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Menara Perkebunan 2009, 77 (1), 58-67. Review

Introduction of microbial inoculants to improve fungsional

relationship between above- and below-ground bio-diversity

Didiek Hadjar GOENADI & Laksmita Prima SANTIIndonesian

Biotechnology Research Institute for Estate Crops, Bogor 16151

Ringkasan

Sebagaimana telah diketahui bahwa

keragaman di muka bumi memainkan peran yang sangat penting dalam menciptakan

lingkungan yang berkelanjutan. Bagaimana-

pun juga, aktivitas manusia sampai tingkat

tertentu mengurangi kompleksitas agro-

ekosistem. Beberapa di antaranya adalah

perubahan proses bio-fisik-kimia yang

mengakibatkan tidak dapat menopang

produktivitas. Untuk mengatasi masalah ini,

banyak upaya telah dipusatkan pada

peningkatan aktivitas mikrob di dalam tanah

dengan menggunakan teknologi yang disebut

bio-fertilizer (pupuk hayati), pengomposan

residu tanaman secara modern, dan membatasi

penggunaan pestisida sintetik. Teknologi

tersebut diyakini dapat meningkat-kan

keragaman hubungan antara bagian per-mukaan dan bawah tanah yang akhirnya

berkontribusi terhadap perubahan dan

membawa fungsi penting secara biologi.

Makalah ini memaparkan hubungan

keragaman yang menguntungkan secara

fungsional antara keaneka-ragaman

permukaan dan bawah tanah untuk

pengelolaan dan pengembangan pertanian

atau perkebunan secara berkelanjutan.

Summary

It has been very well understood that bio-

diversity on the earth plays a very important

role on governing the sustainability of theenvironment. However, anthropogenicactivities have to some extent reduced

drastically the complexity of the agro-

ecosystem. Many of these bio-physic-chemical

processes will be changed and as a result they

can not sustain productivity. To overcome this

problem, a great effort was focused atimproving microbial activities in the soil by

using the so-called bio-fertilizer technology,

new-modern composting plant residues, andlimited use of synthetic pesticides. It is

believed that enhanced relationship between

above-and below-ground biodiversity

contributes to the re-establishment and able tocarry out essential biological functions. This

paper discusses functional relationship between

above- and below-ground bio-diversity

beneficial for sustainable management and

plant development.

[Keywords: Biodiversity, plant development, microbial inoculants, biofertilizer,

sustainable management, legumecover-crop ].

Introduction

Global food supply depends on

intensive agriculture. In Indonesia, largenumbers of farmers have limited access to

inputs but are nonetheless forced by

circumstances to drastically reduce the

complexity of their agro ecosystems in an

attempt to intensify production. Asintensification proceeds, above-ground

biodiversity is reduced, one consequenceof which is that the biological regulationof soil processes is altered and often

substituted by the use of mechanical



59

Goenadi & Santi

tillage, chemical fertilizers and pesticides.

This is assumed to reduce below-grounddiversity. On the other hand, crop

productivity is closely related to the ability

of plant roots to extract water and

nutrients efficiently out of the soils. Thefunction of the roots is governed by an

integrated set of biological processes. In

addition to plants, soil is the habitat of adiverse array of organisms, which their

activities are contribute to the maintenance

and productivity of agro ecosystem by

their influence on soil fertility. In this

case, there are functional relationships between above and below-ground in agro

ecosystem. Swift & Bignell (2001)

suggested that maintenance of diversity ofcrops, other plants, and below-ground in

cropping systems is widely accepted as a

management practice which buffer

farmers against short-term risks.Enhanced relationship between above

and below-ground biodiversity contributes

to the re-establishment and able to carryout essential biological functions. To be

more precise, the enhancement of soil

biodiversity by the retention of crop

residues and other organic matter, inducedmicrobe inoculants, and limitations in the

use of pesticides will also have associated

labor costs which are part of theassessment on efficiency economic value

of management farming. Soil micro-

organism especially bacteria and fungi

contribute a wide range of essential

service to the sustainable function of allecosystem, such as regulating nutrient

cycles and the dynamics of soil organic

matter, soil carbon sequestration, green-house gas emission, bioremediation of

toxics and pollutants, and enhancing the

amount and efficiency of soil nutrient forcrops. In the tropical region, the diversity

of the soil microorganism (bacteria and

fungi) commonly even greater than that of

other soil organism. Directly target the joint conservation of both above (crops)

and bellow-ground (soil microbial)

components of biological diversity willhave environmental benefits at ecosystem

and agricultural production.

