Bypass fat enhances liveweight gain and meat quality but not profitability of smallholder cattle fattening systems based on oil palm frond

Keywords: oil palm frond, total mixed ration, bypass fat, Napier grass, meat quality, feedlot cattle.

Because of the increased demand for quality beef across Southeast Asia, small-scale cattle feedlots are growing in number in this region to take advantage of the high price of beef. Concentrate-based diets are frequently used to achieve high growth rates and high-quality meat when fattening cattle. However, the high cost of concentrate feeds makes them inaccessible to many smallholder farmers; thus, alternative feeds such as agro-byproducts are often used to decrease the cost of production. Oil palm is an important crop in several tropical countries and the oil palm industry generates several waste products, including oil palm frond (OPF), which can be used as roughage source for ruminant feeding (Tuyen et al. 2013; Astuti et al. 2015; Tafsin et al. 2018; Hamchara et al. 2018). Although the use of OPF in beef production is constrained by its complex fibrous structure and low nutrient content, its wide availability and comparative cost advantage as compared with the traditional forage feed (such as cut grass) makes OPF a viable alternative forage feed for cattle.

Many approaches to improve the digestibility of OPF and, thus, its nutritive value as a forage source for ruminants have been tested. These include the use of legumes (Khamseekhiew et al. 2002), enzymes (Wahyuni et al. 2012) and treating OPF using fungi to breakdown its fibre (Chanjula et al. 2017; Hamchara et al. 2018; Tafsin et al. 2018), but with little or no advantages (Chanjula et al. 2017). In addition, the use of fungi treatment to improve the digestibility of OPF is too complicated under smallholder conditions. Offering OPF together with concentrate in total mixed ration (TMR) has been shown to improve feed palatability and intake (Dahlan et al. 2000). Moreover, feeding TMR was shown to be more profitable than integrating grazing and TMR or grazing alone in dairy cows (Tozer et al. 2003).

Supplementation with fats is often used to increase the energy content of cattle rations formulated with agricultural by-products. Mutsuba et al. (2019) reported that coconut and soybean oils inhibited the most potent rumen cellulolytic bacterium (Fibrobacter succinogenes), while palm oil had no such negative effect. Kang et al. (2019) reported that supplementation of palm oil in the form of ‘rumen-protected fat’ in Timothy hay-based diets increased the high-density lipoprotein and carbohydrate metabolites in the blood. However, this improvement was not reflected in growth performance in Korean cattle. Thus, when considering replacing cut forage with OPF in TMR, supplementation of bypass palm fat may help boost the energy content of low-quality OPF-based diets to sustain growth performance.

The present study aimed to evaluate the impact of including bypass fat in OPF-based TMR and compare this to a traditional TMR based on Napier grass. We hypothesised that addition of bypass fat would increase liveweight gain, meat quality and economic returns of the OPF-based diet. The study was designed to mimic the conditions of typical smallholder cattle feedlots in southern Thailand, which are similar to the other countries in Southeast Asia.

This experiment was conducted at a smallholder commercial farm located at Amphoe Mueang district, Phatthalung Province, Thailand. The farm was selected because it is representative of smallholder cattle feedlots in Southeast Asia.

Sixteen Charolaise × Brahman crossbreds of 23 ± 2.0 months of age with an average bodyweight (BW) of 425 ± 59.92 kg (mean ± s.e.) were fattened with TMR based on either freshly chopped Napier grass (Pennisetum purpureum) or OPF, with or without the addition of 5% bypass fat, as follows: (i) Napier grass-based TMR (Napier grass–fat; Control), (ii) Napier grass-based TMR + 5% fat (Napier grass+fat), (iii) OPF-based TMR (OPF–fat) and (iv) OPF-based TMR + 5% fat (OPF+fat). Animals were allocated to treatments in a 2 × 2 factorial (roughage source × fat supplementation) randomised complete-block design, with initial BW of cattle used as blocking criteria. Diets were formulated to be iso-caloric and iso-nitrogenous (Table 1) and offered ad libitum. The animals were kept in individual pens (~8 m²) where clean drinking water and mineral salt were available at all times throughout the experiment. The experiment consisted of a 15-day adaptation period followed by a 255-day experimental period.

