BIOTROPIA Vol. 28 No. 3,2021: 214 - 220 DOI: 10.1 1598/btb.2021.28.3.1333 

EFFECTIVENESS OF INDIGENOUS ENDOMYCORRHIZAL 
BIOFERTILIZER PROTOTYPE O N  ORGANIC 

SALAK LEAVES A N D  FRUITS I N  BALI 

I NYOMAN RAI I*, I I(ETUT SUADA', I WAYAN WIRAATMAJAl AND 
NI ICOMANG ALIT ASTIARI2 

'Stuaj Program ofAgroecotechnology, Faculty afAgriculture, Uniuersitas Udgana, Kampzls Unud Bukit Jimbaran, Kuta Selatan, 
Badung 80361, Bali, Indonesia 

* S t u h  Program OfAgrotechnology, Faculty OfAgriculture, Uniuersitas Warmadewa, Denpasar 80235, Bali, Indonesia 

Received 14 February 2020 /Accepted 1 July 2020 

ABSTRACT 

Organically cultivated salak (Salacca xalacca) o n  dry land has limited production in Bali. Typically, fertilization 
is carried out using leaf litter or other organic fertilizers because soil fertility is low for salak plantations. The 
present study analyzed the effectiveness of an indigenous endomycorrhizal biofertilizer o n  the nutrient and total 
carbohydrate content of salak leaves and fruits. The study used a randomized block design with nine replicates. 
The treatment consisted of three levels, i.e., 1. fertilization with leaf litter only, as is practiced by the farmers and 
as control (C); 2. fertilization with indigenous endomycorrhizae biofertilizer prototype (P); and 3. combined 
fertilization with leaf litter and indigenous endomycorrhizae biofertilizer prototype (PM). Spores of indigenous 
endomycorrhizae from salak plantations were used for making a biofertilizer prototype. The results showed that 
P and CP treatments provided beneficial results such as: 1. significantly increased the chlorophyll, relative water 
content of leaves, as well as the number and weight of fruits per tree; 2. improved fruit quality by increasing 
sweetness and weight per fruit; and 3. had a positive effect o n  water uptake and nutrient absorption as indicated 
by high N and P of leaf tissue and high carbohydrate content of leaves. 

Keywords: biofertilizer, endomycorrhizae, organic, prototype, Salacca xalacca 

INTRODUCTION 

Bali Province is a major tourist destination in 
Indonesia. Increasing the number of domestic 
and international tourists leads to an increased 
demand for fruits, including organic salak fruits. 
Salak cultivation in Bali has been carried out 
organically since the 1500s and is hugely 
beneficial to the farmers; however, the quantity, 
quality, and continuity of organic salak fruit 
produced is low (Rai e t  al. 2014). 

This low productivity can be attributed to the 
nature-dependency of the farmers, who have not 
yet implemented adequate agricultural practices. 
Typically, fertilization only uses leaf litter, while 
irrigation relies only on rainfall. Thus, the 
ferulization of organic salak renders low soil 
fertility thereby decreasing the plant productivity 

*Corresponding author, email: rainyoman@unud.ac.id 

over time (Rai e t  al. 201 4). Rai e t  aL (201 0) found 
that the nutrient content of N, P, and I< in the 
leaf tissue of organic salak in Bali was low; also, 
the soil fertility was low as indicated by the 
levels of C-organic and the content of N, P, and 
K in the soils. In order to maintain the soil 
fertility and environmental sustainability for high 
organic salak productivity, the cultivation should 
be carried out with indgenous endomycorrhizae 
biofertilizer based on the fact that the diversity 
of indigenous endomycorrhizae fungal species in 
nature is very large paslam e t  al. 201 1; Proborini 
2013; Suamba e t  aL 2014; Sarah & Ibrar 2016; 
INVAM 20 1 7). 

