Author’s Accepted Manuscript Natural gastro properties of ficus natalensis, Rhuss natalensis and Harrisonia abyssinica in native east african goats Dorothy Kalule Nampanzira, John David Kabasa, Constantine Bakyusa Katongole, Sam Okello, John Robert Stephen Tabuti PII: S1871-1413(16)30024-5 DOI: http://dx.doi.org/10.1016/j.livsci.2016.02.001 Reference: LIVSCI2942 To appear in: Livestock Science Received date: 18 August 2014 Revised date: 4 February 2016 Accepted date: 5 February 2016 Cite this article as: Dorothy Kalule Nampanzira, John David Kabasa, Constantine Bakyusa Katongole, Sam Okello and John Robert Stephen Tabuti, Natural gastro properties of ficus natalensis, Rhuss natalensis and Harrisonia abyssinica in native east african goats, Livestock Science, http://dx.doi.org/10.1016/j.livsci.2016.02.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. www.elsevier.com/locate/livsci http://www.elsevier.com/locate/livsci http://dx.doi.org/10.1016/j.livsci.2016.02.001 http://dx.doi.org/10.1016/j.livsci.2016.02.001 1 Natural gastro properties of Ficus natalensis, Rhuss natalensis and Harrisonia abyssinica in 1 native East African goats 2 3 Dorothy Kalule Nampanzira 1* , John David Kabasa 2 Constantine Bakyusa Katongole 3 Sam 4 Okello 1 and John Robert Stephen Tabuti 4 , 5 6 1 Department of Livestock and Industrial Development, Makerere University P. O. Box 7062 7 Kampala, Uganda. 8 2 Department of Biosecurity, Ecosystems & Veterinary Public Health, Makerere University, P. O. 9 Box 7062, Kampala, Uganda 10 3 Department of Agricultural Production, Makerere University, P. O. Box 7062, Kampala, 11 Uganda 12 4 Department of Botany, Makerere University, P. O. Box 7062, Kampala, Uganda 13 *Corresponding Author: Department of Livestock and Industrial Development, Makerere 14 University P. O. Box 7062 Kampala, Uganda. Tel: +256-772-192997. Fax: +256-414-554685 / 15 534336. E-mail: dnampanzira@covab.mak.ac.ug / dnampanzira@gmail.com 16 17 Abstract 18 The natural gastro properties of Ficus natalensis, Rhuss natalensis and Harrisonia abyssinica 19 was evaluated with the objectives of determining the rumen degradation properties. Results 20 showed that H. abyssinica presented the highest DM disappearance from the nylon bags 21 throughout the different incubation times followed by F. natalensis and R. natalensis showed the 22 lowest. The DM readily available soluble fraction (a), insoluble but degradable fraction (b), 23 degradation rate (c), potential degradability (PD) and effective degradability (ED) differed 24 significantly (P<0.05) across the three browse species. The CP a, b, PD and ED fractions 25 differed significantly (P<0.05) across the three browse species. The CP c fraction was similar 26 across the browse species. The NDF a, b, PD, and ED fractions differed significantly (P<0.05) 27 across the browse species. The NDF c fraction was not different across the browse species. In 28 conclusion, Rhuss natalensis subsp. romantica has inferior rumen degradability properties, an 29 mailto:dnampanzira@covab.mak.ac.ug mailto:dnampanzira@gmail.com 2 indication of low nutritive value for goats compared to Harrisonia abyssinica subsp. abyssinica 30 and Ficus natalensis subsp. Natalensis. 31 Keywords: Browse species; Ficus natalensis; Harrisonia abyssinica; Rhuss natalensis; Rumen 32 degradability; 33 1. Introduction 34 Native browse species offer an opportunity to provide healthier meat as opposed to other feed 35 resources (Pearce et al., 2010). These browse plants are drought and disease resistant, readily 36 available in the communities and therefore build resilience for goat small holder farming 37 systems. 