Table 1.  Ingredients, cost and chemical composition of experimental diets
Costs of all ingredients were based on the price when the ingredients were purchased from the local feed supplier, inclusive of transportation cost. Napier grass-fat, fresh chopped grass in total mixed ration; Napier grass+fat, fresh chopped grass in total mixed ration supplemented with bypass fat; OPF-fat, oil palm fronds in total mixed ration; OPF+fat, oil palm fronds in total mixed ration supplemented with bypass fat; DM, dry matter; CP, crude protein; NDF, neutral detergent fibre; ADF, acid detergent fibre

Feed ingredients were purchased from local feed suppliers. Napier grass (harvested using a forage-harvester with average length of 7–8 cm) was purchased from Chumphon Animal Nutrition Development Station and the OPF (chopped to particle size of 2–3 cm, Fig. S1, available as Supplementary material to this paper) was purchased from the Oil Palm Community Enterprise, Surat Thani province, Thailand. The bypass fat was prepared by mixing crude palm oil (43 kg/100 kg) with animal fat (20 kg/100 kg) and shell powder (13 kg/100 kg), adjusted with alkaline solution (9 kg NaOH + 15 kg water) to a pH of 8.5, which was then pelleted (Fig. S2).

Feed was provided twice daily in two equal portions at 0900 hours and 1500 hours. Feed refusals were weighed and recorded daily before the morning feeding. Fresh ort samples were bulked by animal and dried at 65°C and subsamples were used for dry-matter (DM) determinations. Daily feed offered and refusals were used to determine daily feed intake of individual cattle. Feed intake was measured daily throughout the experimental period and the amount of TMR offered was adjusted every 15 days according to the weight of each animal. Representative samples of the TMR were taken every week. Composite TMR samples and refusal were analysed for DM, crude protein (CP) ether extract (EE), ash, neutral detergent fibre (NDF), acid detergent fibre (ADF) and gross energy (GE).

Cattle were weighed fortnightly and average daily gain (ADG) was estimated using linear regression.

Digestibility of the diets was estimated using total faecal collection, as described by (Velasquez et al. 2018), during the 9th week of feeding trial. Briefly, feed intake and faecal output were measured by individual animal for 7 days and faecal subsamples were collected, pooled by the animal at the end of 7 days to determine DM content. DM digestibility was calculated using the equation: DM digestibility = [(DM intake – DM in faeces)/DM intake] × 100 (Galyean 2010).

Metabolisable-energy (ME) intake was calculated using the DM intake (DMI) measured in the present study multiplied by the ME values of the ingredient composition in the respective TMR, by using the Thai Nutrition NRC (2010).

Composite TMR samples and refusal were collected weekly and dried in a forced-air oven at 65°C for 24 h. Dried samples were ground to pass a 1-mm screen and then analysed for DM, CP, EE and ash, by using proximate analysis according to AOAC (2000). DM was determined by oven drying in a forced-air over at 105°C for 24 h. The N content of feed was determined using a Kjeltec Auto Analyzer (Kjeldatherm model KT and KT-L series, Gerhardt, Germany), while EE was determined in petroleum ether by using a Soxhlet Extraction SOX 416 (Gerhardt, Germany). The ash content was determined by ashing the sample in a muffle furnace at 550°C for 5 h. Neutral detergent fibre (NDF) and ADF were determined by methods of Van Soest et al. (1991). The GE of the feed was determined using a bomb calorimeter (IKA Calorimeter System, C 2000 basic, IKA-Werke, Staufen, Germany).