This paper is, therefore, aimed to

present basic information regarding tomicrobial inoculants to improve functional

relationship between above and below-

ground bio-diversity for sustainablemanagement and plantation development.

Potential use of bio-fertilizer to improve

functional relationship above- and

below-ground bio-diversity

The influence of plants on microbial population structure and function in the

rhizosphere has important ecological

implications for soil function, including

biogeochemical cycles. Similarly, soil

microbes have a tremendous influence on plant health and productivity (Bloemberg

& Lugtenberg, 2001). For example, large

areas of marginal soils in Indonesia have

been developed for plantation. These soilshave been characterized by low organic

matter content, predominant low activity

clays, and strongly acid in reaction. Thesein effect will depress the microbial

activities which in turn disturb the nutrient

cycle in the soils. On the other hand,under humid-tropic conditions, fertilizer

loss through leaching, volatilization,

and/or fixation represents an economic

loss as well as a potential environmental

contamination. A biotechnologicalapproach is then assumed to be able to

enhance the emergence of biotechnology

in soil management provides a newapproach in tackling efficiently many

problems which remain unsolved by



60

Introduction of microbial inoculants to improve fungsional……..

current conventional technology. Mani-

pulation of soil microbes offers an

efficient technique to stabilize soilaggregates, increase nutrient uptake,

control soil-borne pathogen, and

accelerate the decomposition of solidorganic wastes, without adding new

pollutants to the environment. Bio-

fertilizers are basically microorganismswhich can improve the availability of

nutrient to plants. They have been

believed to be an important component ofsustainable agriculture, as they can reduce

significantly the use of chemicalfertilizers. It is hypothesized that by

improving rhizospheric microbial acti-

vities via bio-fertilizer application,nutrient solubilization can be enhanced

and consequently less conventional

fertilizers will be needed (Goenadi et al.,

2005). An efficient bio-fertilizer producti.e. EMAS (Enhancing Microbial Activity

in the Soils) has been successfully

development by using active ingredientsconsisting of Azospirillum lipoferum,

Azotobacter beijerinckii, Aeromonas

punctata, and Aspergillus niger native oftropical soils (Goenadi et al., 2000). The

application of 6.25 g EMAS per plant

(equivalent with 83.125 kg/ha) + 50%

inorganic fertilizer recommended dosagefor tea, could reduce application of

inorganic fertilizer dosage until 50% and

resulted in the growth of the plant whichwas better than that of inorganic fertilizer

(Wachjar et al., 2006). In addition,

evaluate the effectiveness of EMAS bio-

fertilizer in reducing dosage of conven-tional fertilizers used in corn at Pelaihari,

South Kalimantan indicated that based on

the current production value and total of

cost production, reducing 25, 50 and 75%conventional fertilizer provides the

planters with 1.44, 1.13, and 1.12 revenue

cost ratio. Yield of dry grain of corn was

higher (+41.8%) by application of 75%

standard dosage and 1 gram EMAS biofertilizer/tree (53.3 kg/ha) than by

standard dosage of conventional fertilizer

(Santi et al., 2007).One straightforward and visible

benefit for the plant is a better supply of

and access to nutrients. The role ofmutualistic nitrogen-fixating rhizobia has

been well documented for decades, but

recent data detail the intimate exchange ofnutrients during the symbiosis of plant

roots and bacteria (Lodwig et al., 2003).

