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† Corresponding author 
© 2015 Conscientia Beam. All Rights Reserved. 

EFFECT OF FUNGI AND MANURE ON CADMIUM CONTENT AND 

BIOMASS OF MAIZE GROWN IN CADMIUM CONTAMINATED TAILING 

FROM BANGKA INDONESIA 

 

Nofalia Nurfitriani1† --- Reginawanti Hindersah2 
1Student at Faculty of Agriculture, Universitas Padjadjaran, Bandung, Indonesia 

2Lecturer at Departement of Soil Microbiology, Faculty of Agriculture, Universitas Padjadjaran, Bandung, Indonesia 

 

ABSTRACT 

Cadmium (Cd) contamination form tailings disposal that occur in tin mining in Bangka cause a serious  

soil health problem. One of the ways to reduce Cd concentration in soil is bioremediation. The research was 

conducted to determine the influence of fungi and cattle manure on dry weight and Cd content of  maize  as 

well as  fungi  population in the rhizosphere of maize grown in tailing collected from tin mining area in  

Bangka. Green house research was set up in Factorial Randomized Block Design. Maize hybrid P21 was 

grown  for six weeks in tailing  contaminated by CdCl2.0,5H2O up to 8 mg kg-1 and inoculated with  

Humicola sp. or Fusarium sp. without and with several dose of cattle manure. Interaction effect between 

fungi and cattle manure clearly affect the rhizosphere fungal population, however did not give any 

significant effect to dry weight and Cd content. Application of Fusarium sp. 107 spores mL-1 with manure of 

22 g pot-1 lead to increased fungal population. There was an independent effect of cattle manure to decrease 

Cd content and increase dry weight of maize.  

Keywords: Cadmium, Fungi, Cattle manure, Maize (Zea mays L.) 

 

Contribution/ Originality 

This study contibutes in developing the soil microbiology and soil bioremediation studies in 

Indonesia. This study also as a reference and an information about what kind of fungi and the 

right dose of cattle manure to improve soil quality and productivity in tailing at Bangka Island.  

 

1. INTRODUCTION 

Bangka is the biggest tin mining island in Indonesia. The tin mining activities cause changes 

in the characteristics of the chemical, physical and biological of soil. The decline in soil physical 

properties such as the destruction of soil structure, sensitive to erosion, and low water holding 

ability [1]. In mining site of Bangka, C-organic of both  top soil and bulk soil was less than 1,78% 

Current Research in Agricultural Sciences 
2015 Vol. 2, No. 2, pp. 42-52 
ISSN(e): 2312-6418 
ISSN(p): 2313-3716 
DOI: 10.18488/journal.68/2015.2.2/68.2.42.52 
© 2015 Conscientia Beam. All Rights Reserved. 

 
 
 
 
 
 

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and the texture was sandy. Sandy soils are characterized by a lack of structure, low water 

traction, high water permeability and consequently low indigenius microbial population.  

Pollution by heavy metals such as cadmium (Cd), manganese (Mn), lead (Pb), Zinc (Zn), 

Copper (Cu) and chromium (Cr) due to post mining activities [1] was massive in mining area. In 

Bangka post mining locations, Cd contaminated soil was already exceeds the threshold with a 

concentration range from 0,67 to 12,36 mg kg-1. According to Alloway and Ayres [2], amount of 

Cd in uncontaminated soil is 0-1 mg kg-1 of soil. Heavy metal has a conversely effect to soil, 

agricultural crops and threat food chain. In human being, heavy metal is one the causes of cancer 

incidence [3]. Heavy metal was considered as 10 priority pollutants by the US Environmental 

Protection Agency [4]. Indonesian National Standardization Agency (Standar Nasional 

Indonesia) [5] set a threshold of Cd in food is around 0,1 – 1 mg kg-1.Bioremediation is one of the 

ways to reduce Cd concentration in soil. Microorganisms such as fungi is one of great 

bioremediator. Fungi has bigger potential for bioremediation because of its growth and its wide 

range hyphae in the soil [6]. 

