Nutritive and antinutritive contents of Indigofera zollingeriana: Its potency for cattle feed in Indonesia

R Antari, Y N Anggraeny, A S Putri, P K Sukmasari, N H Krishna Mariyono, M N Aprilliza¹ and S Ginting¹

The Indonesian Beef Cattle Research Station, Grati, Pasuruan 67184 East Java Indonesia
risa.antari@uq.net.au
¹ The Indonesian Goat Research Station, Sei-Putih 20585, North Sumatera, Indonesia

Abstract

The main issue in improving the population of beef cattle in Indonesia is providing nutritious feed as well as enough in quantity, especially in the dry season. Tree legumes are the common feed for goats and can be potentially used for cattle feed because the farmers usually use agricultural by-products that have low nutritive values. Indigofera zollingeriana is well adapted in Indonesia and has been growing since early 2000. It has a high protein content (28-34%), low crude fiber (12-16%), and total digestible nutrient (69-72%) depending very much on the parts of the plant. The nutrient content in the legume enables the legume to be combined with the agricultural by-products and resulted in a good quality feed for cattle. Besides, the legume also has antinutritive content such as saponin (0.8-1.2%) and tannin (2.4-7%). The antinutritive content should be taken into consideration in using I.zollingeriana as a source of protein diet. It is important to find the amount of I.zollingeriana that should be provided for safely use of cattle feed.

Keywords: fiber, protein, saponin, tannin, tree legumes

Introduction

The strategic program from the Indonesian government is to produce the meat that can supply the domestic demand for beef meat. The beef cattle population in Indonesia in 2020 was 17,466,792 heads and East Java province contributes to around 28% of the national population. While the demand for beef meat was around 400,000 tons a year that can be supplied 50% from the domestic population.

The main obstacle for increasing the population of cattle in Indonesia is providing feed that is not only nutritious but also enough in quantity, this is because feed scarcity occurs in the dry season in almost all provinces in Indonesia. The readily available feed sources for cattle are from agricultural by-products that are usually lignified, have low energy, protein, and mineral, high in crude fiber, and have low total digestible nutrient (Agus 2015; Lunagariya et al 2017) that is hard to be digested by the rumen microbes. Therefore, the nutritive content of the feed needs to be improved. There is a necessity to find other nutritious feed sources that do not compete with human needs.

In Indonesia, there is a wide range of roughage sources that can be given to ruminants. One of the options is green fodders that are from agricultural by-products (e.g., rice straw, corn stover, sugarcane shoots) that are commonly used for cattle feed. Another source of forage is tree legume that can increase the nutritive values as well as the production of cattle (Panjaitan et al 2013) and another success story of tree legume used for cattle (see a publication by Dahlanuddin et al 2019). Tree legumes contain crude protein 21-27% (Ali et al 2021; Rusdy et al 2019; Ahmed et al 2018). So, tree legume is a potential feed source that has high nutritive value to improve agricultural by-products-based feeds for cattle.

Indigofera zollingeriana is a tropical tree legume that has high nutritional contents. Jayanegara et al (2019) showed that dried I. zollingeriana had 35% of crude protein content, while ensiling caused lower CP content (26%). Farmers in Indonesia have used I. zollingeriana for feeding their livestock and the legume has been reported to increase the production of livestock especially goats (Tarigan et al 2018). However, there is a dearth of information about the use of Indigofera as cattle feed. Therefore, this paper aimed to show the potency and its limitation of I. zollingeriana as cattle feed.

Photo 1. Nursery of Indigofera zollingeriana (North Sumatera-Indonesia)	Photo 2. Nursery of Indigofera zollingeriana, 1.5 months old (in North Sumatera-Indonesia)

Photo 3. The old tree of Indigofera zollingeriana in the dryland East Java, the regrowth period is about 40 days	Photo 4. The seeds of Indigofera zollingeriana, this tree is usually used for producing the seeds (East Java-Indonesia)
Photo 5. The flower of Indigofera zollingeriana
Photo 6. The pods of Indigofera zollingeriana	Photo 7. The seeds of Indigofera zollingeriana

