Livestock Research for Rural Development 24 (3) 2012 Guide for preparation of papers LRRD Newsletter

Citation of this paper

Benefits and limitations of biofertilization in agricultural practices

J S Carvajal-Muñoz and C E Carmona-Garcia*

Research Group on Urban and Hazardous Waste (GIRPSU)
Integrated Group on Civil Engineering Research (GIIC)
ing.juancarvajal@gmail.com
ing.juancarvajal@yahoo.com
* Research Group on Soil, Environment and Society
University of Magdalena. Santa Marta, Magdalena, Colombia. Carrera 32 No 22-08; Postal Code 2-1-21630

Abstract

The increasing impacts on the environment due to agricultural practices in the world have gradually affected the quality of the soil in terms of structure and biological equilibrium, which has required the development of alternative practices to minimize and mitigate those impacts, parallel to the improvement on the yield per cultivated area and economical benefits for producers and farmers. In addition, the amount of food that society of today require for processing and supply of the industry has encouraged the creation of new options for  agricultural practices, tending to be: i) less invasive to the environment, ii) cheaper than conventional techniques, iii) able to increase efficiency at low costs, iv) able to obtain better characteristics on harvests and, v) ease of use and implementation with no excessive technical requirements.

As a result, technologies such as biofertilization have emerged in order to minimize environmental impacts and take advantage of the resources available in the field. The main scope of this paper is to assess researches performed with the use of biofertilization, mentioning their advantages and limitations, reviewing some results on efficiency and benefits acquired in recent years and highlighting their potential for better agricultural practices worldwide. 

Key words: Agricultural expansion, biological fertilizers, nutrients, sustainability


Introduction

The growing need for supply of agronomic products for food and consumer goods processing by the modern society has caused substantial increases in agrarian activities in recent decades. As a result, the need for implementation of methods that allow, among other things, to improve the efficiency of crops, mitigate adverse impacts on the soil, reduce the use of chemical fertilizers, and increase revenues per cultivated area, have been addressed. For this reason, the implementation of conservative agriculture (CA) models has been a cornerstone of farming practices globally (Benitez et al 2002; Morte et al 2003). The CA focuses on reducing adverse impacts on the environment, increasing crop yields and inputs, and implementing sustainable techniques for development of agriculture. 

Biological fertilization is based on the use of natural inputs including fertilizers, decaying remains of organic matter, crops excess, domestic sewage, animal manure, and microorganisms such as fungi and bacteria (Chirinos et al 2006). They are used to improve fixation of nutrients in the rhizosphere, produce growth stimulants for plants, improve soil stability, provide biological control, biodegrade substances, recycle nutrients, promote mycorrhiza symbiosis, and develop bioremediation processes in soils contaminated with toxic, xenobiotic and recalcitrant substances (Morte et al 2003; Corpoica 2007; Rivera-Cruz et al 2008; Alvarez et al 2007). 

Additionally, the use of bio-fertilizers can improve productivity per area in a relatively short time, consume smaller amounts of energy, mitigate contamination of soil and water, increase soil fertility, and promote antagonism and biological control of phytopathogenic organisms (Chirinos et al 2006; Corpoica 2007; Porcuna et al 2002). The aforementioned aspects are translated into profitable benefits for farmers as a result of lower costs associated with the process of fertilization and higher crop yields (Fundases 2005; Gonzalez et al 2002). In this sense, biologic fertilizers application can bring benefits from an economic, social, and environmental point of view. However, the implementation of fertilization techniques requires feasibility studies, monitoring of environment variables involved in metabolic processes, acquisition of biological inputs, capital investment, time, and trained personnel (Plaster 2000; Vanegas 2003; Alegre 2000; Fresco 2003). In order to achieve a sustainable agriculture is necessary the implementation of plans, programs, projects and initiatives directed toward the minimization of environmental impacts and consequent benefits for farmers and producers.   

As a result of recent investigations performed to effectively assess the implementation of biological fertilizers under varying conditions, a review on their benefits and limitations is required to provide a valid background for academics, farmers and producers to perform future research complementing current work that deeply assess economical, environmental and social aspects related to the agricultural expansion worldwide. This paper focuses on the review of current research resulting from the use of biological fertilizers in different regions of the world to obtain a framework that facilitates the development of future investigations in the agricultural sector and, consequently, promote the reduction of environmental impacts associated to the permanent use of chemical fertilization. Firstly in this article, an introduction to biofertilization techniques is addressed to understand the fundamentals that explain their functioning. Next in the paper, benefits and limitations of biofertilizers are mentioned followed by current researches’ results from the use of the techniques in various geographical backgrounds. Finally, conclusions and recommendations complete the paper. 

