Cassava leaves for monogastric animals

http://www.mekarn.org/procKK/phuc.htm

 

Nutritive value of cassava leaves for monogastric animals

Bui Huy Nhu Phuc, Brian Ogle* and Jan Erik Lindberg*

University of Agriculture and Forestry,
  Thu Duc, Ho Chi Minh City, Vietnam
*
Swedish University of Agricultural Sciences, 
PO Box 7024, SE-750 07 Uppsala, Sweden.

Abstract

Leaves from varieties of cassava (Manihot esculenta Crantz) growing in South Vietnam were collected at the time of harvesting the roots and analysed for their nutrient and cyanide content. Nutritional properties of the dried and ensiled cassava leaves were determined with pigs and rats.

The crude protein of cassava leaves ranged from 240 to 350 g/kg, and the crude fibre from 100 to 150 g/kg on a dry matter basis. It was found that the HCN content was markedly reduced by both drying and ensiling, with the reduction being highest after sun-drying and oven-drying. The ileal and total tract apparent digestibilities in pig and rats of organic matter, crude protein, nitrogen free extractives and energy, and nitrogen retention, were negatively affected by inclusion of cassava leaves. The impaired amino acid profile after drying cassava leaves at 105 oC was found to be related to a slight decrease in digestible protein as well as N retention.  Average ileal digestibility coefficients of organic matter, crude protein and crude fibre in cassava leaves were 0.42, 0.37 and 0.35; total tract digestibility coefficients were 0.57, 0.46 and 0.55, respectively. The average digestible energy content was 11.7 MJ/kg DM and average apparent ileal digestibility of essential amino acids was 0.56.

It was concluded that, under tropical conditions, the low levels of inclusion of leaves from mature cassava plants may be useful in diets for growing pigs to improve the dietary protein supply. Sun-drying and ensiling with cane molasses as additive successfully preserved the nitrogenous constituents and could be a means of preserving fresh green feed.

 Keywords: Pigs, rats, cassava leaves, amino acids, nitrogen utilization, digestibility,  HCN.

 Introduction

In view of the predicted world shortage of cereal grains because of competing needs for the expanding human population, the availability and supply of grains and protein feedstuffs for livestock is likely to become more limited (Close 1993), and more research into the use of non-conventional sources of energy and protein for livestock production has been called for.

Cassava (Manihot esculenta Crantz) is a widely grown crop in most countries in the tropical regions of Africa, Latin America and Asia, and ranks as one of the main crops in the tropical countries (Calpe1992). Cassava is extremely reliable to grow, especially on sloping rain-fed soils of low fertility, survives drought periods and grows well with limited supplies of water. In addition, it is tolerant of acid soils and yields well on marginal soils without excessive use of costly inputs. These qualities have endeared cassava to resource-poor farmers.

Considerable amounts of cassava leaves are readily available as a by-product at the time of harvesting the roots. However, in the rainy season it is difficult to sun-dry, and extending the drying period diminishes the nutritional quality of the product. Ensiling could be a suitable alternative way of preserving the leaves. Numerous reports have shown that cassava leaf has a high but variable protein content (170 to 400 g/kg on a dry matter basis), with almost 0.85 of the crude protein fraction as true protein (Ravindran 1993). While cassava leaf protein is low in sulphur amino acids (Gomez and Valdivieso 1984), the content of most other essential amino acids is higher than in soya bean meal (Eggum 1970).  The high protein content and a relatively good profile of essential amino acids are reasons for believing that cassava leaves could be a potential protein source for monogastric animals.

Chemical composition of cassava leaves

The present studies have demonstrated that there is considerable variation in the chemical composition among leaves of different cassava varieties (Table 1), which is in agreement with earlier reports (Ravindran 1990; Eggum 1970). The variation could be due to differences in plant development as well as in the ratio of leaf/stem. The leaf products were characterized by a higher crude protein content as compared with the stems, while the NDF contents of the leaves were correspondingly lower. Therefore, a further separation of the leaves from the structural plant elements would probably have resulted in an upgrading of their nutritive value.

