Supplementation effect of thermotolerant yeast on nutrient utilization and rumen fermentation in Nellore lambs

Ch Harikrishna, M Mahender, Y Ramana Reddy, M Gnana Prakash, K Sudhakar and M Pavani

Department of Livestock Production and Management,
College of Veterinary Science, Sri Venkateswara Veterinary University
Rajendranagar, Hyderabad - 500030, Andhra Pradesh State, India
drhkvet@gmail.com

Abstract

Eighteen Nellore ram lambs (23.65 ± 0.25 kg body weight, aged 6 months) were used for evaluation of test diets to determine nutrient digestibility, plane of nutrition, nitrogen balance and rumen fermentation pattern. Lambs were fed finishing diets and assigned randomly to one of three dietary treatments. Treatment diets were no yeast (CON; n = 6), with 1 g/kg mesophilic yeast MTCC-1813 (MPY; n = 6) and with 1 g/kg thermotolerant yeast OBV-9 (TPY; n = 6).

Dry matter intake (DMI), DMI (% b. wt.) and DMI/kgW0.75 were higher (P<0.01) for the TPY group than MPY and CON groups. Digestibility of DM, OM (P<0.05), CP, CF, NFE, aNDF, ADF, Hemicellulose (P<0.05) and Cellulose were higher (P<0.01) on TPY diet compared to MPY and CON diets, indicating importance of thermotolerant yeast over mesophilic yeast. All Lambs were in positive nitrogen balance and was higher (P<0.01) on both TPY and MPY diets than CON diet. DCP, TDN and ME were significantly (P<0.01) higher on TPY diet, followed by MPY diet compared to CON diet. All the nitrogen fractions of rumen fluid (except food and protozoal nitrogen), pH and TVFA were higher (P<0.01) on TPY diet, compared to other two diets. Time of sampling also had significant (P<0.01) effect on concentration of all rumen nitrogen fractions and TVFA, which peaked at 4 h post feeding, while ammonia nitrogen and pH, peaked at 2 h post feeding irrespective of rations. The present study demonstrated the potential for supplementing theromotolerant probiotic yeast by improving the digestibility of nutrients, intake and content of DCP, TDN and ME, positive nitrogen balance and rumen profiles without adverse effect on the health of Nellore ram lambs. Thus, incorporation of thermotolerant probiotic yeast in straw based complete diet even when compared to mesophilic yeast, seems to be beneficial for livestock producers.

Keywords: digestibility, N retention, ram lambs, rumen profiles

Introduction

Inadequate availability of good quality feed is a major constraint to the prevalent small ruminant production system (Anbarasu et al 2004). Due to population boom, the available land is mostly diverted for cultivation of cereal and commercial crops to meet the urgent human needs resulting in decreased land for fodder cultivation, forcing livestock to depend on alternate feed resources. Since livestock subsist mainly on poor quality roughages, several new technologies are being tried to improve their digestibility and utilization. One such effort in recent years is supplementation of yeast ‘Saccharomyces cerevisiae’ to livestock rations to improve the utilization of cellulosic materials, health, productivity and reproduction.  

Probiotic yeast used as feed additive to enhance the animal performance by improving the balance of microbial flora in the gastrointestinal tract and nutrient utilization (Moallem et al 2009). There are reports indicating changes in the stimulation of ruminal digestion in goats, cattle and sheep when their feeds were supplemented with yeast (Khadem et al 2007 and Rohilla et al 2009). A number of studies reported increased concentration of specialized bacteria associated with fiber digestion and lactic acid utilization in rumen on yeast supplementation (Khadem et al 2007 and Malik and Singh 2009). But the yeast used so far, was mesophilic in nature and may not exert more beneficial action due to the harsh environmental (temperature variation in pH and bile concentration) conditions under which they have to survive in the gastrointestinal (GI) tract of the animal. The stimulation of rumen bacteria by yeast was different with specific strains as reported by Newbold et al (1995) and in the year 1995, Lankaputra and Shah also reported that high temperature in the gut of animals makes the limitation of using mesophilic strain of yeast as probiotic, acid and bile levels in GI tract of animals vary considerably and the cultures used as dietary probiotic are able to survive these harsh conditions before colonizing the gut. A thermo, acid, bile and osmo tolerant strain of yeast (Saccharomyces cerevisiae, OBV-9) which grows at >42^oC temperature, pH 2, 2% Ox bile and 30% sugars was isolated by Bhima et al (2008a), that can be used as a feed additive in livestock for better productivity.  