All cattle were slaughtered at the end of the experiment. They were transported by truck to a commercial slaughterhouse built to serve the surrounding smallholder cattle farmers of this area. The cattle were slaughtered after being fasted overnight according to the standard practice of the slaughterhouse. Fasted liveweight was recorded before slaughter and hot carcass weight within an hour of slaughter. Carcass yield percentage was calculated as ×100 (hot carcass weight/slaughter weight) as described by Françozo et al. (2013). The carcass was then split longitudinally into left and right halves and kept to chill at 4°C at the facility within the slaughterhouse, where all the carcass measurements were also performed. The pH of muscle was measured using a penetrating electrode (SevenGoTM pH meter SG2, Mettler Toledo, Thailand) after 24 h of chilling, as described by Mach et al. (2008). Cold carcass weight was determined after chilling (4°C) for 7 days (Boonsaen et al. 2017). The longissimus dorsi (LD) muscles from the right side of the 16 carcasses were excised from between the 12th and 13th ribs to determine backfat thickness and loin eye area (Boonsaen et al. 2017) and meat colour (CIE L*, a* and b*, Illuminant C, 0° observer; Hunterlab Miniscan colour meter Mirolta Chromameter CR-300; AMSA 2012), after cutting a slice and blooming for 15 min as described by Boonsaen et al. (2017). Subsequently, three 2.5 cm thick steaks were subsampled from each LD section to determine shear force by using the Instron Universal Testing Machine Model 1011, Instron Corporation, USA (AMSA 2015). In addition, ~700 g of meat from each LD muscle was collected and frozen (–20°C) for chemical composition (Andrae et al. 2001). Laboratory analyses of meat samples were completed 2 months after the meat was sampled. The samples were thawed at room temperature (20°C), analysed as a fresh sample (not lyophilised), ground, homogenised, and analysed in triplicate (Françozo et al. 2013). The DM, CP, EE and ash content were determined following the standard methods of AOAC (2000).

Investment costs were estimated on the basis of the 255-day fattening period on a per animal basis. Costs included (i) cost of buying the cattle, (ii) cost of feed, (iii) cost of labour to raise the cattle, (iv) utilities (water and electricity), (v) medicines and vaccinations, (vi) transportation cost of transporting cattle from farm to the slaughterhouse, (vii) depreciation of farm buildings and machineries, specifically for cattle production, and (viii) opportunity cost. The opportunity cost was the loss of benefit that could have been saved had the study had a choice not to pay for the cost of the cattle. The opportunity cost was estimated as 7% of the cost of cattle according to the interest rate of commercial banks in Thailand at the time of the present study. Cost of feeder cattle for the present study (purchased from nearby smallholder farmers) depended on the condition of the cattle, and averaged ~3 US$ per kg liveweight. Depending on the TMR formulation, cost of feed varied marginally, averaging 0.17 US$ per kg. Labour cost per person was estimated at 10 US$ per day, with one person capable of taking care of 16 heads of cattle.

Data were analysed using the Statistical Analysis System Institute (SAS 1998) software. The mixed procedure was used to analyse the fixed effects of treatment and block on parameters, with animal serving as the experimental unit. The means were statistically compared using Duncan’s multiple-range test (Steel and Torries 1980) to identify differences among means. Statistical significance was considered at P < 0.05. The mathematical model assumption used was

where Y_ijk = observation, µ = general mean, Blk_i = is the ith block effect, α_j = sources of roughage in TMR, β_k = bypass fat supplement effect, αβ_jk = roughage sources × bypass fat-supplement effect, and ε_ijk = is the residual error.

Provision of bypass fat to cattle fed OPF increased ADG during the fattening period (Table 2). While supplementing cattle with bypass fat did not result in a significant increase in feed intake, digestibility or feed conversion efficiency, ME intake tended to be higher. ADG of cattle fed OPF+fat (0.92 kg/day) was similar to that of cattle fed Napier grass-based TMR (0.91 to 0.93 kg/day), and also comparable to gains reported in studies with cattle fed with diets containing various agricultural by-products, such as rice straw and concentrate (Siddque et al. 2015) and pineapple by-products (Hattakum et al. 2019; Pintadis et al. 2020). ME intake of all diets was approximately double the 444 KJ ME/kg BW^0.75 suggested for maintenance for Charolaise crossbred cattle (Subepang et al. 2019), indicating that if properly formulated, diets made up of agricultural by-products could be used effectively for fattening of cattle in developing countries.

