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Pakistan Journal of Nutrition 12 (10): 943-948, 2013
ISSN 1680-5194
© Asian Network for Scientific Information, 2013
Corresponding Author: Yose Rizal, Faculty of Animal Science, Andalas University, Padang, West Sumatra, Indonesia
943
Comparisons of Nutrient Contents and Nutritional Values of Palm
Kernel Cake Fermented by Using Different Fungi
Yose Rizal, Nuraini, Mirnawati and Maria Endo Mahata
Faculty of Animal Science, Andalas University, Padang, West Sumatra, Indonesia
Abstract: An experiment has been conducted to compare the nutrient contents and nutritional values of palm
kernel cake (PKC) from different fermentation processes. This experiment was designed in a Completely
Randomized Design (CRD) with six treatments and five replicates. Treatments were A = unfermented PKC
(control), B = fermented PKC with Neurospora crassa, C = fermented PKC with Penicillium sp., D = fermented
PKC with Trichoderma harzianum, E = fermented PKC with Aspergillus niger and F = fermented PKC with
Aspergillus niger+humic acid. Measured variables were nutrient contents (crude protein, crude fiber and
ether extract) and nutritional values (nitrogen retention, crude fiber digestibility and metabolizable energy) of
fermented and unfermented PKCc. Results of experiment indicated that the crude fiber content of fermented
PKCs was very significantly lower (p<0.01) than that of control, but there was no difference (p>0.05) among
the fermented PKCs. Fermentation with different fungi increased (p<0.05) the crude protein content of PKCs
when it was compared with control. The crude protein content of Aspergillus niger and Aspergillus
niger+humic acid fermented PKCs were significantly higher (p<0.05) than that of Trichoderma harzianum,
Neurospora crassa, or Penicillium sp., fermented PKCs or control. The ether extract content of PKC was very
significantly affected (p<0.01) by treatments. Aspergillus niger+humic acid, Neurospora crassa and
Aspergillus niger fermented PKCs possessed the lower ether extract content (p<0.05) than that of Penicillium
sp., or Trichoderma harzianum fermented PKCs, or control. The crude fiber digestibility of Aspergillus niger
or Aspergillus niger+humic acid fermented PKCs was very significantly higher (p<0.01) than that of
Penicillium sp., Trichoderma harzianum, Neurospora crassa fermented PKCs, or control. The nitrogen
retention of Aspergillus niger+humic acid fermented PKC was significantly higher (p<0.05) than that of
Penicillium sp., Neurospora crassa fermented PKCs, or control, but was not differed (p>0.05) from that of
Trichoderma harzianum or Aspergillus niger fermented PKCs. The fermentation with different fungi improved
(p<0.05) the metabolizable energy content of PKC. Thus, the improvement of the nutrient contents and
nutritional values of Aspergillus niger fermented PKC was better than the other treatments.
Key words: Palm kernel cake, fermentation, Aspergillus niger, humic acid, Penicillium sp., Trichoderma
harzianum, Neurospora crassa, nutrient content, nutritional value
INTRODUCTION
Indonesia is the biggest producer of crude palm oil in
the world with the total production of 22.5 million tones
per year. Seventy percent of the total production of crude
palm oil was located in Sumatra Island (BPS, 2010).
With the development of palm oil plantation, it will
produce a huge amount of waste or by-product of palm
oil industry in the form of Palm Kernel Cake (PKC)
because 45-46% of the by-product of palm oil industry is
PKC.
The nutrient content of PKC was as follows: crude
protein 16,07%, crude fiber 21,30%, ether extract
8.23%, Ca 0.27%, P 0.94% and Cu 48.4 ppm
(Mirnawati et al., 2008), so that it can be utilized as an
animal feed. Even though its crude protein content
was rather high, its utilization in poultry diets was not
optimal yet. According to Supriyadi (1997) the PKC could
be included up to 10% in the duck ration and Rizal
(2000) found that PKC could be utilized up to 10% in the
broiler diet to effectively replace 40% soybean meal.
The low in the utilization of PKC in poultry diets was due
to the low in the nutritive value of this PKC. The low in
nutritive value of PKC was related to the high in crude
fiber content, low amino acids content and the high in Cu
content (Nwokolo et al., 1976; Ezhieshi and Olomu,
2004; Mirnawati et al., 2008) and high in $-manan or
mannose polymere (Dusterhof et al., 1993; et al.,
2007). On the other hand, the ability of poultry to digest
crude fiber is limited (Scott et al., 1982).