Biological nitrogen fixation (BNF) 

Biological nitrogen fixation is considered a key process in the biosphere and fundamental constituent of sustainable agriculture. It allows the conversion of gaseous nitrogen (N2) to the mainly forms of available nitrogen (e.g., nitrite, nitrate, and ammonium) for the development of metabolic processes of plants (Kowalchuk et al 1999). The conversion process of gaseous nitrogen and similar products (more available for plant's growth) takes place by the action of microorganisms in the soil. These microorganisms include: Azospirillum, Azotobacter, Beijerinckia (i.e., microorganisms that establish associations with grass plants), Rhizobium, Bradyrhizobium, and Azorhizobium (i.e., bacteria establishing symbiosis with legumes), Frankia (i.e., symbiotic actinomycetes with woody plants), Nostoc (i.e., blue-green algae establishing symbiosis with different plants) or Anabahena (i.e., ferns) (Araujo et al 2001). 

Development of BNF depends on specialized microorganisms, i.e., those who are carriers of nitrogenase enzyme. These are responsible for its production through biological and physicochemical processes (Aseri et al 2008; Sessitsch et al 2002).Additionally, BNF has shown minimal environmental impacts. Its usefulness and efficiency for the optimum physical plant development have been extensively recognized (Araújo et al 2001; Sessitsch et al 2002). Sessitsch et al (2002) estimated that approximately 80% of fixed nitrogen on the planet is due to gram-negative activity of Rhizobium bacteria (Sessitsch et al 2002). The acquisition strategy for reducing atmospheric nitrogen by Rhizobium-legume-association is a complex process. Rhizobium induces the legume to form nodules, thereby establishing metabolic cooperation, in which the bacteria reduce nitrogen (N2) to ammonia (NH4). The latter is exported to the plant tissue to be assimilated into proteins and other complex nitrogenous compounds. Simultaneously, the leaves reduce carbon dioxide (CO2) into sugars through photosynthesis and transport it to the roots. There, Rhizobium provides ATP for the diatomic nitrogen immobilization, taking advantage from that source of energy and facilitating the development of photosynthetic and growth processes of plants (Kowalchuk et al 1999; Araújo et al 2004; Sessitsch et al 2002). 

In addition, it is estimated that Rhizobium-legume association is responsible for setting annually 35 million tons of nitrogen (Sessitsch et al 2002). This amount significantly influences the fertilization of soils globally and favors the development of agriculture and forestry activities in several parts of the world. 

Biological fertilization techniques 

Society must meet its food needs through agricultural resources. Therefore, the use of methods that are effective and feasible to obtain better yields and meet global demand of inputs has become increasingly necessary. Similarly, alternative methods arise to increase the soil fertility. The main scope of these methods is to provide greater efficiencies, increase the quality of agricultural products, minimize crop time, and reduce costs. On the other hand, contamination of soils, extensive and continuous use of chemical inputs and monoculture has led to the need of incorporating fewer invasive fertilization methods. Next in this research article, some biological fertilization techniques, that represent lower environmental, implementation costs and efficiencies comparable to conventional chemical fertilizers used in the world, are presented and explored. 

Benefits and limitations of biological fertilizers  

Biological practices can offer a wide range of opportunities for the development of better agrarian practices due to the advantages and benefits provided for the soil, products and farmers. Nevertheless, limitations of these practices are also well studied and recognized, which implies that feasibility studies should be carried out to find out better solutions for each particular case in agricultural activities. Next in this section, some benefits and limitations are mentioned to highlight the need of future research on some issues.


Table 1. Benefits and limitations of biological fertilizers (Chen 2006)

Benefits

Limitations

Biological fertilizers can mobilize nutrients that favor the development of biological activities in soils.

 

Maintenance of plant health is enhanced by the addition of balanced nutrients.

 

Food supply is provided and growth of microorganisms and beneficial soil worms is impelled.

 

As a result of the good structure provided to the soil, root growth is promoted.