Therefore, the present study was designed with an objective to see the supplementation effect of straw based complete diet with 1 g/kg thermotolerant yeast (S. cerevisiae, OBV-9) in comparison with 1 g/kg mesophilic yeast (MTCC-1813) on intake, digestibility of nutrients, nitrogen balance and rumen fermentation pattern in Nellore ram lambs.

Materials and methods

Experimental design, animals and diets 

Experiments were conducted at the Livestock Experimental Station, Livestock Research Institute of Sri Venkateswara Veterinary University, Hyderabad, India. Eighteen Nellore ram lambs (23.65 ± 0.25 kg BW, aged 6 months) were assigned randomly to one of three test diets (6 ram lambs/test diet). Complete diets (Table 1) were supplemented with no yeast (CON; n = 6), 1 g/kg mesophilic yeast (MPY; n = 6) and 1 g/kg thermotolerant yeast (TPY; n = 6), formulated to have 12% CP (DM basis) to meet requirements of male lambs according to ICAR (1998). The lyophilized thermotolerant and mesophilic yeasts, obtained from DBT project on “Development and Application of Thermotolerant Probiotic Yeast for Enhanced Animal Productivity”, Department of Animal Nutrition, College of Veterinary Science, Hyderabad was used in the present study. All the experimental animal groups were kept separately under hygienic conditions in well ventilated pens (4 m x 3 m) and were not allowed for grazing. Healthy surroundings and proper cleanliness were maintained in sheds. All animals were injected with ivermectin (Ivectin 1%) for treatment and control of GI and ecto-parasites. The test diets (CON, MPY and TPY) were offered to the animals twice a day (two equal meals at 09:00 and 15:00 h). Diets were mixed biweekly during the study and were sampled upon mixing to ensure consistency in their chemical composition (Table 2).

Digestion and N balance experiment 

Four animals from each treatment were selected randomly and housed individually in metabolic cages that allowed separation of urine and faeces to evaluate digestibility of nutrients and N balance. Animals were offered weighed quantities of respective diets and clean drinking water ad libitum for the duration of the study. Animals were given 10 days as an adaptation period for the metabolism cages followed by 7-day collection period, feed intake and refusals were recorded. Feed samples and refusals were sampled for further analysis. Daily faecal output was collected, weighed and recorded, and then 10% was kept for subsequent analyses. Using glass bottles urine was collected, weighed and recorded, and then 5% was kept to evaluate N retention. Each bottle had 50 ml of 6N HCl to prevent ammonia losses. All samples were dried at 55 ^oC in a forced-air oven to reach a constant weight, air equilibrated, and then ground to pass 1 mm screen and kept for further analysis. During the experiment, feed, refusals and faeces were analyzed for DM, OM, CP, EE, CF, NFE, aNDF, ADF, Hemicellulose and Cellulose. According to procedures of AOAC (1997) feed samples, faeces and residues were analyzed for DM (100 ± 2^oC in an oven for 24 h; method 967.03), OM (550^oC in ashing furnace for 3 h; method 942), CP (Kjeldahl procedure; Kjeltec Auto 1013 Analyzer, Tecator, Sweden), EE was determined by extracting the sample with petroleum ether (60-80^oC) for 8 h in a pre-weighed oil flask using Soxhlet extraction apparatus, CF was estimated by treating the sample with 1.25% H₂SO₄ and 1.25% NaOH and the residue left was ashed in muffle furnace at 550^oC, the loss due to ashing was considered as crude fibre and NFE was obtained by subtracting the sum of CP, EE, CF and total ash percentage from 100. Fibre fractions like Neutral detergent fibre (aNDF), Acid Detergent Fibre (ADF), Cellulose and the Hemicellulose in feed samples, faeces and residues were analyzed according to procedures described by Van Soest et al (1991). Feed, faecal and urine samples were analyzed for N using Turbotherm and Vapodest (Gerhardt, Germany) analyzer (AOAC 1997; procedure Nos. 4.2.0.2).