For increasing the utilization of PKC in poultry diets, the
processing through fermentation had been performed by
using cellulolytic microbes such as: Trichoderma
harzianum, Aspergillus niger and Penicillium sp.
(Sabrina et al., 2001; Nuraini and Yunara, 2001; Aziz
et al., 2003; Harnentis et al., 2005; Mirnawati et al.,
2008), proteolytic such as: Rhizopus sp. (Sabrina et al.,
Pak. J. Nutr., 12 (10): 943-948, 2013
944
2001) and carotenogenic such as: Neurosphora sp.
(Sabrina et al., 2001; Nuraini and Susilawati, 2006).
Poultry response to the utilization of fermented PKC
ranging from 15 to 25% (Sabrina et al., 2001; Nuraini
and Trisna, 2006; Nuraini et al., 2007).
The nutrient content, nutritional value and poultry
response to the utilization of fermented PKC are still
varied, so that it is still necessary to further study the
nutrient quality of processed PKC, so that it can be
utilized in large amount in poultry diets and is available
continuously in the market in the form of complete diets
ready for feeding to poultry.
MATERIALS AND METHODS
This experiment was aimed to study the effect of
fermentation by using different species of fungi on the
nutrient contents and nutritional values of PKC and to
find out the best fungi for fermenting the PKC through the
utilization of Neurospora crassa, Penicillium sp.,
Trichoderma harzianum and Aspergillus niger. They
were also compared with the unfermented PKC. A
Completely Randomized Design (CRD) with 6
treatments and 5 replicates was employed in this
experiment. The treatments were A = unfermented PKC
(control), B = Neurospora crassa fermented PKC,
C = Penicillium sp. fermented PKC, D = Trichoderma
harzianum fermented PKC, E = Aspergillus niger
fermented PKC and F = Aspergillus niger+humic acid
fermented PKC.
The fermentation of PKC by using Neurospora crassa
was performed with the inoculums dose of 9% and
fermentation length of 5 days, Penicillium sp. with
inoculums dose of 6% and fermentation length of 7
days, Trichoderma harzianum with the inoculums dose
of 8% and fermentation length of 7 days, Aspergillus
niger with the inoculums dose of 10% and fermentation
length of 7 days and Aspergillus niger+100 ppm humic
acid with the inoculums dose of 10% and fermentation
length of 7 days. The total amount of substrate used for
each treatment was 100 g, consisted of 80 g of PKC
plus 20 g of rice bran.
Measured variables were nutrient contents (crude fiber,
crude protein and ether extract) and nutritional values
(crude fiber digestibility, nitrogen retention and
metabolizable energy content) of fermented and
unfermented PKCs. Crude fiber, crude protein and ether
extract were determined according to proximate analysis
procedures (AOAC, 1984). Crude fiber digestibility was
measured according to Schneider and Flatt (1975).
Nitrogen retention and metabolizable energy were
performed according to McDonald (1981) and Sibbald
(1975), respectively.
Data were analyzed by analysis of variance of CRD.
Duncan Multiple Range Test (DMRT) according to Steel
and Torrie (1980) was performed for testing the
difference among treatments.
RESULTS
Effect of treatments on the crude fiber content of palm
kernel cake: The means of crude fiber content of
fermented and unfermented PKCs were illustrated in
Table 1.
The result of the analysis of variance indicated that
the crude fiber content of PKC was very significantly
(p<0.01) influenced by the treatments. The crude fiber of
PKC fermented with Neurospora crasa, T. harzianum,
Phenicillium sp., Aspergillus niger, or Aspergillus
niger+humic acid was not differed (p>0.05). However,
the crude fiber content of all fermented PKCs was very
significantly lower than that of unfermented PKC.
Effect of treatments on crude protein content of palm
kernel cake: The effect of treatments on the crude
protein content of PKC was figure out in Table 2. The
crude protein content of PKC was very significantly
affected (p<0.01) by treatments.