 

The content of organic matter in soil is higher than normal levels.

 

Promotes the development of mycorrhizal associations, which increases the availability of phosphorus (P) on the soil.

 

Help to eliminate plantar diseases and provide continuous supply of micronutrients to the soil.

 

Contribute to the maintenance of stable nitrogen (N) and phosphorus (P) concentrations.

 

Improvements on the capacity of nutrients’ exchange in the soil.

Compost products have highly variable concentrations of nutrients. In addition, implementation costs are higher than those of certain chemical fertilizers.

 

Extensive and long-term application may result in accumulation of salts, nutrients, and heavy metals that could cause adverse effects on plant growth, development of organisms of the soil, water quality, and human health.

 

Large volumes are required for land application due to low contents of nutrients, in comparison with chemical fertilizers.

 

Main macronutrients may not be available in sufficient quantities for growth and development of plants.

 

Nutritional deficiencies could exist, caused by the low transfer of micro- and macro-nutrients.

Animal manure 

For several decades, animal manure has been widely used by farmers for soil fertilization, given the low costs associated with its production, transportation, and processing. This wide availability and the nutritional intake of trace elements make it an attractive alternative for the development of fertilization on soils suffering nutritional deficiencies. 

Manure has many benefits (Plaster 2000; Luévano et al 2001), which include: 

Aspects such as the type, age, and health of the animal affect the proportion of macro- and micro-nutrients available in the manure. For example, sheep and poultry manure contain high levels of nitrogen (N), while manure from pigs, cattle, and horses have lower proportions of this element. The type of bedding (i.e., ferns or other plants that serve as disposal of urine and excreta) also affects the quality of manure. Furthermore, the usefulness and usability of the product depends on the proportion of heavy metals and other chemical substances. The application of manure in the soil must be made in quantities or concentrations acceptable by rules and regulations from environmental and health authorities. In most cases, it is recommended that manure is sprayed in a thin layer over large portions of land, rather than stacked on a small portion (Luévano et al 2001). The purpose of the technique is to promote soil aeration, maximize the efficiency of agricultural production, and facilitate the development of biological activities that are able to create a medium rich in nutrients for plants growth.  

Although animal manure provides improved availability of nutrients and facilitates plants growth, it also has disadvantages and limitations of particular interest. Some of the limitations are referred to possible risks on the safety of consumers, physicochemical, and biological stability of soils. In this regard, high contents of ammonia from manure can burn foliage and roots of plants; the presence of manure could increase the amount of weed flora and costs associated with transportation, and manure application are superior to those of traditional techniques. Besides that, the presence of heavy metals (e.g., mercury, chromium, lead) pose a threat as a result of their carcinogenic potential and their capability of bio-accumulation and bio-magnification in the food chain. For this reason, the use of manure to fertilize soils should be well assessed and considered in order to evaluate the cost-benefit ratio. Also, technical tests must be carried out to verify its safety (Plaster 2000). Finally, excessive application of manure can generate important reductions of plants growth, extreme levels of nitrogen, ammonia, and salts that could lead to different undesired scenarios for farmers and the soil itself.

Arbuscular mycorrhiza (AM) 

Most plants of agricultural interest are endomycorrhiza and belong to the arbuscular mycorrhiza type (AM) (Stamford et al 2007; López et al 2001). Mycorrhiza is a mutualistic association existing between fungi and most land plants. These partnerships are easy to locate in distinct places, from aquatic to desert, occurring at different altitudes and latitudes (Guerra 2008). Therefore, its value in terms of availability and ease of use in various geographical conditions is widely recognized. 

The fungi that form symbiotic associations are obligated bio trophic, meaning that they can only complete their life cycle by colonizing roots of host plants. This type of symbiotic association has been called bio-fertilizer and crop bio-protector. It is also considered relevant for integrated management programs of soils and crops (Guerra 2008; Padilla et al 2006). Arbuscular mycorrhiza fungi belong to Glomeromycota division. The most abundant and diverse is the genus' Glomus, consisting of fungal inoculants (i.e., mycorrhiza fungi widely used in agricultural activities worldwide). Mycorrhiza inoculants application in soils provides benefits for agricultural and forest crops such as increased growth rate and tolerance of plants to drought and soil salinity (Guerra 2008). Salinas et al (2005) stated that Glomus (i.e., vesicular-arbuscular) could supplement or replace chemical fertilizers of crops in varying environmental conditions. 