38 Goats are a suitable livestock for resource-poor farmers (Devendra, 2006) because they 39 require less space, less feed and low initial cost compared to large animals. Hence they have an 40 important role in ensuring food security, income generation and employment for the resource-41 poor (Peacock, 2005). Despite the positive role of goats to the socio-economic well-being of 42 resource-poor, the productivity of goats is low (Devendra, 2010). The low productivity of goats 43 is mainly attributed to poor nutrition, which is brought about by inadequate feed resources 44 especially during the dry conditions (Ben Salem and Smith, 2008). Leaves of browse plants have 45 been reported to have the potential to support goat production during periods of scarcity since 46 they maintain sufficient levels of protein (Yayneshet et al., 2009; Safari et al., 2011) even during 47 the dry season. This is because of their ability to remain green and hence maintain their 48 nutritional value long in the dry season (Safari et al., 2011). However, information on the natural 49 properties in the rumen of small ruminants of most locally available browse plants is inadequate. 50 In Uganda, several studies (Kabasa et al., 2004; Tabuti and Lye, 2009) have reported the 51 availability of browse plants such as F. natalensis, R. natalensis, H. abyssinica, Acacia 52 3 sieberiana, Acacia senegal etc. However, there is inadequate information on the natural gastro 53 properties of these browse plants. The available information is from other regions and is largely 54 limited to nutrient composition. The CP and NDF values for the browse plants reported by 55 Abdulrazak et al. (2000), Rubanza et al. (2005a, 2005b and 2006) Kendric et al. (2009), Nsahlai 56 et al. (2011) and Abebe et al. (2012) range between 53 – 238g/kg DM and 245 – 494g/kg DM, 57 respectively. A full understanding of the natural gastro properties of these browse plants would 58 afford the opportunity of a better and efficient utilisation of these locally available browse plants 59 to increase goat production in Uganda. The objective of this study was to determine the natural 60 gastro properties of F. natalensis, H. abyssinica and R. natalensis leaves as feed for indigenous 61 goats, through determining their rumen degradation properties. 62 63 2. Materials and methods 64 All the procedures performed in this study involving animals were in accordance with the 65 internationally accepted welfare standards for animal experimentation 66 2.1. Location and climate of the study area 67 This study was conducted in Buyende district, Uganda. The district is located between 1°14- 68 1°29N and 1°28- 33°16E at an altitude of 1,083 m above sea level. The area has a bimodal 69 rainfall pattern with March to May and September to November as the first and second rain 70 seasons respectively. The average annual rainfall is 1200 mm. The mean daily maximum and 71 minimum temperatures of the area are about 28 o C and 16 o Crespectively. 72 73 2.2 Collection of samples of browse species 74 4 Samples of browse species were collected from Kidera sub-county. Leaves were collected 75 from three browse speciesncn, namely F. natalensis, H. abyssinica and R. natalensis. The three 76 browse species are among the most common and preferred by farmers in the area. The leaves 77 were harvested during the dry (June - August) seasons. For each browse species, leaves were 78 harvested from at least 5 randomly selected trees. The leaves chosen contained all the categories, 79 since the goats eat all the leaves they come across regardless of their position (upper part, lower 80 part, close to the stem). The harvested leaves were bulked, thoroughly mixed and thereafter two 81 sub-samples were drawn. For each season, 4 samples were collected at intervals of 21 days. This 82 resulted in a total of 4 samples per browse species for the season. On each day of sample 83 collection, sampling started between 08:00 and 09:00 hours and lasted 30 minutes. After 84 collection, the samples were placed in plastic bags, sealed, labeled pending transportation to the 85 laboratory for weighing and oven drying. After oven drying (at 60 o C for 48 hours), the samples 86 were weighed and divided into two sub-samples: one for chemical analysis and the other for 87 rumen degradability determination. 