Table 1. Nutrient content  (g/kg DM) of leaves of some varieties of cassava grown in South Vietnam

Variety / source

Crude protein

Ether extract

Crude fibre

NFE

Ash

KM94

347

133

120

338

62

India

310

141

117

317

78

Gon

285

135

146

355

79

Japan

271

146

101

421

61

KM60

254

144

97

455

50

KM95

239

156

107

439

59

The cassava leaf products investigated in the present study were found to be high in crude protein (21 to 34 % of DM), and had an acceptable amino acid profile (Table 2), in comparison with,  for example, alfalfa and soybean meal (Figure 1) (Phuc and Lindberg 2001). The contents of threonine in cassava leaves were quite acceptable compared with the ideal amino acid pattern for pigs, while the concentration of methionine and cystine, would be limiting (NRC 1998). The amino acid composition of cassava leaves is therefore of great importance when they are used as protein sources for monogastric animal species.  

Table 2. Chemical composition (% of DM), and essential amino acid (EAA) and non-essential amino acid (NEAA) content (g per 16 g N) and energy content (MJ/kg DM) in two batches of cassava leaves

 

Batch A

 

Batch B

 

Sun dried

Dried
60 oC

Dried
105 oC

Sun dried

Ensiled

Chemical composition

 

 

 

 

  Organic matter

92.8

92.4

92.8

91.4

92.8

  Crude protein

32.4

32.7

32.2

33.3

31.7

  Ether extract

6.4

7.5

8.2

7.2

8.1

  NDF

27.5

25.3

37.6

24.4

24.8

 Gross energy

-

-

-

21.4

21.2

Essential amino acids

 

 

 

 

   Arginine

6.3

6.4

5.8

6.5

5.6

   Histidine

2.2

2.0

2.0

1.8

1.7

   Isoleucine

4.1

4.4

4.5

4.2

4.2

   Leucine

8.7

8.9

9.1

8.3

8.3

   Lysine

5.1

5.1

4.2

5.5

5.4

   Methionine

1.6

1.4

1.5

1.6

1.4

   Phenylal.

6.3

6.2

6.2

6.2

5.6

   Threonine

4.4

4.2

4.4

4.1

3.9

   Tyrosine

4.3

4.6

4.6

4.4

4.4

   Valine

5.9

5.6

5.7

5.6

5.3

S EAA

48.9

48.8

48.0

48.2

45.8

Non-essential amino acids

 

 

 

   Alanine

6.3

6.5

6.4

6.0

6.4

   Aspartic acid

9.7

9.4

9.6

10.3

9.3

   Glutamic 

11.0

10.4

10.7

9.3

9.6

   Glycine

4.5

4.4

4.8

4.3

4.1

   Proline

3.8

3.7

3.6

4.1

4.3

   Serine

3.4

4.1

4.2

3.3

3.8

S NEAA

38.7

38.5

39.3

37.2

37.5

S AA

87.6

87.3

87.3

85.5

83.3

 

 


Figure 1. Amino acid contents of cassava leaves (CL), alfalfa and soybean meal

 Increased levels of protein replacement by cassava leaf protein in pig diets at the  expense of soybean, or in rat diets of casein, led to increased fibre contents of the diets (Phuc et al 2000, 2001a; Phuc and Lindberg 2000). The reduction of feed intake was noted in both the rat and pig experiments at high levels of inclusion of cassava leaves. This was partly due to the increased content of dietary fibre but also possibly to antinutritional factors present in the leaves. Most soluble polyphenolics have a bitter or astringent taste (Van Soest 1994; Kumar and D’Mello 1995), which would also tend to reduce intakes. The bitter taste of cassava leaves has been attributed partly to the presence of tannins as well as high HCN levels, also seen in other studies, for example by Mahendranathan (1971). The results show that consumption problems occured at inclusion levels of more than 10% and 15% of dry matter in diets for rats and pigs, respectively. 

Effect of inclusion of cassava leaves on digestibility and nitrogen retention

Our studies have clearly demonstrated that increasing levels of inclusion of cassava leaves  in diets for rats, as well as for growing pigs, lowered the ileal and total tract digestibility of organic matter and crude protein (Table 3). Figure 2a,b demonstrates the relationship between the dietary fibre (NDF) content and digestible organic matter for rats and pigs (Phuc and Lindberg 2000; Phuc et al 2001a).