The crude protein content of Aspergillus niger fermented
PKC was not differed from Aspergillus niger+humic
acid fermented PKC, but was higher (p<0.05) than
those of Penicillium sp., Trichoderma harzianum and
Neurospora crassa fermented PKCs as well as
unfermented PKC. The crude protein content of
Aspergillus niger + humic acid fermented PKC was
higher (p<0.05) than those of Trichoderma harzianum
and Neurospora crassa fermented PKCs as well as
unfermented PKC, but was not different from Penicillium
sp. fermented PKC. Penicillium sp. fermented PKC crude
protein content was not differed from Trichoderma
harzianum fermented PKC, but was higher than those of
Table 1: Crude fiber content of palm kernel cake as affected by
treatments
Treatments Crude fiber (%)
A (Control) 18.86a
B (Neurospora crassa)14.75b
C (Penicillium sp.) 13.42b
D (Trichoderma Harzianum)14. 04b
E (Aspergillus niger)14.34b
F (Aspergillus niger + Humic Acid) 13.98b
SEM* 0.68
Means with different superscript are very significantly different
a,b
(p<0,01). *Standard Error of the Mean
Table 2: Crude protein content of palm kernel cake as affected by
treatments
Treatments Crude protein (%)
A (Control) 23.30e
B (Neurospora crassa) 24.49de
C (Penicillium sp.) 26.34bc
D (Trichoderma harzianum) 26.21cd
E (A. niger) 28.41a
F (A. niger + Humic Acid) 28.06ab
SEM* 0.59
Means with different superscripts are significantly different
a,b,c,d,e
(p<0.05). *Standard Error of the Mean
Pak. J. Nutr., 12 (10): 943-948, 2013
945
Neurospora crassa fermented PKCs as well as
unfermented PKC. Trichoderma harzianum fermented
PKC was not differed from Neurospora crassa fermented
PKC, but was higher than that on unfermented PKC. The
crude protein content of Neurospora crassa fermented
PKC was not different from unfermented PKC.
Effect of treatments on ether extract content of palm
kernel cake: The means of the ether extract content of
fermented and unfermented PKC can be seen in
Table 3. The treatments affected the ether extract content
of PKC very significantly (p<0.01).
The ether extract content of unfermented PKC (control)
was very significantly higher (p<0.01) than those of fungi
fermented PKCs. Penicillium sp. fermented PKC ether
extract content was higher (p<0.05) than that of
Trichoderma harzianum fermented PKC and was very
significantly higher (p<0.01) than those of Aspergillus
niger, Neurospora crassa and Aspergillus niger+humic
acid fermented PKCs and unfermented PKC. The ether
extract content of Trichoderma harzianum fermented
PKC was not different (p>0.05) from those Aspergillus
niger and Neurospora crassa fermented PKCs, but was
higher (p<0.05) than that of Aspergillus niger+humic acid
fermented PKC. There was no difference (p>0.05) in the
ether extract content of Aspergillus niger, Neurospora
crassa and Aspergillus niger+humic acid fermented
PKCs.
Effect of treatments on the crude fiber digestibility of
palm kernel cake: The means of the crude fiber
digestibility of fermented and unfermented PKC was
seen in Table 4.
Results of the experiment indicated that treatments very
significantly influenced the crude fiber digestibility of
PKCs. This crude fiber digestibility of Aspergillus niger
and Aspergillus niger+humic acid fermented PKCs was
not differed (p>0.05), but was significantly higher
(p<0.01) than those of Neurospora crasa, Trichoderma
harzianum and Penicillium sp. fermented PKCs and
unfermented PKC. The Neurospora crassa fermented
PKC crude fiber digestibility was higher (p<0.05) than
those of Trichoderma harzianum and Penicillium sp.,
fermented PKCs and was very significantly higher
(p<0.01) than that of unfermented PKC. There was no
difference in crude fiber digestibility between
Trichoderma harzianum and Penicillium sp., fermented
PKCs. However, both of them were differed (p<0.01)
from control.
Effect of treatments on the nitrogen retention of palm
kernel cake: The effect of treatments on the nitrogen
retention of fermented and unfermented PKC was
depicted in Table 5. Treatments influenced the nitrogen
retention of fermented and unfermented PKCs
significantly (p<0.05).