IGm e t  al. (2017) established a close 
correlation between soil, plants, and 
endomycorrhizae. Indigenous endomycorrhizae 
isolated from plants in certain locations, will be 
more effective if applied directly to the target 
plant concerned where it is taken as compared 



Effectiveness of indigenous endomycorrhizal biofertilizer prototype o n  organic Salak leaves - Rai e t  all 

to the endomycorrhizae brought from outside 
(non-indigenous endomycorrhizae) . The 
arbuscular mycorrhzal symbiosis between plants 
and fungi exerts a positive impact on improving 
the soil structure, expanding the water 
absorption areas, increasing the plant tolerance 
to biotic and abiotic stresses, increasing the 
nutrient uptake, and increasing the plant growth 
and yield (Nikhat 2014; Olagunju et al. 2014; 
Soka & Ritchie 2016). In addition, 
endomychorrizae increases plant tolerance to 
various biotic and abiotic stresses, including 
alkalinity and metal toxicity (Abbasi et al. 2015; 
Bitterlich et al. 2018). The endomycorrhizae 
fungus whch is also called arbuscular 
mycorrhizae is beneficial to the host plants as it 
plays a role in increasing nutrient absorption 
through the endomycorrhizal structures that 
form large root surface areas so that the plant 
roots can absorb the nutrients (Baslam et al. 
2011; Sasvari 2012; Brundrett & Tedersoo 
2018). Endomycorrhizae plays a role in 
increasing plant resistance to root pathogen 
attack through antibiotics produced during 
symbiosis with plant roots that weaken and also 
kill the pathogenic bacteria, viruses, and fungi 
(Brundrett 2017; Sasvari, 2012). 

Furthermore, the diversity and activity of 
indigenous endomycorrhizae in plant roots are 
mainly determined by the type of the host plant 
(Ningsih et al. 2013; Sadhana 2014), 
environmental growth factors, such as climate 
and soil moisture/drought (Hernadi 2012; 
Quiroga et al. 2017; Mathimaran et al. 2017; 
I<ehri et al. 2018), and the level of soil fertility 
(Tahat & Sijam 2012; Kavitha & Nelson 2013; 
Mo et al. 2016). Rai et al. (2019a) explored 
and identified morphologically and genetically 
the indigenous endomycorrhizae from salak root 
areas in three regencies in Bali: Icarangasem, 
Gianyar, and Tabanan. In our study, two genera 
of indigenous endomycorrhizae in salak 
were identified i.e., Glomzls and Entrophospora. 
The genus Glomzls consisted of three species 
(Glomzls cabens, Glomzls czlstos, and Glomzls indicum) , 
while genus Entrophospora consisted of only 
one species (Entropbospora-sp-SH 197095.06FU). 
After propagation, the spores of these species 
were formulated into prototypes of biological 
ferulizers/bioferulizer with carrier medla zeolite, 
quartz sand, sea sand, and volcanic sand. The 
most effective method to be applied in salak 

seedling is a prototype composed of a mixture 
of 100 spores from Glomzls species in 500 g 
volcanic sand carrier media. This phenomenon 
was shown by the optimal growth of salak 
seedling and the maximum (100%) colonization 
of endomycorrhizae at the roots (Rai et al, 
2019b). Positive test results on salak seedling 
growth need to be followed up by evaluating the 
efficiency of the prototype of indigenous 
endomycorrhizae biofertilizer on organic salak 
plantations in the field. Thus, the present study 
aimed to determine the effect of prototype 
indigenous endomycorrhizae biofertilizers on 
organic salak production and its effect on the 
nutrient and carbohydrate content of the leaves. 

MATERIAJ3 AND METHODS 

The study was conducted from February to 
December 2019 in organic salak farms owned by 
farmers in Sibetan Village, Bebandem District, 
Icarangasem Regency. The study used 15-year- 
old salak trees and a randomized block design 
with nine replicates. Three levels of fertilization 
were applied as follows: 1. fertilized with leaf 
litter only, as is practiced by the farmers and as 
control (C); 2. fertilized with prototype 
indigenous endomycorrhizae biofertilizer 0; 
and 3. combination of leaf litter and prototype 
indigenous endomycorrhizae bioferthzer (CP) . 
Therefore, 27 salak trees with a total plot size of 
216 m square were needed. 