88 89 2.2. Rumen DM degradability 90 The samples of each browse species from the dry season designated for rumen degradability 91 determination were bulked and ground using a 2mm screen. Two grams of the ground samples 92 were weighed in triplicate into labeled weighed nylon bags with a pore size of 36µ. Following 93 the recommendations of Osuji et al. (1993) the nylon bags were incubated in the rumens of three 94 fistulated mature indigenous ewes weighing 18kg (S.D. 1.0). The ewes were fitted with 95 permanent rumen cannulae with an internal diameter of 5cm. The ewes were left to graze freely 96 in a paddock containing mainly Commelina benghalensis, Panicum maximum and Digitaria 97 5 abyssinica. The ewes also had free access to clean drinking water and mineral licks on a daily 98 basis. The nylon bags were withdrawn at 3, 6, 12, 24, 48 and 72 hours after insertion. Using the 99 sequential addition method, 9 bags were incubated in the rumen of each ewe at a time. The 0 100 hour measurement was estimated by washing triplicate bags under clean running tap water until 101 the water squeezed out of them was colourless. Following removal from the rumen, the bags 102 were washed as described above and then oven dried at 60 o C for 48 hours and weighed 103 immediately. 104 Using the PROC NLIN procedure of SAS the DM degradation data was fitted to the 105 equation Y = a + b (1- e –c(t-lag time) ) (McDonald, 1981) to determine the degradation 106 characteristics (a,b,c and lag time); where Y is the DM degradation at time t, a the soluble 107 fraction of the feed (Zero intercept), b the slowly degradation, a + b the potential degradability 108 (PD) of the feed when time is not limited and c the rate of degradation of the slowly degradable 109 fraction. The effective degradability (ED) of the DM was calculated using the equation of AFRC 110 (1993), assuming a rumen out flow rate of 0.02 per hour. 111 112 2.4. Chemical analysis 113 The samples designated for chemical composition were ground using a 1mm screen. The 114 samples were analyzed for CP (AOAC, 1990). NDF was determined according to Van Soest and 115 Robertson (1985). 116 2.5. Statistical analysis 117 All data analyses were carried out using SAS (2003). To compare rumen DM degradation 118 parameters between the forages, the following statistical model was used: Yij = µ + Bi + eij, 119 6 where Yij is the dependent variable, µ is the overall mean effect, Bi is the browse effect and eij is 120 the random error. 121 122 3. Results 123 Rumen DM, CP and NDF degradation 124 The DM readily available soluble fraction (a), insoluble but degradable fraction (b), 125 degradation rate (c), potential degradability (PD) and effective degradability (ED) differed 126 significantly (P<0.05) across the three browse species (Table 1). The DM a was highest (P<0.05) 127 in H. abyssinica (478g/kg) followed by R. natalensis (418g/kg) and lowest (P<0.05) in F. 128 natalensis (378g/kg).The DM b was highest (P<00.05) in F. natalensis, but not different between 129 H. abyssinica and R. natalensis. The DM c was highest (P<0.05) in H. abyssinica but not 130 different between F. natalensis and R. natalensis. The DM PD was highest (P<0.05) in H. 131 abyssinica (848g/kg) and F. natalensis (793g/kg). The DM ED was highest (P<0.05) in H. 132 abyssinica (743g/kg) followed by F. natalensis (632g/kg) and lowest (P<0.05) in R. natalensis 133 (608g/kg). 