The plant attracts nitrogen-fixating

bacteria to invade the cells in the root and

provides them with carbohydrates as afood source while the bacteria reduce

nitrous compounds in the soil that are then

used by the plant. These microbes useroot exudates as a source of energy and

cellular carbon. Endophytic associations

in rice have a N-fixing potential of 150 kg

N/ha/year, but are at times unreliable(Shenoy et al., 2001). Similarly, inter-

actions between plants and fungi can also

provide nutrients for the plant. Arbuscularmycorrhizal fungi, which form an intricate

internal symbiosis with the roots of most

flowering plants, are associated with the

provision of phosphorous to the plant inexchange for organic carbohydrates

(Smith & Read, 1997).

Microbes also indirectly aid nutrientuptake bacteria of the Azospirillum genus

promote increased root mass and more

efficient nitrogen uptake from the soil in

response to the plant hormone indole-3-acetic acid. Using these bacteria and fungi

could provide significant environmental

benefits as they would allow a reduction in

the application of nitrogen and phosphorous fertilizers. The overuse of such

fertilizers has become a major concern



61

Goenadi & Santi

because they cause nitrate contamination

of soil and groundwater by leachates and because microbial denitrification converts

residual nitrogen into the greenhouse gas

nitrous oxide (Nosengo, 2003; Reay,

2004). Equally, excess phosphorouscompounds leach into groundwater, rivers

and streams, where they promote algal

growth and other environmental problems.Microbial seed inoculants are able to

enhance biological nitrogen fixation. The

inoculants are claimed to be cost effective,

eco-friendly, renewable and generally

capable of supplementing chemical ferti-lizers in sustainable agricultural system.

Amongst nitrogen fixing bacteria such as

Rhizobium (symbiotic), Azotobacter and Azospirillum (non-symbiotic), the most

widely used inoculant is Rhizobium. It has

long been known that the inoculation of

effective strains of the symbiotic Rhizobium can be beneficial for legu-

minous pulses and oilseed (Isherwood,

2002). Inoculation with effective Rhizobium is a well known agronomic

practice to insure adequatenitrogen

nutrition of legume instead of fertilizer N.

Although commercial fertilizer products based on below-ground diversity

are already available, their effectiveness

depends on the natural conditions and plant clay organic soil and microbe

interaction. Regarding the product itself,

the inoculants is a living material and

there are problem due to the needs to

select the most effective strains, thedifficulty of quality control, the short

shelf-life, and the need to avoid high

temperatures in storage. The Food andFertilizer Technology Center for the Asia

and Pacific Region (FFTC, 1997)

reported that, while there is an increasinginterest in Asia in the use of N-fixing

bacteria, the technology of producing and

using them still at an early stage. There are

a very large number of differentmicroorganisms in microbial products and

they are often not identified yet, whereas

some are crop-specific. There is a greatneed for standards, simple and accurate

ways of measuring their effectiveness.

Therefore, an appropriate management of

bio-fertilizer in agriculture and plantationsoil quality could be maintained.

Benefits of legume cover crops as

above-ground bio-diversity and its

relationship with below-ground bio-

diversity

In the land farming, legume covercrops can reduce fertilizer costs and

herbicide or other pesticides, improveyields by enhancing soil health, prevent

soil erosion, conserve soil moisture,

protect water quality, and help safeguard

personal health. Many legume cover crop

offer harvest possibilities as forage,grazing or seed that work well in system

with multiple crop enterprises and

livestock. For instance, fertilizer

recommendation made for oil palm plantation is of higher dosages on non-

legume cultivation than on legume

cultivation. In addition, Sarrantonio(1998) stated that cover crops provide

many benefits, but they are not do-it-all

“wonder crops”. To find a suitable covercrop or mix of covers need to identify the

best time and place for a cover crop in

farming system. Cover crops improve soil

by (i) speeding infiltration of excess

surface water, (ii) relieving compactionand improving structure of over tilled soil,

(iii) adding organic matter that encourages

beneficial soil microbial life, and (iv)enhancing nutrient cycling. Further,

nitrogen is a central component of cell



62


proteins and is used for seed production. It

exists in several chemical forms and

various microorganisms are involved in itstransformation. Legume cover crops, in

association with specialized bacteria

called rhizobia are able to convert nitrogengas in the atmosphere into soil nitrogen

that plants can use. Crops grown in fields

after legumes can take up at least 30 – 60 percent of the N by legumes.