Rumen fermentation study

Rumen liquor was obtained with the help of a stomach tube fitted with vacuum pump from each animal at 0 (before feeding) 2^nd, 4^th and 6^th h after feeding.  Approximately 150 ml of rumen liquor was siphoned from different depths and directions of reticulo-rumen and transferred into pre heated thermos flask, strained through a fourfold muslin cloth. pH of strained rumen liquor (SRL) was estimated immediately after collection using glass electrode pH meter and samples were preserved in deep freeze after adding 1 ml of saturated mercuric chloride solution per 100 ml SRL for further analysis. Rumen liquor samples were analyzed for total nitrogen (Micro-Kjeldahl), Trichloro acetic acid (TCA), TCA-insoluble protein nitrogen (Cline et al 1958), Residual nitrogen, Food and protozoal nitrogen, (Singh et al 1968), Ammonia nitrogen (Conway 1957) and Volatile fatty acids (Barnett and Reid 1956).

Statistical methods

Data were analysed using the GLM procedures (SAS 2001). In all analyses, when least squares means were different at P<0.05, they were separated by the PDIFF option of SAS.

Results and discussion

Digestion and N balance 

Least square means of Dry matter (DM) intake, digestibility of nutrients and N balance of lambs fed diets are presented in Table 3.  

DM intake (g/day or g/kg W^0.75/day) was higher in lambs fed TPY ration than those fed CON and MPY rations, while intake of OM and CP was similar among all the groups. The DM intake was higher than those recommended by ICAR (1998) in all lambs indicating, all test diets were adequately palatable to maintain the intake due to blending of roughages and concentrates in correct proportions and inclusion of thermotolerant yeast might have influenced the intake in lambs. The results of current study were consistent with the reports of Salem et al. (2000), who reported sheep diets supplemented with yeast significantly improved voluntary feed intake. The results were also consistent with the findings of Gonzalez (1993), Abd El Hafez et al (1997) and Wohlt et al (1998) in lambs fed yeast based diets. Higher DM intake on yeast based complete diets was also reported in lambs (Plata et al 2004) and in Marwari kids (Rohilla et al 2009) thus, the findings of present study corroborate with their results.  

Digestibility of DM, OM, CP, CF, NFE, aNDF, ADF, Hemicellulose and Cellulose was higher on TPY diet followed by MPY diet than CON diet. Higher DM digestibility was reported by Abd El Hafez et al (1997), Salem et al (2000), Haddad and Goussous (2005) and Mahender et al (2006) with dietary yeast in lambs. Higher OM and CP digestibility was also reported by Salem et al (2000), Mahender et al (2006) and Haddad and Goussous (2005) in sheep and Rohilla et al (2009) in Marwari kids fed complete diets with yeast. The results indicated that, yeast inclusion might have exerted selective stimulatory effect on specific rumen bacteria responsible for fibre degradation and microbial protein synthesis in rams (Erasmus 1991 and Rossi et al 1995). Higher CF digestibility in the TPY diet might be due to inclusion of thermotolerant yeast, which might have shown a complementary effect by providing favourable rumen environment for stimulating cellulolytic and hemicellulolytic bacteria along with concentrates over MPY and CON diets. The results of current study were consistent with findings of Abd El Hafez et al (1997), Salem et al (2000 and 2002) and Mahender et al (2006), who reported significant improvement in CF digestibility in lambs and Rohilla et al (2009) in Marwari kids fed yeast supplemented feed. These results were in accordance with Bhima et al (2008b), who reported higher CF digestibility with dietary addition of thermotolerant yeast in buffalo calves. It was observed that, the NFE digestibility was increased by 3.45 and 1.55 percentage units on TPY and MPY diets, respectively than CON diet. Improved efficiency in feed utilization, better CF digestion and higher DM digestibility might have resulted in higher NFE digestibility. The results were in agreement with the findings of Salem et al (2000) and Mahender et al (2006) on yeast based diets in lambs. Increased aNDF digestibility recorded in the present study corroborate with the findings of Haddad and Goussous (2005), who reported similar results on dietary incorporation of yeast in lambs. Carro et al (1992) and Mpofu and Ndlovu (1994) also reported increased aNDF degradability due to addition of yeast in rations under incubation trials. On contrary, Arcos Garcia et al (2000) and Kawas et al (2007) reported no difference in digestibility of aNDF, when sheep fed on mixed ration with or without yeast. Higher ADF digestibility for test diets MPY and TPY, recorded in the present study was in agreement with findings of Wohlt et al (1998) in cows and Bhima et al (2008b) in buffalo calves, who reported increased ADF digestibility due to dietary supplementation of yeast, whereas Adams et al (1981) and Andrighetto et al (1993) recorded no impact of yeast addition in complete diets on ADF digestibility in sheep. Higher hemicellulose and cellulose digestibility recorded in the present study was consistent with findings of Bhima et al (2008b), who observed higher hemicellulose digestibility due to the feeding of thermotolerant yeast supplemented complete diets in buffalo calves.  