Fungi are good in heavy metal retention through the accumulation of heavy metals such as 

Cd, Cu, Hg, Ti and Zn in both of miselium or spora of fungi. Fungi release its metabolite such as 

sulphide acid or oxalic acid and other extracell materials such as polysaccharide and melanin, 

which could reduce the heavy metal concentration in soil [7] and furthermore limited heavy 

metal uptake by plant roots.According to Environmental Research Institute of Agriculture [1] 

viability of Fusarium sp. and Humicola sp. in the liquid culture with Cd verified that those fungi 

are relatively resistant to Cd and potentially to be used as biological agents of bioremediation of 

heavy metal contaminated soil. Other scientist has been reported that there are some fungi 

survived in polluted soil with heavy metals such as (Humicola grisea, Fusarium sp., Nannizzia sp., 

Curvularia sp. dan Helementrho sporium [8]. 

Organic matter amendment is necessary to enhance bioremediation by using of heterotrophic 

microbes. The growth of fungi would be increased in the presence of  organic matters as an 

energy source. Organic matter could improve soil condition, soil chemical and physical 

characteristics and also affect stability of soil structure [9], and subsequently  would increase the 

availability of oxygen for its proliferation and activity. Long term effect of organic matter 

application are improve microbial population and influence availability of nutritions [10]. 

Alongside that, decomposed organic matters released some organic acids which could bind the 

heavy metals [11] so as the availability of heavy metal will be decreased [12]. Cattle manure 

application may reduce the availability of heavy metals, in addition, it is a right way to maintain 

soil quality and increase fungi population [13]. Organic manure provide C-organic and high 

nutrition to increase microbes activity. Research conducted by Vinhal-Freitas, et al. [14] resulted 

in increases in microbial activity after application of 20 g kg-1 of compost. Application of cattle 

manure up to 30 t ha-1 is able to improve dry weight of maize plant [15]. Application of 20 t ha-

1organic manure and inoculation of arbuscular mychorriza fungi reveal that this combination 



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strongly support the growth of maize plant [16]. Under these conditions, the addition of organic 

material has an important role in increasing crop yields. 

 

2. MATERIALS AND METHODS 

The experiment was conducted in a green house at Faculty of Agriculture Universitas 

Padjadjaran, Bandung - Indonesia on April – Juli 2013. The tin tailing used in this experiment 

obtained from Bangka tin mining field in Indonesia. Composite soil samples (0 to 20 cm depth) 

were collected from the various sites in Air Hitam Village, Bangka Island. Prior to experiments, 

soil were sterilized and analyzed in laboratory. C-organic content of sample was 0,56%, N-total 

0,056% and 19,5 x 103 cfu/g of fungi population. 

 

2.1. Cd Spiking 

Cd pollution was simulated through the application of CdCl2.0,5H2O to achieve a soil 

concentration of 8 mg kg-1. This Cd spiked is aimed to reach the same condition with one in the 

native field (Bangka Island). The Cd-spiked treatments were left for estimated 2 weeks prior to 

transplanting of maize seed.  

 

2.2. Metal-Resistant Fungi 

Cadmium resistant fungi Humicola sp. and Fusarium sp. were isolated from the rhizosphere of 

native plants grown in tailing at Bangka tin mining.  Fusarium sp. was from native Akasia (Acacia 

auriculiformis) and Humicola sp. was from native Harendong (Melastoma). At previous research, the 

resistance of both of species on Cd  was determined.    

 

2.3. Pot Experiment 

The pot experiment was set up in a Factorial Randomized Block Design with two treatment 

factors and three replications using maize (Zea mays L) as a test plant. The  first factor was fungi 

species i.e without and with non pathogenic Humicola sp. or Fusarium sp., and the second one was 

dose of cattle manure i.e without and with 11 or 22 g pot-1.   