Consequently, the farmer can reduce

N fertilizer applications. The beneficial of N value of legume cover crop could

evaluated, both agronomically andeconomically. The nitrogen provided by

N-fixation is used efficiently in natural

ecosystems. Sarrantonio (1998) suggestthat in an agricultural system, however,

soil and crop management factor often

interfere with nature’s ultra-efficient use

of organic or inorganic N. Learning a bitabout the factors affecting N-use

efficiency from legume plants will help

build the most sustainable croppingsystem.

Management of above-ground covers

is an important aspect of rubber and oil palm cultivation. In these area, Pueraria

phaseoloides, Calopogonium caeruleum,

and Centrosema pubescens are widely

cultivated for rubber and oil palm.Legume cover crops, normally compete

successfully against volunteer weed

growths, particularly Mikania and Asystasia. Therefore, a good legume

cover crops should be maintained for as

long as possible after planting. In some

environments it will be possible tomaintain legume cover crops throughout

the life of the rubber and oil palm. Also,

Ahmad Tajuddin & Wan Zahari (1991)

stated that forage species that grow in oil palm and rubber plantations include all the

palatable plant species that thrive under

this microenvironment. The leguminous

cover crops are grown at early stages of

the tree crop development in first fiveyears, and they are gradually replaced by

the shade-tolerant species when the

canopies close. Some common goals forcover crops are to provide nitrogen, add

organic matter, improve soil structure,

reduce soil erosion, provide weed control,manage nutrients, and furnish moisture-

conserving mulch. Like other plants,

legumes cover crops need nitrogen togrow. They can take it from soil if present

enough in forms they can use. Legume

roots also seek out specific strains of soil-

dwelling bacteria that can fix nitrogen gas

from the air for use by the plant. Whilemany kinds of bacteria compete for space

on legume roots, the root tissues will only

begin this symbiotic N-fixing processwhen they encounter a specific species of

Rhizobium bacteria.

The nitrogen fixation bacteria as a

simple model for expressing rela-

tionship between above- and below-

ground bio-diversity

Plants of the family Leguminoseae

play many roles in agriculture, but perhapsmost important is their ability to use free

nitrogen gas (N2) in the atmosphere as a

source of nitrogen. Only certain

prokaryotes possess the nitrogenaseenzyme required to convert N2 to

ammonia (NH3), a process called nitrogen

fixation. Legumes fix atmosphere N byestablishing a functional relationship

(symbiotic) with a group of soil bacteria

collectively called rhizobia. The life cycle

of the rhizobia has been intensivelystudied. It is now understood that a

particular strain of Rhizobium in the soil is



63

Goenadi & Santi

attracted to its particular host. Since the

rhizobia are motile, they actually swim totheir host. Once they reach the host’s root

system they attach to single root hair and

release substances that stimulate the hair

to allow the Rhizobium to penetrate it.The Rhizobium proceeds to invade

certain cells in the root where they

produce chemicals that stimulate thegrowth of these cells to produce the

tumor-like nodule (Hurlbert, 1999).

Nitrogen gas (N2) from air in the spaces

between soil particles enters the nodule.

The bacteria contribute an enzyme thathelps convert the gas to ammonia (NH3).

The plant uses this form of N to construct

amino acids, the building blocks for protein. In return, the host legume supplies

the bacteria with carbohydrates to fuel the

N-fixation process. The nitrogen fixed by

rhizobia gives benefits to legume covercrops production in two ways: (i) by

meeting most of the legume cover crops

nitrogen needs and (ii) by enriching thesoil for the benefit of subsequent crops.