Materials and methods

The study was conducted from July to December 2020. The sample collection was done by harvesting the existing I. zollingeriana trees from three different sites (Probolinggo, East Java as represents upland and lowland), South Kalimantan (represents site having acid soil, peatland), and North Sumatera (represents low, middle, and upland and has high acid soil). The plants were cut 1.5 m above the surface. The plants then left for 2 months for regrowth and sample collection. The samples were collected from many parts of the plants (the whole plants, leaves, and stems). The samples were then weighed, dried and the dry weight was recorded. The dried samples were then grounded and proximate analysis was conducted based on AOAC (2005) and the content NDF and ADF were analyzed according to Van Soest (1991) and Spectrophotometry UV-vis for analysis of antinutritional contents. The data was then analyzed descriptively.

Results and discussion

Indigofera zollingeriana is well adapted to many types of soils

Indigofera zollingeriana is a tree legume containing high protein and is well adapted to many types of lands, e.g. dry, muddy, high salinity, acidic soil (Nadir et al 2018; Herdiawan and Krisnan 2014). In the eastern part of Indonesia, most of the land is dry with very low rainfall. Whereas acid soils dominate in the northern part of Indonesia. Not all grasses and forages can be grown in these types of soils. Therefore, it is needed to provide forage that can be grown in many types of soils to provide nutritious forage for ruminants.

In the dry season, I. zollingeriana can produce leaves even when the water is scarce. It has a physiological mechanism with proline expression and interaction with mycorrhizae hypha enabling the legume to produce leaves and hold the water during the dry season (Abdullah 2014). Therefore, Indigofera has a potency to be used as a feed supplement in the dry land and dry season.

Moreover, the survival life of this legume in acid soils is also high. The main issue in acidic land having a low pH (≤5.5) is a high concentration of Al³⁺. That Al³⁺ suppresses the growth of the plants and their production (Meriño-Gergichevich et al 2010). Herdiawan and Krisnan (2014) showed that Al³⁺ in the leaves, stems and roots of I. zollingeriana is lower thanCalliandra calothyrsus and Gliricidia sepium. I. zollingeriana does not show a symptom of toxicity because it can eliminate the Al³⁺ in all parts of the plants and has a good morphological condition when they were grown in acidic soil. Therefore, Indigofera is well adapted to acid soils.

Nutritive content of Indigofera zollingeriana

The proximate analysis of I. zollingeriana (Table 1) showed that the nutritive value depends very much on the parts of the plants. This may be related to soil fertility. Syamsuddin et al (2016) stated that the nutritional content especially the crude protein of the plants is affected by soil fertility and the use of fertilizer.

The dry matter content of the whole plant was recorded relatively high. This was probably because the stem and branches were included in the sample. The stem itself has >90% of DM content, except the samples taken in East Java that had slightly low DM content. Similarly, the ash content is also relatively high in whole plant samples. Both leaves and stems had comparable ash contents. The variety was high because the ash content from samples taken in East Java was low.

The CP content of I. zollingeriana reaches 30% on a DM basis. The whole plant samples had >30% CP content. Our results were slightly higher than a result reported by Tarigan et al (2018) and Telleng et al (2020) who found I. zollingeriana had 26-28% CP. In Indonesia, the common CP content of commercial concentrate for beef cattle was around 12-16%, therefore, I. zollingeriana might substitute the commercial concentrate as a protein source. Moreover, studies reported that the palatability of feed containing I. zollingeriana in preweaning calves (Rianty 2020) and goats (Wahyudi 2019) were good, although the published data about the palatability of I. zollingeriana in mature beef cattle were very limited. Therefore, a feeding strategy of I. zollingeriana as cattle feed should be taken into consideration because goats and cattle have different eating behaviour.