Pots were filled with one kilogram of sterilized tailing contaminated with CdCl2.0,5H2O up to 8 

mg kg-1 and incubated for two weeks. Then, different dose of manure were added and incubated 

for a week prior to sowing. After that, seeds of the commercial hybrid maize P21 were sown and  

grown for six weeks. Two days after sowing, 10 mL of fungi species containing 107 spora mL-1 

was pour around seedling. At the end of experiment, Cd content and dry weight of maize as well 

as rhizosphere fungi population were determined. 

 

2.4. Fungi Population Count 

For fungi population analysis, total plate count method (Johnson and Curl, 1972 in [17]) was 

followed using Potato Dextrose Agar (PDA) medium incubated at 300C for one week. Soil 

samples were taken from maize rhizosphere. Colony forming units (CFU) were estimated by 



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© 2015 Conscientia Beam. All Rights Reserved. 

counting the number of colonies. Humicola sp. has black cottony on its surface, while Fusarium sp. 

has red colour on its surface. 

 

2.5. Dry Weight Quatification 

The sample plants for biomass quantification were harvested after 6 weeks. Roots and shoots  

were dried at 700C to constant weight [18] and then weighed separately. 

 

2.6. Heavy Metal Assay  

Cadmium concentrations were determined by using spectrophotometer at 228,8 nm. One mL 

 of HClO4  and 5 mL of HNO3 was added to 2,5 g dried plant samples (0.5 mm) in disgestion tube, 

and leave overnight. The samples were then heated in digestion block 1000C within 1,5 hours, 

then temperature spiked to 1300C within 1 hour, 1500C within 2 hours subsequently. After the 

yellow vapor runs out, digestion temperature increased to 2000C to form a white vapor. After 

cooling, the solution was diluted to 10 mL with deionized water and filtered through a 

Whatmann No.40 filter paper. The filtrates were analyzed for Cd by Atomic Absorption Spectroscopy 

(AAS). 

All preparations and performances for soil analysis presented in this paper were undertaken 

within a standard methods described by Soil Research Institute of Indonesia (Balai Penelitian 

Tanah) [19]. 

 

2.7. Statistical Analysis 

All data were statistically analyzed using the SPSS. Differences between treatments were 

determined by the least significant difference (P<0.05) from the analysis of variance (ANOVA) 

[20]. 

 

3. RESULTS 

3.1. Fungi Population in Rhizosphere of Maize 

Result revealed that there was an interaction between fungi and cattle manure to fungi 

population in rhizosphere of maize was significant. Result of statistical analysis in Table 1 showed 

that application of fungi Fusarium sp. and cattle manure at 22 g generate the highest fungi 

population in rhizosphere, 6,91 x 105 cfu g-1. Application of without fungi treatment and cattle 

manure at 22 g resulted as the lowest fungi population in maize rhizosphere, 0,64 x 105 cfu g-1. 

Before experiment, soil fungi population was 1,95 x 104 cfu g-1. Following inoculation of 

Fusarium sp., total fungi population was increased at any dose of cattle manure. It showed that 

inoculation of 10 ml of Fusarium sp. at the same time of cattle manure at 22 g was the best 

treatment and it could increase fungi population in maize rhizosphere up to 10,7 fold from the 

lowest fungi population (0,64 x 105 cfu g-1) (Table 1). 

 



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Table-1. Effect of Fungi and Dose of Cattle Manure to Fungi Population in Maize Rhizosphere Grown in Cd-

Contaminated Tailing  

Cattle manure  
Fungi Population (105 cfu g-1) 

Without Fungi  Humicola sp.  Fusarium sp. 

0 g 
2,83  b 
A 

2,67  b 
A 

4,66  a 
B 

11 g 
0,98  a 
A 

0,81  a 
A 

5,07  a 
B 

22 g 
0,64  a 
A 

0,70  a 
A 

6,91  b 
B 

         Description: values followed by the same letter are not significantly different according to 5% Duncan's Multiple Range Test. 