Similarly, intake (g/day or g/kg W^0.75/day) of DCP, TDN and ME was higher on TPY diet followed by MPY diet than CON diet. This might be due to higher energy density as well as higher CP and other nutrients digestibility recorded on these rations. Further, all the ram lambs were adequately met with the DCP, TDN and ME requirements as recommended by ICAR (1998). The results of the present study were in agreement with findings of Mahender et al (2006), who reported higher DCP and TDN intake in lambs fed yeast based diets. Bhima et al (2008b) also reported higher TDN (g/d) and ME (MJ/kg DM) in buffalo calves fed diets with varied levels of thermotolerant yeast.  

The N intake, N balance (% intake) and N balance (% absorbed) of yeast supplemented diets were higher than CON diet, while there was no difference observed among the MPY and TPY diets. The higher daily average N intake and balance on test diets reflecting the CP intake and digestibility pattern among the treatment groups might be due to addition of yeast. Positive nitrogen balance recorded in lambs indicating, all the rations met with the nitrogen requirements of lambs and was because of optimum utilization of dietary nitrogen by microbes due to matching supply of energy (Reddy and Reddy 1991). Tagel Din et al (1989 and 1990) also reported positive nitrogen balance in lambs fed complete diets. The results of the present study were consistent with the findings of El Waziry et al (2000), who reported nitrogen degradability and N balance were increased by the addition of yeast in sheep. Other workers²⁸ also reported higher N retention in lambs fed diets with yeast.  

Rumen fermentation pattern

Rumen profiles in respect of nitrogen constituents, pH and total volatile fatty acids (TVFA) of the test diets are presented in Table 4. The ruminal total nitrogen, TCA insoluble nitrogen, ammonia nitrogen, residual nitrogen, pH and TVFA concentrations of test diet TPY containing thermotolerant yeast was higher followed by MPY diet than CON diet. Differences in the ruminal total nitrogen, TCA insoluble nitrogen, ammonia nitrogen, residual nitrogen, food and protozoal nitrogen, pH and TVFA concentrations due to time of sampling were also significantly different (Table 5). Peak levels of ruminal total nitrogen, TCA insoluble nitrogen, residual nitrogen and TVFA were recorded at 4 h post feeding, while ammonia nitrogen and pH concentrations were peaked at 2 h post feeding, in all the experimental complete diets.

Higher total nitrogen recorded on TPY diet, might be due to higher intake and better digestibility of nitrogen with the addition of thermotolerant yeast. Higher total nitrogen at 4 h after feeding in all test diets might be due to active degradation of protein and hydrolysis of NPN substances in rumen and stimulatory effect of yeast on protease producing bacteria resulting in enhanced microbial metabolism and synthesis of microbial protein. Results of current study were consistent with the findings of Mahender (2004) in lambs fed yeast included diets. Petkova et al (2002) also reported that the utilization of yeast clearly displayed a stimulating effect on fermentation in the rumen of lambs. The pattern of TCA insoluble nitrogen was similar to that of total nitrogen. Higher levels of TCA insoluble nitrogen observed on TPY diet might be due to higher intake of CP and stimulatory effect of yeast on certain bacteria resulting in higher microbial protein. The results were consistent with the findings of Kumar et al (1994), who reported marginally increased TCA insoluble nitrogen in calves fed yeast based diets.