The rate of N fixation is determined

largely by genetic potential of the legume

species and by the amount of plant-available N in the soil. Rhizobium

inoculation should be considered in all

legume green manure crops to gainmaximum benefit from nitrogen fixation

in the shortest possible time. The fixed

nitrogen is subsequently made available to

the host plant. When the host plants die,

their nitrogen is returned to the soil for use by other organisms.

Inoculants technology for functional

relationship induction between above-

and below-ground bio-diversity

Although rhizobia seem to be as

widely distributed as the legumes

themselves, many soils used for legume

cultivation do not contain adequate

numbers of highly effective rhizobia.They may be devoid of rhizobia, they may

contain low numbers of effective strains or

they may contain high numbers ofineffective or partially effective strain

(Herridge et al. 2002). Allen & Allen

(1961) listed four indicator that, if

positive, would necessitate inoculationrhizobia for optimum growth of legume

i.e. (i) the absence of the same or

symbiotically-related legume in theimmediate past history of the land, (ii)

poor nodulation when the same crop was

grown on the land previously, (iii) when

the legume followed a non-legume in the

rotation, (iv) when the land wasundergoing reclamation. Microbial ino-

culants have received only limitedacceptance by farmers in developing

countries. They show considerable

promise but more development is

required. Inoculants technology is used

widely on commercial scale in thedevelopment countries, specifically in

South East Asia i.e. Thailand, Philippines,

Vietnam, and Indonesia. Research is

necessary to adapt legume nodulating bacteria technology and develop

appropriate Rhizobium strains and ino-

culation procedures for use in the tropicalarea. Current inoculation technology from

Indonesian Biotech-nology Research

Institute for Estate Crops (IBRIEC),Indonesia, i.e. RhiPhosant have been used

in North Sumatera, East Java and Papua.

In these area, legumes are grown under

marginal conditions with minimal input

and confronted with one or more soil andclimatic stresses. Field experiment in

Ngawi (East Java), indicated that by

inoculating Rhiphosant to soybean(Glycine max var. Wilis), the yield could

increase up to 16.8-48%/ha (Rijono,

personal communication).



64


In other case, Hatfindo (2000)

suggested that the biodiversity of below-

ground communities, as well as theirfunctions are strongly influenced by the

diversity of above-ground communities.

Rapid rates of land-form disturbancesfollowed by land degradation due to

mining operations and infrastructure

development activities at PT. FreeportIndonesia, in Papua, may result in

reduction in soil-biota biodiversity. In

addition, alterations of biological regu-lation activities within soil may lead to

loss of ecosystem function. Consequently,the ability of the ecosystem to recover and

the sustainability of land system may be

reduced. Hatfindo have applied inoculanttechnology of RhiPhosant to identify

potential “entry points” for improving

tailings reclamation through the

introduction or management of potentialsoil microorganism and plantation

development in tailing areas. The number

of nodule of Pterocarpus indicus,Paraserianthes falcataria, and

Enterolobium cyclocarpum could increase

38.7, 63.7, and 30.9% respectively byinoculating RhiPhosant to seeds before

putting them in the seeder.

RhiPhosant (Rhizobial & Phosphate

Solubilizing Inoculants) consisting of Bradyrhizobium japonicum a symbiotic N

fixation and Aeromonas punctata a

phosphate solubilizing bacteria. Thecommercial inoculants are formulated by

growing the bacteria in broth and mixing

the broth with ground peat and highly

active mineral as a carrier which is storeddry. Application technology is carrier

based inoculants. The inoculant that has

been formulated with a carrier was mixed

with seed just before putting it in theseeder. Development of this inoculants

technology was bases on interaction of

soil minerals with natural organic and

microbes.

Peat is the most commonly-usedcarrier for rhizobial inoculants because of

its high moisture-holding capacity and

dual abilities to foster multiplication orrhizobia in the peat itself and protect the

rhizobia once they are applied to the seed

coat, however, it by no means the onlycarrier tested or used. Brockwell et al.