Figure 2a: Effect of level of dietary NDF on digestibility of organic matter in  rats

 

Figure 2b: Effect of level of dietary NDF on digestibility of organic matter in  pigs

This can be explained by differences in chemical composition between the basal diet and the leaves, and the depressive effect of fibrous constituents on the apparent digestibility of the non-fibrous components of the diet (Stanogias and Pearce 1985a,1985b; Fernandez and Jřrgensen 1986). The negative effects of dietary fibre are partly a result of a reduced transit time of the ingesta in the small intestine caused by fibrous components, limiting the time for nutrient digestion and absorption (Den Hartog et al 1985; Sarwat et al 1986;). The extent of the reduction in digestibility has been shown to vary with the level of fibre and the feeding level (Oke 1990; Dierick et al 1989; Ravindran 1990). Furthermore, anti-nutritional factors in the cassava leaf products may have interfered with the process of digestion (Makkar 1993). Tannins are known to occur in cassava leaves (Ravindran 1993; Oke 1994), which may have adversely affected digestibility of crude protein.

Our study with pigs (Phuc and Lindberg 2000) has shown that part of the dietary fibre had been digested at the terminal ileum and that this slightly increased with the incorporation of cassava leaves in the diets (Table 3). This suggests that the pigs were able to digest a substantial part of plant fibre pre-caecally, which is in agreement with earlier reports (Dierick 1989; Andersson and Lindberg 1997a,1997b). 

Effects of inclusion of cassava leaves on digestibility of AA at the terminal ileum

Most of the amino acids were digested to a greater extent than the crude protein (Phuc and Lindberg 2001). The reduction in apparent ileal digestibility of essential amino acids when cassava leaves were included in the diets was due to an increase in the ileal flow of amino acids with increasing fibre content in the diets, as reported by Reverter et al (1999). Furthermore, an increase of endogenous amino acids secretions could also be expected (Sauer and Ozimek 1986; Boisen and Moughan 1996; Jondreville et al 2000). The magnitude of this effect will depend on the digestibility of the basal diet, the level and type of the fibre and the contribution of the fibre source to the dietary amino acid supply (Lenis et al 1996). In addition to fibre level and quality, the presence of tannins and enzyme inhibitors (Kidder and Manner 1978) might also influence the digestibility of protein and amino acids. The estimated apparent ileal digestibilities of histidine, lysine  and tyrosine were found to be highest, while that of threonine was the lowest (Table 4). 

Also the low arginine digestibility of cassava leaves could be due to the binding of this amino acid to lignin (Nongyao et al 1991). The average apparent ileal amino acid  digestibility was 0.56, close to the value reported for perennial ryegrass meal (0.61) (Reverter et al 1999).  

Table  3. Estimated  ileal and total tract digestibility coefficients of nutrients and energy (%) in cassava leaves in pigs

 

Ileal digestibility

Faecal digestibilty

 

sun-dried

ensiled

sun-dried

ensiled

 

Mean

s.d

Mean

s.d

Mean

s.d

Mean

s.d

Organic matter

0.41a

0.03

0.42 a

0.04

0.54 a

0.03

0.59 a

0.05

Crude protein

0.37

0.02

0.37

0.03

0.45

0.04

0.46

0.02

Crude fat

0.34 a

0.02

0.41 b

0.03

0.36 a

0.02

0.43 b

0.03

NFE

0.38

0.06

0.40

0.09

0.65

0.09

0.60

0.09

Crude fiber

0.34 a

0.06

0.37 a

0.04

0.50 a

0.03

0.59 b

0.03

NDF

0.26 a

0.04

0.23 a

0.02

0.32 a

0.02

0.31 a

0.02

ADF

0.16 a

0.02

0.17 a

0.02

0.20 a

0.03

0.21 a

0.04

Energy

0.40 a

0.06

0.41 a

0.07

0.52 a

0.04

0.57 b

0.05

ab Means with different superscripts within rows are significantly different (P<0.05)