The spores of indigenous endomycorrhizae 
were taken from salak roots in Sibetan Village. 
The isolation of the spores was carried out using 
the wet filtering technique, followed by 
centrifugation as described by Brundrett (2017). 
These spores were propagated according to the 
method described by Rai et al. (201 8), using corn 
as a host plant with water stress treatments. 
Topping or shoot cutting was carried out at the 
age of 4 weeks. Watering to field capacity was 
carried out from the beginning of seed planting 
to 1 week of age, followed by watering to 50% 
of field capacity until 4 weeks of age. After 
topping at the end of the 4th week, watering was 
stopped so that the plant experienced stress. 
Then, the plant was dismantled to harvest the 
spores from the multiplication at the end of the 
5th week. Subsequently, the resulting spores were 
placed on volcanic sand: 100 spores/500 g sand. 



BIOTROPIA Vol. 28 No. 3,2021 

Fertilization was conducted by making a hole, 
30 cm wide and 20 cm deep, around the tree at a 
distance of 40 cm from the base of the tree. The 
salak trees in treatment C were fertilized with 4 
kg leaf litter of salak/tree. The leaves were cut 
into 20-cm-long pieces, placed in a hole, and 
covered with soil. O n  the other hand, the trees 
in the P treatment were fertilized with prototype 
indigenous endomycorrhizae made from a 
mixture of 100 spores of three Glomas species 
(Glomas cabense, Glomtls Czlstos, and Glomas 
indicum) in 500 g volcanic sand carrier media per 
plant. The prototype of the biofertilizer was 
evenly spread around the tree and covered with 
soil. Interestingly, the CP treatment was carried 
out by spreading a prototype of the biofertilizer 
made from a mixture of 100 spores of three 
Glomzts species in 500 g of volcanic sand carrier 
media per plant, followed by spreading the salak 
leaf litter on it evenly around the tree. 

The chlorophyll content and the relative 
water content (RWC) of the leaves, the 
percentage of fruit set, the number and weight 
of fruits per tree, weight per fruit, fruit diameter, 
fruit sweetness level, N and P content of the 
leaves, and total sugar, reducing sugar (R-sugar) 
and sucrose content of the leaves, and root 
colonization by indigenous endomycorrhizae 
were recorded. The colonization of roots by 
indigenous endomycorrhizae was observed by 
the slide method of Giovannetti and Mosse 
(1980) using the following formula: percentage 
of colonized roots = the number of colonized 
roots/the total number of roots observed x 
100%. The percentage of fruit set was calculated 
as follows: the number of flowers developed 
into fruits/the number of flowers x 100%. The 
leaf chlorophyll content measured three times by 
Chlorophyll Meter SPAD-502 in April, June, 
and August, and the average was calculated. The 
total sugar was analyzed by anthrone method, R- 
sugar by Nelson-Somogyi method, and the 
sucrose content was calculated by subtracting 
the value of total sugar content from that of R- 
sugar, and multiplied by 0.95. The RWC was 
measured from matured leaves. After being cut 
from the tree, the mature leaves were then 
immediately wrapped in aluminium foil, stored 
in an icebox, and transported to the laboratory 
for further analysis. Thirty pieces of leaf samples 
(10 pieces from the tip of the leaf, 10 pieces 
from the middle, and 10 pieces from the 
bottom), with a diameter of 1 cm, were taken 
from leaf sheaths using a round punch and 

weighed ( W I ) .  These leaf samples were 
immersed in water and irradiated with 40 W 
fluorescent light at room temperature for 5 h. 
Then, each piece of leaf sample was carefully 
dried with paper towel, and weighed (Wz), 
followed by oven-drying at 70 OC for 24 h 
before being estimated ( W 3 ) .  The value of RWC 
was calculated by the formula: p ~ - W z ) /  
(W3-Wz) x 100%. The nutrient content of N 
and P leaves was analyzed by Kjeldahl method 
and the P-availability was analyzed by Olsen 
method. The number and weight of fruits per 
tree were calculated cumulatively at the end of 
the study. Moreover, the weight of each fruit 
was calculated as follows: total weight of fruit 
per tree/the number of fruits per tree. 