(1995) presented an imposing list of

alternative inoculants carriers thatincluded the following: coal, charcoal

alone or with composted straw, mixtures

of soil and compost, mixtures of soil, peat,

composted bark and wheat husks, bagasse,

coir dust, composted corn cobs, filter mud,lignite, bentonite and talc. Goenadi

(1995) have been determined most

suitable carrier material, particularly in theform of clay and organic minerals. The

quality of the mixture as carrier was

evaluated on the basis of microbial

population dynamic. As the results ofthese, addition of humic substance to

minerals up to 2.5% (v/w) yielded a

significant increase to the bacterial population at two weeks after inoculation.

Keyser et al. (1992) regarded the

properties of a good inoculants carrier as:

(i) high water holding capacity, (ii) non-toxic to the rhizobia, (iii) easy to sterilise

by autoclaving or gamma irradiating, (iv)

readily available and inexpensive, (v)sufficiently adhesive for effective

application to seed, (vi) pH buffering

capacity, and (vii) cation and anion-

exchange capacities.Furthermore, the rhizobial strain used

in inoculants should have the ability to

form nodules and fix N2 with the target

legume, compete in nodule formation with populations of rhizobia already present inthe soil, fix N2 with a wide range of host



65

Goenadi & Santi

genotypes and across different

environments, form nodules and fix N2 in

the presence of soil nitrate, grow inartificial media, in inoculants carrier and

in the soil, persist in the soil, particularly

for annually regenerating legumes,migrate from the initial site of inoculation,

colonize the soil in the absence of the

legume host, maintain genetic stability,and be compatible with agrochemicals.

They should also have as wider host range

as possible, have low mortality oninoculated seed and have the ability to

colonize the rhizosphere or the host plant.Strains of rhizobia used in inoculants are

selected in strain trials that ideally cover

the physical environments and soil typesthat the inoculants are to cover. This may

mean a number of multi-site evaluations

over a number of seasons. Legume cover

crops inoculants are prone to loss ofquality because of variation in the

organism and from unforeseen factors

affecting some aspect of growth orsurvival. It is therefore essential that a

quality control system be established. The

control laboratory maintains and suppliesrecommended strains annually for ability

to fix nitrogen, assess quality of culture

during and after manufacture, and

conductany research that is necessary toovercome problems associated with

production and survival.

Conclusions

Soil organisms as a below-ground

bio-diversity are contribute a wide rangeof essential services to the sustainable

function of all ecosystems, such as

regulating nutrient cycles and the

dynamics of soil organic matter, soilcarbon sequestration and greenhouse

emission, enhancing the amount and

efficiency of nutrient acquisition by the

vegetation. Few data are available fromIndonesia regions, where it is suspected

that the highest level of bio-diversity may

be found. Although the bio-diversity ofthe community of organism below-ground

is probably higher in most cases than that

above-ground, it has generally beenignored in surveys of ecosystem bio-

diversity.

The process of land conversion andagricultural intensification are significant

cause of below-ground biodiversity loss

with risks of impact on ecosystem service.

Enhancement of below-ground bio-

diversity may be accomplished by directmanipulation, such as re-inoculation with

indigenous of N2-fixing bacteria and other

microbes. Agro technology based on

relationship between above and below-ground bio-diversity have beneficial effect

on development of agriculture.

A lack of domestic inoculants production plants also constrains research,

development, and production enterprises.

Relationship between above and below-

ground technology would benefit forincreasing economic and political pressure

for greater energy efficiency in

agriculture, increased recognition bydecision makers in funding agencies and

in governments of the potential for

exploiting below-ground diversity in

developing country. With the advent ofmodern biotechnology, there is potential

to develop crops suited to diverse agro-

ecological conditions. By using the casestudy of functional relationship between

above and below-ground biodiversity, this

paper examines to extent to which

smallholder access to modern biotechnology innovations.



66


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