Table 4. Estimated apparent ileal digestibility of crude protein, and essential and non-essential amino acids in sun-dried and ensiled cassava leaves

 

Sun-dried

Ensiled

 

Mean

s.d

Mean

s.d

Crude protein

0.37

0.02

0.37

0.03

Essential amino acids

 

 

 

  Arginine

0.50a

0.07

0.56 a

0.05

   Histidine

 0.61

0.05

 0.68

0.03

   Isoleucine

0.48 a

0.02

0.45 a

0.04

   Leucine

0.50 a

0.03

0.57 a

0.02

   Lysine

0.64 a

0.04

0.64 a

0.04

   Methionine

0.56 a

0.03

0.55 a

0.04

   Phenylalanine

0.55 a

0.05

0.52 a

0.06

   Threonine

0.52 a

0.07

0.54 a

0.02

   Tyrosine

0.64

0.06

0.61

0.03

   Valine

0.60 a

0.05

0.62 a

0.03

Non-essential amino acids

 

 

   Alanine

0.56 a

0.02

0.57 a

0.04

   Aspartic acid

0.60 a

0.04

0.62 a

0.03

   Glutamic acid

0.55 a

0.08

0.53 a

0.04

   Glycine

0.50 a

0.06

0.54 a

0.08

   Proline

0.62 a

0.04

0.57 a

0.07

   Serine

0.62 a

0.03

0.61 a

0.04

ab Means with different superscripts within rows are  different (P<0.05)

 

Effect of inclusion of cassava leaves on N retention and weight gains 

The utilization of N deteriorated with increasing inclusion of  cassava leaves. The most likely explanation for this is a low digestibility of cassava leaves protein and a poorer amino acid profile. In addition, the protein of cassava leaves is, compared with the basal diet, deficient in the sulphur-containing amino acids (Eggum 1970; Yeoh and Chew 1976), and these may be used in the detoxification of HCN (Oke 1978, Ravindran 1993). This could further have imposed limitations on the efficiency of amino acid utilization from HCN-containing cassava leaves in the present study. Stepwise regression analyses indicated that methionine as well as lysine were the major limiting amino acids for N retention as well as biological value (Phuc et al 2001). The cassava leaf-based diets generally resulted in inferior weight gains of the animals compared with the control diet, despite calculated isoenergetic feed supply. 
 

Effect of preservation techniques on chemical composition of cassava leaves

Ensiled cassava leaves tended to have higher digestibility coefficidents than sun-dried leaves (Table 3), but differences were only significant for crude fat. Sun-drying had only a small effect on the crude protein content compared to the 60oC oven- drying of CLM, which is in agreement with earlier studies (Ravindran et al.1987). However, after drying at 105 oC Maillard reactions occurred and lysine content was clearly lowered in CLM105 (4.2 g per 100 g crude protein versus a value of about 5 g in the other cassava treatments, Table 2), most likely due to the formation of lignin-like polymers, which also resulted in a higher fibre content (Van Soest and Mason 1991). Therefore, rats fed diets with inclusion of cassava leaves dried at 105 oC had clearly reduced N utilisation as well as weight gain as a result of the lower digestible protein and lysine content (Phuc et al 2001b).

Ensiling had only a limited effect on the content of EAA as compared with drying (Table 2). The high content of lactic acid (83.6 g/kg) and low content of ammonia (3.5 g/100 g N) as a percentage of total N also confirmed the ideal ensiling conditions (Van Soest 1994) resulting from cane molasses addition (Phuc et al 2001b). However, the unpleasant taste and/or smell related to the low pH and the occurrence of organic acids in the ensiled products were possibly the cause of the reduced feed intake in rats. The negative influences on digestibility of organic matter, crude protein and N utilisation, which also reduced the weight gain of the rats, were observed when the silage cassava leaves  were included in the diet.