 

Cadmium has adversely affects to plant growth and decreases the diversity and biomass of 

microoganisms, however, there are quite a lot of microoganisms that resistant to heavy metals 

and play a role in detoxification mechanisms [21]. In this study, in pot with cattle manure, effect 

of Fusarium sp. to fungi population was better than that of Humicola sp. (Table 1). Fusarium sp. 

was more rapidly growing and its hypae was more spreading fast than Humicola sp. According to 

Sanyal, et al. [22], metals ion are not harmful to the Fusarium oxysporium, even Fusarium 

oxysporium could grow faster with the presence od heavy metals ion. The high population of 

Fusarium sp. was also influenced by root exudates. Fungi population are common in rhizosphere 

due to organic matter and exudate which is a source of additional nutrients for microorganism 

[23]. 

Organic matter affects to the availability of plant nutrients which is in turn could induce the 

presence of microbes [11]. Increased presence and activity of microbes due to its organic manure 

contains carbon which is used as a source of energy [24] thus fungi population is increasing. 

Besides that, with addition of organic manure such as cattle manure leads to higher Cd 

absorption. Cattle manure is able to bind Cd ion [25] and also could help the growth of fungi 

through the supply of nutrition, thus fungi and plant could grow well. 

 

3.2. Plant Dry Weight  

Research revealed that there was no interaction effect between fungi and dose of cattle 

manure on maize dry biomass. However, there was an independent effect of cattle manure on 

maize dry biomass. Table 2 describes that application of cattle manure at 22 g could afford 

highest maize dry biomass up to 1,116 g. 

Plant dry weight (root and shoot) indicate efficient level of plant metabolism [26]. Plant dry 

weight is consider as plant growth indicator, due to it is an accumulation net result during the 

plant life [27]. Maize plant treated with Cd contamination causes a decrease on plant dry weight 

and yield, as well as reducing nitrogen content in the plant tissues also lowering protein content 

in its seed [28]. The lowest maize dry weight belongs to maize plant without cattle manure, 

0,348. It caused by the lack of nutrient supply and the availability of Cd lead to stunted growth. 

 



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Table-2. Effect of Cattle manure to Plant Dry Weight of Maize Grown in Cd-

contaminated Tailing 

Treatments Plant Dry Weight (g) 

Fungi 
    Without Fungi 
    Humicola sp. 
    Fusarium sp. 

0,643  a      
0,794  a 
0,745  a 

Cattle manure 
    Without manure  
    Cattle manure (11 g) 
    Cattle manure (22 g) 

0,348  a 
0,717  b  
1,116  c 

Description : values followed by the same letter are not significantly different according 

to 5% Duncan's Multiple Range Test. 

 

Application of cattle manure at 22 g in maize was able to provide sufficient nutrients in order 

to be able to photosynthesis properly thus the plant metabolism running out well. In addition, 

this treatment could improve plant dry weight up to 3,2 fold than without cattle manure 

treatment.  

 

3.3. Cd Conctent in Maize 

According to statistics analysis, there was no interaction effect between fungi and cattle 

manure, however, there was an independent effect of manure on lowering Cd content in maize 

biomass (Table 3). Cadmium content in plant decreased along with manure application at 11 g 

and 22 g. The application of organic matter caused heavy metal bound strongly to organic 

compound, thus heavy metal such as Cd was unavailable to the plant. The highest Cd content in 

plant (16,837 mg kg-1) belongs to plant without manure treatment, this happened because of there 

was no compound which could bind heavy metal, and plant could not survive any longer in the 

condition with Cd. The more Cd uptake by plant, the more Cd content in plant, generally. 

 

Table-3. Change in Cd Content in Maize Following Fungi Inoculation and Cattle Manure 

Treatments Plant Cd Content (mg kg-1) Cd Uptake (mg/g) 

Fungi  
    Without Fungi 
    Humicola sp.  
    Fusarium sp. 

 
11,014   a 
  9,140   a 
  8,087   a 

 
7,082 
7,257 
6,025 

Cattle manure  
    Without manure 
    Cattle manure (11 g) 
    Cattle manure (22 g) 

 
16,837   b 
  6,352   a 
  5,052   a 

 
5,859 
4,554 
5,638 

  Description : values followed by the same letter are not significantly different according to 5% Duncan's Multiple Range Test. 