These data were analyzed using analysis of 
variance with SPSS (Statistical Product and 
Service Solution) software version 26. If the F 
test showed a significant difference, the least 
significant difference (LSD) test was performed 
to differentiate the average value among 
tretaments. 

RESULTS A N D  DISCUSSION 

The results of the analysis of variance 
(ANOVA) showed that the fertihzation 
treatment significantly affected all the observed 
variables. The weight and number of fruits per 
tree (790.80 g and 16.81 fruits, respectively) in 
the treatment of indigenous endomycorrhizae 
biofertilizer prototype (100 spores/500 g 
volcanic sand carrier me&a) were sipficantly 
hgher than those fertilized with leaf 
litter/control (653.81 g and 14.94 fruits, 
respectively), but were not significantly different 
from CP (790.14 g and 16.56 fruits, respectively) 
(Table 1). The quality of salak fruit in the P and 
CP treatments was significantly improved as 
compared to that in treatment C, as shown by 
the increased sweetness of the fruit (Table 2) 
and the weight per fruit (Table 1). The high 
number and weight of fruit per tree, as well as 
the increased fruit quality due to the 
administration of indigenous endomycorrhizae 
biofertilizer prototype, elevated the N and P 
content of the leaves as compared to the control 
(Table 2); also, the chlorophyll content and 
RWC of the leaves were increased (Table 1). 
Visually, the trees treated with C and CP 
treatments had dark green and fresh leaves as 
compared to the control. 



Effectiveness of indigenous endomycorrhizal biofertilizer prototype on organic Salak leaves - Rai e t  al: 

Table 1 Effect of prototype indigenous endomycorrhizae biofertilizers on the leaf chlorophyll content, RWC of leaves, 
number and weight of fmits per tree, weight per fruit, and fruit sweetness in salak plants 

Leaves chlorophyll Leaves relative Number of Weight of Weight per Fruit 
Treatments content water content fruit per tree fruit per tree fruit sweetness 

(SPAD) ("0) (unit) 0 0 (% Brix) 

LSD 5% 0.67 0.98 1.59 96.34 7.27 0.51 

Note: Numbers followed by the same letter in the same column did not differ significantly in the LSD 5% level. 

Higher production and yield quality in P and 
CP treatments as compared to control (C) were 
related to h g h  leaf chlorophyll content (Table 1) 
and the ability of salak tree to absorb nutrients 
and water (Table 2). The high P and N content 
in the leaves resulted from the P and CP 
treatments was significantly associated with root 
colonization as compared to the C treatment. 
Table 2 displayed that root colonization by 
indigenous endomycorrhizae in the P and CP 
treatments was 100%, but only 23.14% in 
treatment C. The high root colonization in P 
and CP revealed a mutualism symbiosis between 
indigenous endomycorrhizae and salak trees, 
which in turn, increased the P and N content 
and the RWC in the leaves. The 
endomycorrhizae infects the roots of plants but 
does not cause injury, whch in turn causing 
mutual reciprocal processes. Host plants obtain 
nutrients from endomycorrhizae, while 
endomycorrhizae obtain carbohydrates or food 
from host plants (Hernadi e t  al. 2012; Zasvari e t  
al. 2012). 

H ~ g h  nutrient content and RWC in the leaves 
resulted from the P and CP treatments increased 
the chlorophyll content, which improved the 
photosynthesis as indicated by elevated total 
sugar, R-sugar, and sucrose content in the leaves 
resulted from the P and CP treatments as 
compared to that in C (Table 2). The present 
study showed that indigenous endomycorrhizae 
fungus isolated from root of salak trees is 
suitable to be used as a biofertihzer. The 
administration of indigenous endomycorrhizae 
resulted in the absorption of nutrients and water 
through the endomycorrhizae structure that 
enlarges the surface area of salak root, so that 
the plant roots can absorb the nutrients and 
water (Baslam e t  al. 201 1; Zasvari 2012; 

Brundrett & Tedersoo 2018, Bitterlich e t  al. 
201 8). 