134 The CP a, b, PD and ED fractions differed significantly (P<0.05) across the three browse 135 species. The CP c fraction was similar across the browse species. The CP a fraction was highest 136 (P<0.05) in R. natalensis (337g/kg) followed by F. natalensis (283g/kg) and lowest (P<0.05) in 137 H. abyssinica (233g/kg). The CP band ED fractions were highest (P<0.05) in H. abyssinica 138 followed by F. natalensis and lowest (P<0.05) in R. natalensis. The NDF a, b, PD, and ED 139 fractions differed significantly (P<0.05) across the browse species. The NDF c fraction was not 140 different across the browse species. The NDF a fraction was highest (P<0.05) in R. natalensis 141 (62g/kg) but not different between F. natalensis (27g/kg) and H. abyssinica (11g/kg). The NDF 142 7 b fraction was lowest (P<0.05) in H. abyssinica, but not different between F. natalensis and R. 143 natalensis. The NDF ED was highest (P<0.05) in F. natalensis (464g/kg), followed by H. 144 abyssinica (410g/kg) and lowest (P<0.05) in R. natalensis (335g/kg). 145 146 147 4. Discussion 148 4.3. Rumen DM, CP and NDF degradation 149 The effective DM, CP and NDF degradabilities for R. natalensis were significantly lower 150 than those of F. natalensis and H. abyssinica. This is partly attributed to the high fibre fraction 151 (NDF, ADF and ADL) of R. natalensis compared to F. natalensis and H. abyssinica as well as 152 other factors not measured in the present study, for instance the presence of condensed tannins. 153 Condensed tannins have been reported to have a greater negative effect on degradability than 154 NDF and ADF (Frutos et al., 2004, Nshahlai et al., 2011; Sebata et al., 2011). Abebe et al. 155 (2012) reported up to 224.5 g/kg DM of condensed tannins in R. natalensis compared to the total 156 tannin content of 60g/kg DM reported by Kendrick et al. (2009) in F. natalensis. High fibre has a 157 negative relationship with rumen degradability (Abdulrazak et al., 2000; Kamalak et al., 2005). 158 Similarly, Gasmi–Boubaker et al. (2005) reported a negative relationship between lignin 159 concentration and extent of digestion of forages. Lignin is an indigestible fraction and inhibits 160 the access of microbial enzymes to the structural polysaccharides (Van Soest, 1994). 161 Although the chemical composition was comparable to that reported by Abebe et al. (2012) 162 and Bamikole et al. (2004) for R. natalensis and Ficus species, the degradation characteristics 163 were different. For R. natalensis, Abebe et al. (2012) reported values lower by 20 and 26% than 164 those observed in this study for DM a and ED, respectively. For Ficus species, Bamikole et al. 165 8 (2004) reported values lower by 26 and 35% than those observed in this study for DM b and ED 166 respectively. The differences may be attributed to other factors not measured in the present 167 study. Data on degradation characteristics of H. abyssinica are unavailable. Basing on the DM, 168 CP and NDF degradation characteristics, F. natalensis and H. abyssinica are of a superior 169 nutritional quality to R. natalensis. 170 5. Conclusion 171 In conclusion, Rhuss natalensis subsp. romantica has inferior rumen degradability properties, an 172 indication of low nutritive value for goats compared to Harrisonia abyssinica subsp. abyssinica 173 and Ficus natalensis subsp. Natalensis. Further research is needed to determine how best H. 174 abyssinica and F. natalensis can be used as nitrogen supplements for goats. 175 176 Conflict of interest 177 The authors report that there is no conflict of interest relevant to this publication. 