 Hydrogen cyanide (HCN)

The HCN content varied among the varieties, from 285 to 762 mg/kg DM. It seems that the slow drying rate achieved by sun-drying resulted in an increase of cyanogenic activity, thereby eliminating cyanides as compared with the fast artificial drying at 60 oC, which is in line with earlier work (O’Brien and Jones 1994) (Phuc et al 2001). However, at 105 oC the drying temperature had a marked effect on the cyanide content of cassava leaves  and their consequent toxicity (Ravindran 1993; Nambisan 1994; Oke 1994). The higher total HCN content in cassava leaf silage as compared to cassava leaf meal (Table 5) is confirmed by other studies (Gomez and Valdiviesi 1988; Oke 1994; Westby 1994).  

Table 5. Contents of total HCN, intermediary products (cyanohydrine), free HCN and glucoside (linamarin) (mg/kg DM) of cassava leaves

 

Cassava leaves  A

Cassava leaves B

 

Sun dried

Dried 60 oC

Dried 105 oC

Sun dried

Ensiled dried

Total HCN

59

86

28

255

250

Cyanohydrine

13

47

1

152

215

 Free HCN

13

33

9

62

5

 Linamarin

33

6

18

42

30

HCN content of ensiled cassava leaves (not dried): total HCN: 762; Cyanohydrine: 673;  Free HCN: 17 and Linamarin: 73.

It can be concluded that drying and ensiling are effective ways of reducing the toxicity of cassava products, which is in agreement with the conclusion of Twe (1991). There were no indications of cyanide toxicity on any of the diets in the present study in the rat as well as the pig experiments, for both sun-dried and ensiled cassava leaves (Phuc et al 2000; Phuc et al 2000a,b; Phuc and Lindberg 2001). This finding contrasts with the recommended safe level of HCN in the diet, which is below 50 mg HCN/kg according to Bolhuis (1954), a level which was not achieved in any of the diets tested. 
 

Estimation of the nutritive value of cassava leaves in rats and pigs

The chemical composition of the cassava leaves tested with rats and pigs and their nutritive value estimated by the difference and regression methods are shown in Table 6. The present data do not allow testing of the hypothesis that estimates of the nutritive values assessesed with rats are applicable to pigs, as the chemical composition of cassava leaves used for the two animal species were different, and also because the number of products tested was too limited. 

Table 6. Energy (GE, MJ per kg DM), crude protein (CP) and NDF (% of DM), digestibility coefficients (%) and estimated digestible energy content (DE, MJ/kg DM) of cassava leaves investigated in pigs and rats

 

CLM

ECL

 

Rats

Pigs

Rats

Pigs

 

I

I

 II

II

I

III

IV

Chemical composition

 

 

 

 

GE

21.3

19.2

21.4

-

18.4

21.2

-

OM

92.8

91.4

91.3

89.1

92.8

89.5

89.7

CP

32.4

33.3

26.4

26.0

31.7

24.5

27.6

NDF

24.5

27.4

32.1

33.5

24.8

32.6

33.5

Digestibility

 

 

OM

59

59

54

51

60

59

52

CP

61

59

45

44

62

46

59

DE

11.5

11.3

11.0

-

11.0

12.0

-

I Phuc et al 2001a; II Phuc et al 2001b; III. Phuc and Lindberg 2000;  IV Phuc et al 2000

 

Practical considerations

The present studies have demonstrated that growing pigs have the capacity to utilize the nutrients and energy of cassava leaves. However, the potential benefits of an early harvest of the leaves (eg: when it is managed as a forage; Preston 2001) should be stressed. A separation of leaves and stems could further improve the nutritional properties of the cassava biomass, and this would be more critical for pigs. As the capacity of the pig to digest fibrous components improves as the pig matures (Kenneth et al 1990) this strategy would be most beneficial for the nutrient supply of piglets, young growing pigs and lactating sows, which  have high demands for nutrients.  

Cassava leaves contain more protein and amino acids per energy unit than cereal grains, thereby also reducing the need for protein supplements. However, the content of crude protein in cassava leaves as well as its digestibility, is much lower than that of soybean meal or other traditional protein supplements. Therefore, it is necessary to determine the extent to which they can contribute to the supply of nutrients for different categories of animals, as well as their nutritional limitations, especially antinutritional factors. If these are known, feeding strategies based on cassava leaves could be developed that would provide an adequate supply of both energy and protein to meet the animals’ nutritional requirements. 
 

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