Table 3: Ether Extract Content of Palm Kernel Cake as Affected
by Treatments
Treatments Ether extract (%)
A (Control) 9.18a
B (Neurospora crassa)2.78cd
C (Penicillium sp.)4.39b
D (Trichoderma harzianum)3.35c
E (A. niger)3.00cd
F (A. niger + Humic Acid) 2.34d
SEM* 0.25
Means with different superscripts are significantly different
a,b,c,d
(p<0.05). *Standard Error of the Mean
Table 4: Crude fiber digestibility of palm kernel cake as affected
by treatments Crude fiber
Treatments digestibility (%)
A (Control) 12.02d
B (Neurospora crasa)27.89b
C (Trichoderma harzianum)23.48c
D (Penicillium sp.) 22.40c
E (Aspergillus niger)38.71a
F (Aspergillus niger + Humic Acid) 40.86a
SEM* 4.23
Means with different superscripts are very significantly different
a,b,c,d
(p<0.01). Standard Error of the Mean
Table 5: Nitrogen retention of palm kernel cake as affected by
treatments
Treatments Nitrogen retention (%)
A (Control) 18.67c
B (Neurospora crassa) 28.44c
C (Penicillium sp.) 34.48bc
D (Trichoderma harzianum) 56.40ab
E (A. niger) 42.31abc
F (A. niger + Humic Acid) 63.73a
SEM* 8.26
Means with different superscripts are significantly different
a,b,c
(p<0.05). *Standard Error of the Mean
Table 6: Metabolizable energy of palm kernel cake as affected
by treatments Metabolizable
Treatments Energy (Kcal/Kg)
A (Control) 2252b
B (Neurospora crasa)2368a
C (Trichoderma harzianum)2371a
D (Penicillium sp.) 2404a
E (Aspergillus niger)2411a
F (Aspergillus niger+Humic Acid) 2424a
SEM* 40
Means with different superscripts are significantly different
a,b
(p<0.05). *Standard Error of the Mean
The nitrogen retention of the Aspergillus niger+humic
acid, Trichoderma harzianum and Aspergillus niger
fermented PKCs was significantly higher (p<0.05) than
those of Penicillium sp. and Neurospora crassa
fermented PKCs and control, but it was not different
among them. The Penicillium sp., fermented PKC
nitrogen retention was not different (p<0.05) from
Neurospora crassa fermented PKC and unfermented
Pak. J. Nutr., 12 (10): 943-948, 2013
946
PKC. The nitrogen retention of Neurospora crassaproduce high quality products through increasing the
fermented PKC was also statistically the same as the
unfermented PKC.
Effect of treatments on the metabolizable energy of
palm kernel cake: The means of the metabolizable
energy content of fermented PKC by using different
species of fungi and unfermented PKC are depicted in
Table 6.
Based on the result of analysis of variance, the
fermentation by using different kind of microbes
significantly affected (p<0.05) the metabolizable energy
content of PKC. The metabolizable energy content of
Neurospora crasa, T. harzianum, Penicillium sp.,
Aspergillus niger, Aspergillus niger+asam humat
fermented PKCs was higher (p<0.05) than the
unfermented PKC.
DISCUSSION
Effect of treatments on the crude fiber content of palm
kernel cake: The low in crude fiber of PKC after
fermented with Neurospora crasa, T. harzianum,
Penicillium sp. and Aspergillus niger, was due to the
cellulolytic characteristics of these fungi which posses
high cellulase activity (Mirnawati et al., 2011), so that they
can degrade cellulose into glucose which in turn at the
end of fermentation process the declining in crude fiber
occurs. The result of the reduction of crude fiber was in
accordance with the results of experiments by Sabrina
et al. (2002) and Nuraini and Yunara (2001).
Effect of treatments on crude protein content of palm
kernel cake: When it was compared with the
unfermented PKC (control), there was an increase in
crude protein content of fermented PKCs (treatments B,
C, D, E and F). It was clearly found that there was the
growth of fungi in each fermented PKC. The growing
fungi contribute to the increase in crude protein
content of PKC, so that there was an augmenting in
crude protein of fermented PKC. Crueger and Crueger
(1989) reported that fungi contained high crude protein
(40-60%). According to Carlile and Watkinson (1995),
the increase in crude protein content of substrate after
fermentation was associated with the process of protein
enrichment which was similar to the formation of a
single cell protein and in this process it was not
separated between protein from fungi and substrate.
The height in crude protein content of PKC Aspergillus
niger, Aspergillus niger+humic acid, Penicillium sp. and
Trichoderma harzianum fermented PKCs was also
related to the enzymes (cellulase, protease, etc.)
produced by these fungi as the protein which could
contribute to the height in crude protein content of the
PKC as compared with Neurospora crassa fermented
PKC and control. According to Hidayat (2007)
fermentation is the activity of microbes in food or feed to
nutrient content and nutritional value of the products.