Spore density and root colonization of host 
plants are largely determined by the 
compatibility of endomycorrhizae with 
host plants, environmental factors, and 
interactions between endomycorrhizae and 
chemical compounds produced by host plants 
(Beltrano e t  al. 2013; Sarah & Ibrar 2016). 
Thus, a correlation between indigenous 
endomycorrhizae biofertilizers prototype and 
salak trees can be suspected, which increases the 
yield, the quality of the yield, and the 
physiological processes of salak trees. The 
results of this efficiency test are in accordance 
with those of previous studies wherein 
endomycorrhizal fungi biofertilizer can increase 
the growth, production and quality of pineapple 
yield (Nurhandayani e t  al. 2013), chill (Tanwar e t  
al. 2013), teak (Proborini, 2013), tea (Nepaleon 
e t  al. 2012) and apple (Fediala e t  al. 2018). 
Endomycorrhizae plays a role in increasing plant 
resistance to drought or lack of water in the dry 
season because the root of the plants possess 
mycelium that can reach water in the wider 
rhizosphere area of the soil and adsorb water 
despite h t e d  availabihty (Sasvari 2012). 
Furthermore, it is involved in producing various 
growth regulators such as auxins, cytokmins, and 
gibberellins and vitamins that can increase the 
growth of plant organs and roots that do not 
rapidly age and hence can function effectively in 
the absorption of nutrients and other solutes 
(Baslam e t  al. 201 1; Tanwar e t  aL 2013). The 
endomycorrhizae also improve the soil structure 
because the mycelium on the outside of the 
roots of plants (covering soil grains) produces 
polysaccharide gels that increase the stability of 
soil aggregates (IO-uger 2011; Sasvari 2012; 
Sadhana 201 4; Jansa e t  al. 201 6; I<lm e t  al. 201 7). 



BIOTROPIA Vol. 28 No. 3,2021 

Table 2 Effect of prototype indigenous endomycorrhizae biofertilizer application on the N and P nutrient, total sugar, 
R-sugar, and sucrose content of the leaves and root colonization on salak plants 

Total sugar R-sugar 
N content P content of of Sucrose content Root content of 

Treatments of leaves leaves of leaves colonization leaves 
("4 ("/o) 

leaves 

("10) ("10) 
("10) 

LSD 5% 0.03 0.01 0.51 0.22 0.79 3.16 

Note: Numbers followed by the same letter in the same column did not differ significantly in the LSD 5% level. 

Although C was not given indigenous 
endomycorrhizae bioferulizer, root colonization 
occurred albeit with significantly lower intention 
as compared to that in P and CP treatments. 
The data showed that indigenous 
endomycorrhizae were naturally present in salak 
root area; however, for a positive influence on 
the production and quality of salak, the 
population needed to be increased by giving 
indgenous endomycorrhizae biofertihzer for the 
optimal production of the plants. The 
indigenous endomycorrhizal fungi, also known 
as arbuscular mycorrhizal fungi, in nature is 
diversified (Baslam e t  al. 2011; Proborini 2013; 
Suamba e t  al. 2014), with a positive effect on the 
salak trees (Juliadewi e t  a/. 2014). Indigenous 
endomycorrhizae is naturally associated with 
plant roots without human intervention and has 
a high potential for extensive colonization 
because it recognizes the host plant and has a 
higher tolerance to environmental conditions, 
such as high stress (Sadhana 2014; Quiroga e t  al. 
2017). Based on these characteristics, it can be 
speculated that indigenous endomycorrhizae 
isolated from salak roots has great potential to 
be developed as biofertilizer because it adapts to 
host plants to be fertilized (Sasvari 2012; 
Sadhana 2014; Hohmann & Messmer 2017). 

CONCLUSIONS 

ACKNOWLEDGEMENTS 

Our gratitude goes to Universitas Udayana 
for financial support through Udayana 
Invention Grants in 2019. The authors also 
thank the Directorate General of Higher 
Education, Ministry of Research, Technology 
and Higher Education for financial support 
through the Higher Education Applied Grants 
2018. 

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