Time of sampling had significant effect on TCA insoluble nitrogen and it reached peak at 4 h post feeding, and was stated to be due to active degradation of protein, synthesis of microbial protein in the rumen and subsequent decline in its concentration due to change in the rumen volume through inflow of saliva (Murali et al 1989). Higher levels of rumen ammonia nitrogen observed on TPY diet might be due to active degradation of protein and hydrolysis of NPN substances in rumen. The results were consistent with the findings of Yldz et al (1995), Salem et al (2000) and Petkova et al (2002), who reported higher NH₃-N on yeast supplemented rations in sheep. Rohilla et al (2009) was also reported NH₃-N was efficiently utilized in kids with the addition of yeast in rations. Time of sampling also had a significant effect on NH₃-N level, which peaked at 2 h post feeding irrespective of test diets. Similar results were observed by Samantha et al (2003) in Barbari goats fed complete diets. On contrary, El Waziry et al (2000), Salem et al (2002) and Khadem et al (2007) observed either significantly low or no difference in NH₃-N in sheep when diets were supplemented with yeast. The higher residual nitrogen on TPY and MPY diets than CON diet might be due to higher total nitrogen levels in the rumen, which was a resultant from yeast inclusion (Reddy et al 1993). This result was also consistent with the findings of Mahender (2004) in ram lambs fed yeast based diet. Time of sampling had significant effect on residual nitrogen level, which peaked at 4 h post feeding irrespective of ration, might be due to variations in the substrate availability and salivary secretion (Reddy et al 1996). The test diets had no effect on ruminal food and protozoal nitrogen and were comparable, but time of sampling had significant effect on food and protozoal nitrogen level. Peak levels were recorded 4 h post feeding in all test diets. This result is consistent with the findings of Arcos Garcia et al (2000) in Suffolk sheep fed yeast based diets. Increase in the ruminal pH favours the activity of certain microorganisms like cellulolytic bacteria and increase in the ruminal pH on yeast supplementation might therefore be one of the reasons for significant increase in the number of these microorganisms. Monika Singhla et al (2000) and Krupavaram (2000) observed significant effect on time of sampling in buffalo bulls fed yeast based diets.

Higher ruminal pH values recorded in the current study on TPY diet followed by MPY diet might be attributed to decrease in the level of lactic acid as a result of stimulation for removal of lactate by ruminal lactate utilizing bacteria in the presence of yeast (Nisbet and Martin 1991). The results were in agreement with the findings of Williams et al (1991) and Girard (1996), who reported increase in pH from 6.66 to 6.73 with yeast inclusion. Increase in ruminal pH was also recorded by Adams et al (1981), Gray and Ryan (1988), Mahender (2004) and Khadem et al (2007) in lambs and Rohilla et al (2009) in kids fed yeast based diets. On contrary, no effects were detected in rumen pH by Garcia et al (2000) in sheep fed yeast based diets. Time of sampling had significant effect on ruminal pH values, and highest pH was observed at 2 h post feeding in all test rations indicating, yeasts did not assimilate lactate. Similar results were also reported by Williams et al (1991) in cows and Monika Singla et al (2000) in calves.

Higher TVFA level recorded in the rumen fluid of lambs on TPY diet followed by MPY diet reflecting, better plane of nutrition. The results were in agreement with the findings of Gray and Ryan (1988), Andrighetto et al (1993), Arcos Garcia et al (2000), El Waziry et al (2000), Salem et al (2000) and Khadem et al (2007) in sheep fed yeast based diets. Malik and Singh (2009) also reported that, yeast has increased cellulose degrading bacteria in the rumen and increased the relative concentration of acetate in the rumen. These results indicating, when conditions in the rumen were stabilized, there was an increase in rate of fibre degradation and with the effect on cellulolytic bacteria, propionate production was increased (Williams 1989). Girard and Dawson (1994) showed that specific strains of fibre digesting bacteria were stimulated by yeast, which have a major role in the digestion of fibre and the production of acetic and succinic acids and other bacterial population will produce propionic acid by using succinic acid. Peak levels of TVFA were recorded at 4 h post feeding in all test rations. These results corroborated with that of Salem et al (2002), who reported significantly higher TVFA at 6 h and 3 h post feeding in yeast supplemented group than control group of sheep. The results of rumen profiles study revealed that the TPY diet supplemented with thermotolerant yeast had higher pattern of nitrogen fractionalization, its absorption and utilization from the rumen of lambs compared to  MPY and CON diets, resulting in relatively better performance in lambs.

Conclusions

• The study on digestibility and rumen profiles on ram lambs demonstrated the potential for supplementing theromotolerant yeast that improved digestibility of nutrients, intake and content of ME, positive nitrogen balance and rumen profiles reflecting, the digestibility coefficients of nutrients without any ill effect on the health of ram lambs under study. Thus, incorporation of thermotolerant probiotic yeast in complete diet even when compared to mesophilic yeast, is recommended for the benefit of livestock farmers.

Acknowledgements

The authors are thankful to the financial assistance from DBT Project, College of Veterinary Science, Hyderabad. Appreciation is expressed to technical staff of Dept. of Animal Nutrition and LRI for conducting the experiments and laboratory analyses. Appreciation is also expressed to the Central Research Institute for Dryland Agriculture, Hyderabad for conducting analysis of fibre fractions.

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Received 24 February 2012; Accepted 15 April 2013; Published 1 May 2013

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