.M., and Mosjidis J.A. Efficacy of sericea lespedeza hay as a natural dewormer in goats: dose titration study. Vet. Parasitol. 163 (2009) 52-56
76. Titus C.H., Provenza F.D., Perevolotsky A., and Silanikove N. Preferences for foods varying in macronutrients and tannins by lambs supplemented with polyethylene glycol. J. Anim. Sci. 78 (2000) 1443-1449
77. Van Soest P.J. Nutritional Ecology of the Ruminant. 2nd ed. (1994), Cornell University Press, Ithaca, NY, USA
78. Villalba J.J., and Provenza F.D. Preference for polyethylene glycol by sheep fed a quebracho tannin diet. J. Anim. Sci. 79 (2001) 2066-2074
79. Villalba J.J., and Provenza F.D. Self-medication and homeostatic endeavor in herbivores: learning about the benefits of nature's pharmacy. Animal 1 (2007) 1360-1370
80. Villalba J.J., Provenza F.D., and Banner R.E. Influence of macronutrients and polyethylene glycol on intake of a quebracho tannin diet by sheep and goats. J. Anim. Sci. 80 (2002) 3154-3164
81. Waghorn G. Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production - Progress and challenges. Anim. Feed Sci. 147 (2008) 116-139