Table 2.  Feed intake and liveweight gain of cattle fed Napier grass-TMR and OPF-TMR supplemented with and without bypass fat (n = 4 per treatment)
Napier grass–fat, fresh chopped grass in total mixed ration without bypass fat; Napier grass+fat, fresh chopped grass in total mixed ration supplemented with bypass fat; OPF–fat, oil palm fronds in total mixed ration without bypass fat; OPF+fat, oil palm fronds in total mixed ration supplemented with bypass fat; BW, bodyweight; ADG, average daily gain; DMI, dry matter intake; DMD, DM digestibility; DDMI, digestible DM intake; CPI, crude protein intake; NDFI, neutral detergent fibre intake; GEI, gross energy intake; MEI, calculated metabolisable energy intake ; FOR, forage type; FAT, bypass fat supplement. s.e.m., stand error of the mean. Values within a row followed by different letters are significantly different (at P = 0.05)

In comparison, supplementation with bypass fat did not affect ADG of cattle fed grass-based TMR. This result is consistent with Kang et al. (2019), who reported that supplementation with bypass fat did not affect ADG in growing Korean cattle steers fed a Timothy hay-based diet. Kang et al. (2019) concluded that, although not affecting growth performance, bypass-fat supplementation affected some blood lipids and carbohydrate metabolites. The reason why fat supplementation improved the ADG of cattle fed OPF, but not grass-based diet, in the present study, is unclear. However, one possibility could be that the Napier grass, being more digestible than OPF, contributed a higher proportion of the total digestible energy from the diet, thus reducing the beneficial role of the supplemented fat for weight gain, as compared with the less digestible OPF diet.

The average daily DMI of cattle fed OPF-based diets was significantly (P < 0.01) higher than that of cattle fed grass-based diets (Table 2). However, the OPF diets were less digestible (P < 0.01). The above results contradicted the general observation that DMI is positively associated with DM digestibility. Feed intake in ruminant animals is controlled by many factors, including gut fill and rate of passage (Jung and Aller 1995). However, rate of passage can be increased by chopping or grinding the feed to smaller particle sizes before feeding, so as to increase feed intake (Minson 1963), especially when it is a poor-quality roughage (Campling and Freer 1966). Thus, the higher intake of OPF-based diets in the present study could be partly influenced by the higher passage rate because of the smaller particle size (2–3 cm), which resulted in a lower digestibility (Martz and Belyea 1986; Udén 1988) than with the longer (7–8 cm) grass used in the study. There was also no difference in the intake of CP or GE, since diets were formulated to be iso-nitrogenous and iso-caloric (Table 1).

Results from the present study showed that neither forage type nor fat supplementation had any significant effect on warm and cold dressing percentage, averaging 57.7% and 56.2% respectively (Table 3), which indicated a carcass weight loss of 2.6% during chilling. The above values were close to the 58.9–59.5% dressing percentage reported for steers of the same breed as in the present study (Charolaise × Brahman crossbred) fed TMR contained cassava chip and ground corn (Boonsaen et al. 2017), as well as the 55.4–60.6% for Australian commercial cross bulls fed with different levels of urea-treated OPF silage and concentrate diets (Ishida and Abu Hassan 1997). Comparing with other breeds, the present results were marginally higher than the 54.7–55% warm dressing percentage for Nellore bulls fed feedlot diets having different glycerine concentrations (Françozo et al. 2013) and the 53.5–54.0% for Holstein steers fed with Napier silage, corn silage and pineapple by-product silage-based TMR (Hattakum et al. 2019), but marginally lower than the 59.89–60.71% for Angus crossbred beef steers fed different levels of corn oil (Andrae et al. 2001). The minor differences recorded among studies could be due to different breeds, and the type and level of oil used in the experiments.