The variety of crude fiber content of I. zollingeriana was low. Regardless of the plant parts, the CF content was from 12 to16 %. This was because the samples were harvested within a relatively narrow range of maturity stages. Our results are comparable to those reported by previous studies (Tarigan et al 2018; Kumalasari et al 2017) but slightly lower than another study that can reach 21% (Suharlina et al 2016). The difference is probably because of the age at which the tree legumes were harvested. Because of low CF content, the legume is expected to have high DM digestibility. For example, the DN digestibility was >76% in goats fed a green concentrate diet containing I. zollingeriana (Tarigan et al 2018) while DM digestibility in male growing goats offered a diet containing 30% of I. zollingeriana and 70% of Pennisetum purpureum cv Mott, was >80% (Jusman 2019). Another study showed that the inclusion of 20% I. zollingeriana increased DM digestibility (Suharlina et al 2016). A laboratory test of in vitro digestibility of I. zollingeriana for DM, OM, and CP of this legume were 68-73%, 65-71%, and 87-91%, respectively (Suharlina and Abdullah 2010). The low content of CF can facilitate the utilization of feed by ruminant microbes, which in turn induce higher fermentation rates and improve digestibility (Van Soest 1994). Conversely, diets containing high fiber and low protein are negatively correlated with digestibility coefficients in sheep, goats, cattle, and buffalo (Riaz et al 2014). Thus, Indigofera may replace concentrate feed in the diet.

The total digestible nutrient (TDN) content of I. zollingeriana was high (>69%) in all parts of the plants. The TDN value represents the energy content that can be used for livestock to survive (Jayanegara et al 2019). This determines the production of animals for meat or milk for human consumption. The values of TDN in our study showed high energy content of I. zollingeriana, Hall, and Eastridge (2014) showed that the energy sources come from calories and absorbable nutrients that can be metabolised by the animals to produce energy or can be used for anabolic purposes. The energy is used for both microbial and host-animal requirements. The TDN content in our study was comparable to another study (Telleng et al 2020) as well as to other tree legumes such as Gliricidia (68%) (Adrizal et al 2021), Leucaena 80%, and Sesbania 75% (Tahuk et al 2017).

The neutral detergent fiber (NDF) content of I. zollingeriana varied depending on the site where the samples come from. The samples taken from South Kalimantan had an NDF content of 36-38%, the samples were harvested from I. zollingeriana trees grown in peatland that has high acid soil. A published article showed that Indigofera grown in an acid soil resulted in high NDF content, >35% depending on the age of the harvest time (Ali et al 2021), the peatland is a type of soil that has low fertility and high acidity, therefore, not all types of trees or grasses can be well grown in this type of soil.

There was a great variation of ADF content, for example, the ADF content in leaves taken from low land East Java was relatively high. But the ADF content in leaves was low in stem from upland East Java. The whole plant sample taken from low land in North Sumatera had high ADF content. The ADF content can be used as an index of the percentage of indigestible material in the forage, it represents cellulose, lignin, and silica (Newman et al 2009). The ADF content in our result was relatively higher than the ADF content of other tree legumes (Gliricidia sp. was 6.8% DM (Rusdy et al 2019); Leucaena lencephala was >31% (Sulistijo et al 2020) that also depending on the seasonal changes. This indicated that sites, soil type, and environmental conditions affected the NDF and ADF content of Indigofera.

Antinutritive contents of Indigofera zollingeriana.

The antinutritive contents of Indigofera (Table 2) showed that the tannin content varied. Our results were comparable to the result reported by Tarigan et al (2018) ranging from 0.85 to 4.66%. The amount of tannin content in the legume trees might impede the digestibility for the animals, although <5% of tannin content does not affect the animals and potentially prevent the protein degradation in the rumen and improve the feed efficiency and productivity of the ruminants (Ahmed et al 2018). Excess content of tannin may negatively affect the plane of nutrition for ruminants, the high content of tannin usually occurs in tropical plants (Aboagye and Beauchemin 2019). Therefore, a low concentration of tannin is beneficial for ruminants.

The tannin contents of the samples taken from South Kalimantan as represent of peatland were similar both from wet and drylands. While the whole plant samples from North Sumatera showed slightly different tannin content between upland and the lowland. Interestingly, the tannin content of leaves taken from upland was double from those samples taken from lowland in East Java, conversely; the samples from stem part taken from low land were double in comparison with those taken from upland. Overall, tannin content collected from all parts and sites was higher than those reported from a previous study, about 0.8% DM (Tarigan et al 2018). The variety of the values was probably caused by some factors such as soil types, maturity stage of the plants, elevations, and management system (fertilizer, water, planting distance, etc).