178 Acknowledgements 179 The authors gratefully acknowledge the financial support from African Natural Products 180 Research and Training Network (RISE-AFNNET 2/2011-14) and International Foundation for 181 Science (IFS, B5484-1) 182 183 References 184 Abdulrazak, S.A.,Fujihara, T. Ondiek, J.K., and Ørskov.E.R., 2000. Nutritive evaluation of 185 some Acacia tree leaves from Kenya. Anim Feed Sci Technol.85, 89-98. 186 Abebe, A., Tolera, A., Holand, O., Adnøy, F. and Eik, L. O., 2012. Seasonal variation in 187 9 nutritive value of some browse and grass species in Borana rangeland, Sothern 188 Ethiopia.Trop. subtrop. agroecosyst. 15, 261 -271. 189 AFRC, 1993. Energy and protein requirements of ruminants: an advisory manual prepared by 190 AFRC Technical committee on Response to Nutrients. CAB International, Wallingford, 191 Oxon OX10 8DE, UK. 192 AOAC, 1990. Official Methods of Analytical Chemists Inc., Arlington, Virginia, USA. 193 Bamikole, M.A., Ikhatua, U.J., Arigbede, O.M., Babayemi, O.S. and Etela, I., 2004. An 194 evaluation of the acceptability as forage of some nutritive and Anti nutritive components 195 and of Dry matter Degradation profiles of five species of Ficus. Trop Anim Health Prod. 196 36, 157-167. 197 Ben Salem, H. and Smith, T., 2008. Feeding strategies to increase small ruminant production in 198 dry environment. Small Rumin. Res. 77, 174-194. 199 Devendra, C., 2006. Small ruminants in Asia: Contribution to food security, poverty alleviation 200 and opportunities for poverty enhancement. In, James De Vries., 2008. Goats for the 201 poor: some keys to successful promotion of goat production among the poor. Small 202 Rumin. Res. 77, 221-224. 203 Devendra, C., 2010. Concluding synthesis and the future for sustainable goat production. Small 204 Rumin. Res. 89, 125-130. 205 Frutos, P., Hervás, G., Giráldez, J.F. and Mantecón, R.A., 2004. Review. Tannins and ruminant 206 nutrition. Span J. Agric Res. 2, 191-202. 207 Gasmi-Boubaker. A., Kayouli.C. andBuldgen. A., 2005.In vitro gas production and its 208 relationship to in situ disappearance and chemical composition of some Mediterranean 209 browse species. Anim Feed Sci Technol. 123, 303 – 311. 210 10 Kabasa, J. D., Opuda-Asibo, J., Thinggaard, G., and Meulen, U., 2004. The Mineral Scoring 211 Technique and Evaluation of Indigenous Browse Species as Natural Mineral 212 Phytocentres for Goats in African Rangelands. Trop Anim Health Prod. 36, 365-380. 213 Kamalak, A., Onder, C., Yavuz, G., Adem, E., and Osman, O., 2005. Effect of maturity stage on 214 chemical composition, in vitro and in situ dry matter degradation of tumbleweed hay ( 215 Gundeliatournefortii L.). Small Rum Res. 58, 149 -156. 216 Kendrick, E.L., Shipley Lisa. A., Hagerman Ann. E. and Kelly L.M., 2009. Fruit and 217 fibre: the nutritional value of figs for a small tropical ruminant, the blue duiker 218 (Cephalophusmonticola).Afri. J. Ecol. 47, 556-566. 219 McDonald, I., 1981. A revised model for the estimation of protein degradability in the rumen, 220 J. Agr Sci. (Cambridge), 96, 251 -252 221 Nsahlai, I.V., Fon, F.N and Basha, N.A.D., 2011. The effect of tannin with and without 222 polyethylene glycol on invitro gas production and microbial enzyme activity. S.African J. 223 Anim. Sci. 41, 337-344. 224 Osuji, P.O., Nsahlai, I.V. andKhalili, H., 1993. Feed evaluation. ILCA Manual 5. ILCA, Addis 225 Ababa, Ethiopia, pp 14 -16 226 Peacock, C., 2005.Goats a pathway out of poverty. Small Rumin Res. 60, 179 – 186. 227 Pearce,K.L., Norman, H.C. and Hopkins, D.L., 2010. The role of salt bush-based pasture systems 228 for the production of high quality sheep and goat meat. Small Rumin Res.91,29-38. 