Table 3.  Carcass characteristics of cattle fed OPF-TMR or Napier grass-TMR with and without bypass fat supplementation
Napier grass–fat, fresh chopped grass in total mixed ration without bypass fat; Napier grass+fat, fresh chopped grass in total mixed ration supplemented with bypass fat; OPF–fat, oil palm fronds in total mixed ration without bypass fat; OPF+fat, oil palm fronds in total mixed ration supplemented with bypass fat; FOR, forage type; FAT, bypass fat supplement. s.e.m., standard error of the mean

Fat supplementation had a bigger impact on meat quality than did forage type (Table 4). Meat from cattle fed OPF had a lower pH than did meat from cattle fed grass-based TMR (P = 0.05), while fat supplementation decreased pH, moisture, CP and ash content, and increased meat colour (lightness, redness, yellowness), backfat thickness and fat content (P < 0.05, Table 4). Meat colour is related to carcass maturity and muscle pH, and is an important component of meat-quality grades (USDA 1997). In the present study, meat from cattle supplemented with fat had higher (P < 0.05) lightness, redness and yellowness in meat, which are preferred by the consumers. The lightness L*, redness a* and yellowness b* of meat in the present study were close to values of aged and non-aged commercial meat from Simental bulls (Gasperlin et al. 2001) and feedlot Nellore bulls fed with diets with different glycerine contents (Françozo et al. 2013) and from pasture- and concentrate-fed cattle (Realini et al. 2004).

Table 4.  Physical characteristics and chemical composition of Longissimus dorsi muscle from cattle fed Napier grass-TMR and OPF-TMR supplemented with and without bypass fat
Napier grass–fat, fresh chopped grass in total mixed ration without bypass fat; Napier grass +fat, fresh chopped grass in total mixed ration supplemented with bypass fat; OPF–fat, oil palm fronds in total mixed ration without bypass fat; OPF+fat, oil palm fronds in total mixed ration supplemented with bypass fat; CP, crude protein; FOR, forage type; FAT, bypass fat supplement. s.e.m., standard error of the mean. Values within a row followed by different letters are significantly different (at P = 0.05)

Forage type also affected loin eye area and moisture content, with meat from cattle fed OPF–fat having the smallest loin eye area and meat from OPF+fat having the lowest moisture content. Warner–Bratzler shear force was not affected by forage type or bypass-fat supplementation (P > 0.05).

Meat pH and colour are important indicators of quality, with a low pH and higher colourimeter readings being correlated with tenderness (Purchas 1990; Watanabe et al. 1996; Wulf and Wise 1999). Changes in the pH of meat post-slaughter are primarily caused by the glycogen in the muscles of animals. The amount of glycogen available at the point of slaughter determines the postmortem energy metabolism in the skeletal muscles through the anaerobic glycolysis, which results in accumulation of lactic acid and, thus, a reduction in pH in the respective skeletal muscles. The pH of meat in live animals is ~7.0 and normally decreases to ~6.1 and lower (5.4–5.8) after slaughter (Page et al. 2001; Adzitey and Nurul 2011). Meat of abnormally high pH are usually dark, firm and dry, while meat of abnormally low pH are usually pale, soft and exudative. Results of the present study showed that pH of meat from the OPF+fat (5.45) and Napier grass+fat (5.78) groups were within the pH of normal meat and close to those reported for commercially slaughtered meat from various breeds, such as Charolais, Holstein, Bonsmara, Angus and Nguni (Gasperlin et al. 2001; Mounier et al. 2006; Pfuhl et al. 2007; Muchenje et al. 2009), while meat from cattle without fat supplementation had unfavourably higher (P < 0.01) pH (6.20 and 6.73 for OPF–fat and Napier grass–fat respectively), which may lead to dark firm dry meat (Adzitey and Nurul 2011). This result clearly showed the advantage of fat supplementation on meat quality in cattle fed tropical forage and agricultural by-product such as OPF.