There was no big variation of saponin content taken from different elevation and soil types, except for the stem samples taken from lowland East Java had high saponin content. The results from the current experiment were higher than other studies reported previously, at about 0.4 % (Herdiawan and Krisnan 2014a). A study reported that the inclusion of saponin in the diet at >0,8% may reduce DM and OM digestibility (Jadhav et al 2017), but another study reported that feed containing saponin improve the apparent OM, N, NDF, and ADF digestibility as well as suppress methane emission (Liu et al 2019). The feeding strategy of fresh Indigofera for ruminants especially cattle should be more careful by withering under the sun because high saponin content can be decreased by increasing the temperature (Gunawan 2018).

Indigofera zollingeriana and its potential for cattle feed

Indigofera has potential as cattle feed because it has a high content of protein and TDN (Table 1), which is higher than available commercial concentrate in Indonesia, ranging from 12-16% of CP content and around 65% of TDN content. The price for concentrate diets with those specifications is around 4000 IDR/kg (in 2021) depending very much on the protein content. This price is expensive for smallholder farmers in Indonesia. There is a necessity to find diverse alternative feed sources that are affordable, close to their residential areas, and most importantly can be supplied throughout the years.

Although tree legumes have been reported as protein sources for ruminants (Mataveia et al 2019; Rusdy et al 2019), they also have antinutritive content that should be taken into consideration in using them as feed. This is because antinutritive contents that appear in tree legumes may decrease their benefits as nutritious forage for ruminants (Ahmed et al 2018). Depending on the types of ruminants, tree legumes may need special treatment before feeding to the ruminants, the toxicity may be low but a high tannin content can decrease feed intake. Waghorn (2008) reported that it is related to the digestibility of tree legumes. So, in cattle, tree legumes may only be used as a supplement. This may be a different case in goats as they are usually fed tropical pastures and easily adapt to forages containing high tannin in comparison with other ruminants. This is because goats have salivary protein (proline or histatins) binding to tannins causing a defensive mechanism that prevent the negative effects of feed containing tannin consumption (Shimada 2006).

Although high anti-nutritional compound (tannin) containing tree legumes may have deleterious effects on the ruminants (reduce digestibility and intake), tannin also contributes to the mitigation of methane emissions by suppressing methanogenesis in the rumen (Fagundes et al 2020; Aboagye and Beauchemin 2019), and divers beneficial effects of tannins for ruminants (for reference see Huang et al 2018)). Unlike non-ruminants, ruminants can denaturize the anti-nutritional content in the tree legumes in the rumen. The deleterious effects of toxins are measured by the degradation rate of the rumen microbiome, and then affect the productivity of ruminants (Lakshmi et al 2020). Thus, tannin content may have both benefits and harmful for ruminants, a feeding strategy is needed for the safe use of tree legumes.

Do we need to remove tannin from the tree legumes? A study reported that tannin can be removed from the cassava leaves using a fermentation technique with Saccharomyces cerevisiae (Hawashi et al 2019), other methods that can be used include wilting, drying, and ensiling were reduce tanning contents from tree legumes (Lakshmi et al 2020). However, from our view, the best method for feeding ruminants with tree legumes containing tannin is using a good feeding management practice, understanding the level of tree legumes for cattle becomes important to derive the benefits of its nutritional contents and prevents the harmful of antinutritional contents of tree legumes. Studies have reported that the maximum level of Leucaena leucochephala or Gliricidia sepium was given to cattle is 30% of the total diet and mixing with other non-legume fodders (Lakshmi et al 2020). However, there is no published data available on how much I. zollingeriana should be provided to cattle in appropriate quantities depending on management practices for safe use of the tree legume.

Conclusion

• To conclude, I. zollingeriana is a nutritious tree legume that has high protein and TDN contents. It might be used as a supplement in cattle feed, however; the amount of I. zollingeriana that should be provided needs more studies to achieve the high growth rate and safely use of the legume for beef cattle.

Acknowledgment

The authors wish to thank the Australian Centre for International Agricultural Research (ACIAR) for providing funding for this research, Dr Stuart R. McLennan for his help with the sample collection methods,casual workers, and laboratory staff at BCRI for their help with the current study.

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