229 Rubanza, C.D.K., Shem, M.N., Otsyina, R., Bakengesa, S.S., Ichinohe, T. and Fujihara, T., 230 2005a. Content of phenolic extractable and bound condensed tannins and their effect on 231 invitro gas production from browse leaves. J. Anim Feed Sci. 14, 193-210. 232 Rubanza, C.D.K., Shem, M.N., Otsyina, R., Bakengesa, S.S., Ichinohe, T and Fujihara, T., 233 11 2005b. Polyphenolics and tannins effect on in vitro digestibility of selected Acacia 234 species leaves. J. Anim Feed Sci Technol. 119, 129-142. 235 Rubanza, D.K.C., Shem, N.M., Ichinohe, T and Fujihara, T., 2006.Polyphenolics and minerals 236 composition of selected browse tree species leaves native to north-western Tanzania 237 traditional fodder banks. J. Food Agric Environ. 4, 328-332. 238 Safari, J., Mushi, D.E., Kifaro, G.C., Mtenga, A.L. and Eik, L.O., 2011. Seasonal Variation in 239 Chemical composition of native forages, grazing behavior and some blood metabolites 240 of Small east African goats in a semi- arid area of Tanzania. Anim Feed Sci Technol. 241 164, 62-70. 242 SAS, 2003. User’s Guide Version 9.1. SAS Institute Inc., Cary, N.C. (USA). 243 Sebata, A., Ndlovu, L.R. and Dube, J.S., 2011. Chemical composition, in vitro dry matter 244 digestibility and in vitro gas production of five woody species browsed by matebele goats 245 (caprahircus L.) in a Semi–arid savanna, Zimbabwe. Anim Feed Sci Technol. 170, 122 – 246 125. 247 Tabuti J.R.S. and Lye, K.A., 2009.Fodder plant for cattle in Kaliro District, Uganda. Afr. 248 Study Monogr. 30, 161-170. 249 Van Soest, P.J. and Robertson, J.B., 1985. Analysis of forage and fibrous foods, A laboratory 250 manual for animal science 613. Cornell University Press, Ithaca, New York, U.S. 251 Van Soest, P.J., 1994. Nutritional ecology of the ruminants, 2 nd ed. Cornell University Press, 252 Ithaca, NY, USA, 476pp. 253 Yayneshet, T., Eik, L.O. and Moe, S.R., 2009. Seasonal variations in the chemical composition 254 and dry matter degradability of exclosure forages in the semi-arid region of northern 255 Ethiopia. Anim Feed Sci Technol. 148, 12-33. 256 12 Table 1. Rumen degradability parameters of the browse species 257 Ficus nantalensis Harrisonia abyssinica Rhuss nantalensis SE Significance level DM Readily available fraction,g/kg 378 c 478 a 418 b 5.4 *** Slowlydegradable fraction,g/kg 415 a 370 b 317 b 17.9 * Degradation rate, per hour 0.032 b 0.05 a 0.032 b 0.004 * Lag time, hours 0.92 b 0.21 b 6.71 a 1.05 ** Potential degradability, g/kg 793 ab 848 a 735 b 13.5 ** # Effective degradability, g/kg 632 b 743 a 608 c 2.2 *** CP Readily available fraction,g/kg 283 b 233 c 337 a 7.5 *** Slowlydegradable fraction,g/kg 516 b 664 a 365 c 32.6 ** Degradation rate, per hour 0.04 0.05 0.032 0.006 NS Lag time, hours 0 0 0 0 - Potential degradability, g/kg 799 ab 897 a 702 b 31.8 * # Effective degradability, g/kg 610 b 708 a 558 c 3.1 *** NDF Readily available fraction, g/kg 27 b 11 b 62 a 5.03 * Slowlydegradable fraction, g/kg 581 a 469 b 500 ab 14.7 * Degradation rate, per hour 0.061 0.123 0.024 0.02 NS Lag time, hours 1.24 3.20 3.99 1.3 NS Potential degradability, g/kg 608 a 480 b 562 a 10.4 ** 13 # Effective degradability, g/kg 464 a 410 b 335 c 6.6 ** # Effective degradability calculated assuming a ruminal flow rate of 0.02/h (AFRC, 1993) 258 abc Means within rows with different superscripts are significantly different (P<0.05) 259 *P<0.05; **P<0.01; ***P<0.001; NS Not Significa 260 261 262 Research highlights. 263  The natural gastro-enteric properties of Ficus natalensis, Rhuss natalensis and 264 Harrisonia abyssinica leaves was evaluated. 265  This was done by determining their chemical composition, rumen degradation, DM 266 intake and digestibility. 267  Rhuss natalensis was of an inferior nutritive value for goats compared to Harrisonia 268 abyssinica and Ficus natalensis. 269 270 271 272