Backfat thickness was higher in cattle supplemented with bypass fat (1.37 vs 1.30 cm, P < 0.05), indicating that, in addition to improving the colour of muscle, and irrespective of forage type, the additional energy from bypass-fat supplementation was utilised for production of backfat thickness in the LD muscle. This result is interesting since fat depth is usually positively correlated with dressing percentage, but no difference in dressing percentage was recorded in our study (Table 3). Backfat thickness recorded here was close to values (1.25–1.46 cm) reported for steers of similar breeds (Charolais × Brahman crossbred) fed different TMR containing cassava chip and ground corn (Boonsaen et al. 2017) and those (1.2–1.3 cm) fed with Napier grass hay and rice straw with or without palm oil in the concentrate (Matsuba et al. 2019). Others have also reported near similar backfat thickness for other breeds, such as Angus crossbred steers (1.20–1.30 cm) fed with different oil-corn diets (Andrae et al. 2001) and for Holstein steer (1.20–1.29 cm) fed diets containing 4 and 5 kg/day concentrate with pineapple stem by-product as roughage (Pintadis et al. 2020). The near similar values reported among the different studies seem to suggest that there is little difference in backfat thickness among the common cattle breeds fed various forms of agricultural by-products and concentrates.

Thicker backfat resulted in a higher fat content in meat of fat-supplemented cattle than in that of non-supplemented cattle (11.5% vs 8.1%), and lower proportions of CP and ash in cattle supplemented with bypass fat. Increased fat content was also negatively related to moisture content in both the OPF- and grass-based diets (P = 0.01), which is consistent with results reported elsewhere (Abubakr et al. 2013; Hattakum et al. 2019). However, the above negative relationship between moisture and fat contents did not occur when comparing the values across the present study with those of Matsuba et al. (2019). The above researchers, working with feedlot cattle fed diet supplemented with palm oil, reported lower values of moisture (65.4–68.1% vs 69.8–72.5%) and lower fat (7.2–8.1% vs 7.9–11.8%) contents of meat than in the present study.

Average total investment cost was US$2299 per head, with cost of purchasing the feeder cattle the highest cost, followed by feed cost (Table 5). Feed cost was the only cost to vary among treatments, and had an impact on net profit. Profit from cattle fed Napier grass diets was two to three fold higher (P < 0.01) than that from cattle fed OPF diets. Although the unit cost of OPF was much cheaper than that of cut grass (Table 1), the higher DMI, and lower feed efficiency, of cattle fed OPF diets, which increased the feeding cost but not growth rate, was the primary reason for the lower profit than with cattle fed Napier grass. While supplementation of OPF with bypass fat increases ADG, the high cost of further increased feed cost leads to the lowest profit among the four treatments.

Table 5.  Average cost and return (US$ per head) of fattening cattle farming using different TMR
Napier grass–fat, fresh chopped grass in total mixed ration without bypass fat; Napier grass+fat, fresh chopped grass in total mixed ration supplemented with bypass fat; OPF–fat, oil palm fronds in total mixed ration without bypass fat; OPF+fat, oil palm fronds in total mixed ration supplemented with bypass fat; FOR, forage type; FAT, bypass fat supplement. The timeframe for estimation of costs was 255 days fattening period and based on per animal. s.e.m., standard error of the mean. Values within a row followed by different letters are significantly different (at P = 0.05)

The above finding is rather unexpected from the perspective of our intention to promote the use of OPF as animal ruminant feed. However, in the present study, it was assumed that there was no limitation in the supply of cut forage, which is not always true, particularly during the dry (low-yield) and raining (difficult to harvest) seasons. In contrast, by-products such as OPF, which are abundantly available, can be preserved in the form of silage and fed to animals throughout the year. In fact, feeding a mixture of cut grass and various agro-industrial by-products such as OPF or rice straw has been shown to be viable and is commonly practiced by farmers in Malaysia (Wong et al. 2012), Thailand (Chanjula et al. 2017; Hamchara et al. 2018) and other developing countries in Asia, such as Bangladesh (Siddque et al. 2015).

Results of the present study showed that although OPF-based diets were marginally cheaper than grass-based diets, the higher DMI of cattle fed OPF diets was not accompanied by higher ADG, making feeding of OPF diets less profitable. While the growth rate of cattle fed OPF diet can be improved by supplementation of bypass fat, the high cost of bypass fat made it uneconomical, unless there is demand for high-quality beef, and consumers are prepared to pay a higher price.

The authors declare no conflicts of interest.