 

Chelation processes between metal and organic acid usually occurs while the increase of 

organic acids causing ligand exchange between organic anions (such as humic acid and fulvic acid 

to the free –OH). Increased levels of organic matter followed by increased cation exchange 

capacity (CEC) and clay fraction. Soil containing organic matter generally contains clay coloid 



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which be able to bind cations in soil [27]. Humic acid takes a role in stimulates root and plant 

shoot growth, furthermore humic acid has high CEC which is could bind toxic heavy metal.  

Humic acid released by organic manure leads to Cd cheating by its humic, thus Cd 

availability in soil will be decreased [12]. In this study, plants treated with manure typically have 

higher plant height due to nutrient intake from organic matter and Cd binding by organic acids 

released by decomposed organic matter. Statictic analysis described that there was no significant 

effect of fungi inoculation. Regardless on statistical analysis, Cd content of whole maize biomass 

decreased by fungal inoculation (Table 3) although it was not significant. However, Humicola sp. 

and Fusarium sp. were potentially reduce Cd uptake by plant through organic acids released by 

those fungi, one of organic acids was oxalic acid [29]. Oxalic acid could reduce Cd toxicity in 

plant and could improve root length, alongside that, oxalic acid could hinder Cd uptake by plant 

root [30]. Cadmium immobilization by fungi as well as manure also influenced Cd uptake by 

roots. Our research verified that phenomenon clearly. This evidence demonstrated that Cd 

resistant fungi might be used as bioremediation bioagents; and that eficacy of bioremediation 

could improve by manure addition.  

 

3.4. Symtomps of Cd Toxicity in Plant 

Impaired growth of maize in this study due to the poor condition of soil physical 

characteristics, the presence of heavy metals and limited space to grow and soil nutrients. In this 

study, maize faced obstacles in its growth this could happened due to the plants were suffered by 

heavy metals Cd poisoning. Maize could accumulate Cd [31], however with the presence of Cd 

even in low concentrations could decrease root growth. 

Cadmium has adversely effect to photosynthesis process due to Cd could interfere chlorophyll 

synthesis [32] and photosynthetic electron transport by inhibit the located in photosystem II 

[33]. Presence of Cd hinder growth of lateral roots while main root turn to brown, stiff and 

circular [34]. Heavy metals are toxic to maize, plant shoot had stunted growth [28]. Nitrogen 

content in shoot and root would be decreased in plant which is exposed by metals. Cadmium 

could cause wilted, yellowing leaves and blackened roots. In this study, maize plant also had the 

same symptoms which seem to wilt and yellowing leaves (Picture 1) and stunted growth (Picture 

2). 



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      Picture-1. Symptoms of Cd toxicity, the leave were yellowing and wilting. 
 

 

 

 

 

 

 

 

 

 

 

 

 

 

Picture-2. Picture showed different plant height of treatments of aobo (left), aob1 (centre) and aob2 (right). Treatment of 

aobo has stunted growth due to Cd existence. 

 

4. CONCLUSION 

There was an interaction between fungi isolate with cattle manure to fungi population in the 

rhizosphere of maize. However there was no interaction between fungi and cattle manure to plant 

dry weight and Cd concentration of maize plant. There was an independent effect of cattle manure 

to plant dry weight and Cd concentration of maize plant. 

Combination of the best treatment was inoculation of Fusarium sp. with addition of cattle 

manure at 22 g pot-1 to fungi population in the rhizosphere of maize plant. Application of heavy 

metals resistant indigenus fungi and cattle manure were quite able affected decreasing Cd 



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concentration in plant and also capable to increase plant dry weight and total fungi population 

which then affect to maize plant growth. 

 

5. ACKNOWLEDGEMENTS 

We would like to thank Head of Graduate School of Agriculture; Dr. Betty Natalie Fitriatin, 

Faculty of Agiculture and Universitas Padjadjaran - Indonesia for supporting this research paper. 

 

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