Effect of treatments on ether extract content of palm
kernel cake: There was a reduction of ether extract
content when the PKC was fermented by using fungi.
The dramatic decreased in ether extract content of PKC
occurred at the fermentation by using Aspergillus niger,
Neurospora crassa and Aspergillus niger+humic acid.
According to Falony et al. (2006) fungi was known a
microbe which produce high lipase and Aspergillus
niger was one of fungi that produce high amount of
lipase. Penicillium sp. was also a high lipase producer
(Pimentel et al., 1997; Lima et al., 2003). Ulker et al.
(2010) found that Trichoderma harzianum was also a
fungi which produce lipase. Neurospora crassa was
also well known as a lipase producer (Kundu et al.,
1987). Thus, the lipase produced by each fungi could
hydrolyze lipid content in fermented PKC, so that the
ether extract/lipid content of fermented PKC declined.
Effect of treatments on the crude fiber digestibility of
palm kernel cake: The crude fiber digestibility among
Neorospora crasa, A. niger and A niger+humic acid
fermented PKC was relatively high. This was due to the
height in cellulolytic activity of these species of fungi. The
higher the cellulolytic activity of the fungi, the more
cellulose could be degraded into glucose, so that at the
end of fermentation the amount of crude fiber
decreased. This finding was in accordance with the
results of experiments by Nuraini and Susilawati (2006)
and Mirnawati et al. (2010) who reported that there was
a decline in crude fiber content of PKC fermented by
using Neorospora crassa and Aspergillus niger.
Effect of treatments on the nitrogen retention of palm
kernel cake: The height in nitrogen retention of
Aspergillus niger+humic acid fermented PKC was
related to the height in crude protein of this fermentation
product (28.06%), so that the amount of protein
consumed increased. The high amount of protein
consumed resulted in the high in retained nitrogen in the
body which could be utilized by animals. According to
Farrell (1974) the nitrogen retention was the retained
feed protein in the animal body. The nitrogen retention
was influenced by several factors such as crude protein
content of feed, amino acid content and protein
digestibility. Lloyd et al. (1978) said that nitrogen
retention was one of methods for determining the
protein quality of feed or diet.
Effect of treatments on t he metabolizable energy of
palm kernel cake: The metabolizable energy (ME) of
fermented PKC by using Neurospora crassa,
Trichoderma harzianum, Penicillium sp., Aspergillus
niger and Aspergillus niger + humic acid was higher
Pak. J. Nutr., 12 (10): 943-948, 2013
947
than that of unfermented PKC (control). The increase inDesserheine, S.D.S., 1998. The utilization of Aspergillus
this ME was resulted from the fermentation process
which lead to the degradation of crude fiber into the
simple carbohydrates. These simple carbohydrates are
readily digested and absorbed by animals. Fardiaz
(1989) reported that the biosynthesis of
macromolecules such as protein, lipid, polysaccharide
and nucleic acid was originally produced from variety of
monomer units such as amino acids, fatty acids, simple
carbohydrates, etc.
The result of this experiment was also in accordance
with the result of experiment by Desserheine (1998) who
reported that there was an increase in ME of PKC which
was fermented by using Aspergillus niger from 1844 to
2103 kcal/kg. The increase in the ME content of
Aspergillus niger fermented PKC was due to the
increase in the crude fiber digestibility of this fermented
PKC which produced simple sugars as the source of
energy by animals.
Conclusion: The fermentation of palm kernel cake by
using Aspergilus niger was the best when it was
compared with the fermentation by using Neurospora
crasa, Trichoderma harzianum, Penicillium sp. or
Aspergillus niger+humic acid, or without fermentation
(control).
ACKNOWLEDGEMENTS
This experiment was supported by the MP3EI Funding
Program provided by Directorate General of Higher
Education, Ministry of Education and Culture of the
Republic of Indonesia. I am very grateful to the Dean of
the Faculty of Animal Science, the Head of Research and
Extension Institute and the Rector of the University of
Andalas who have given me a chance to compete with
others in obtaining this funding. My special thanks is
also directed to the Director General of Higher Education
and the Minister of Education and Culture who have
provided this funding.
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