The proper selection and application of arbuscular mycorrhiza fungi improves plant nutrition and increases the resistance of plants against pathogens and stress conditions (both biotic and abiotic). Furthermore, the wide range of options and applicability of AM in different regions makes it an attractive technique to replace, partially or completely, chemical fertilization of soils.

Biosolids 

Dumping of human waste treated at Sewage Treatment Plants (STP) on the soil has a fairly broad historical trajectory. In the early seventies, application of sewage sludge in soil or sediment began for agricultural and forestry purposes in the United States. In fact, the Environmental Protection Agency (U.S.EPA) estimates that half of the sludge produced in the United States are spread on the soil mostly applied as fertilizer in large portions of land (Dáguer 2003; Celis et al 2006). Biosolids can be applied to the soil through techniques such as dumping, injection, irrigation, among others, depending on the local environmental and financial conditions. These techniques help to decrease spreading of odors, insects influence on crops, minimize runoff losses, and loss of ammonia in the air (Dáguer 2003). 

Several options for using the sludge from STP are suitable, for example: landfill disposal, incineration, and direct application on the soil. The latter requires dissolving the sludge, before being applied to the soil, where it is decomposed by microorganisms and filtered by the soil matrix. Therefore, it is the most promising use from the economic and environmental perspective. Moreover, the composition of biosolids is useful for soil nutrition, which explains the increased rate of use as amendment in several countries (Jurado et al 2004). The U.S.EPA classifies biosolids according to their content of heavy metals. Those with lower concentrations can be applied under more flexible security controls. Biosolids with higher concentrations are not likely to be used. Hence, they must be incinerated or landfilled (Eddy 1999; Luévano et al 2001). The acceptance or denial of biosolids used as fertilizers is based on safety parameters, such as hazardous characteristics (i.e., corrosivity, reactivity, explosivity, toxicity, flammability, and biological hazards). If biosolids do not exhibit these characteristics, they can be certified as safe to the soil and may be applied (Jurado et al 2004). These sanitary regulations are primarily intended to reduce risks to human health and the environment based on the potential for contamination of water resources, crops, and ecosystems (Dáguer 2003).

Composting 

Composting is one of the oldest techniques used for the stabilization of natural wastes and soil biologic fertilization. The main objective of this practice is to obtain a stable, chemical and biological rich product with micro and macro nutrients (Coker 2006; Peigné et al 2004; Tognetti et al 2005).

The composting process works as follows: initially, strains of microorganisms break down living waste, generating temperature differentials (Petiot 2004), while the pH of the medium decreases as a result of the production of natural acids. Once the temperature gets close to 40°C, thermophilic bacteria initiate degradation processes, making the temperature to reach 65ºC (under these conditions the metabolism of certain fungi is deactivated). During this stage, biological transformation reactions are developed by actinomycetes and fungi spore forming bacteria. These quickly consume easily degradable compounds such as sugars, proteins, starch, and fat. In addition, the pH tends to be alkaline due to the release of ammonium ion. Once degraded the organic material, the reactions rate decreases as well as temperature. This stage is known as cooling. Both thermophilic and mesophilic fungi are capable of degrading cellulose during this phase. Finally, ripening process begins, which requires several months at least four to be completed. This stage can lead to the complete degradation of compounds and to obtain stable material. The composting process can lead to obtain: stable humus and humic- and fulvicin-acids; characterized by high nutritional value and potential for fertilization of soils with nutriment deficiencies (Plaster 2000; Tognetti et al 2005). 

Benefits provided by compost are broad and can be from the physical, chemical, biological and environmental realm. Application of compost depends on the conditions of organic matter, moisture, temperature, the pH and presence of microorganisms in the pile. For example, compost increases drainage and absorption of moisture in soils with structural deficiencies or lack of nutrients. It also permits to: (1) increase crop productivity, (2) promote plant growth by incorporation of essential nutrients, (3) facilitate implementation in different types of soil, (4) reduce runoff, and (5) obtain economic benefits for farmers (Tognetti et al 2005; Mills 2006).

Green manures 

Green manures consist of green plant tissue incorporated on the soil to correct or improve physical characteristics or its chemical properties. Fast-growing crops such as oats, vetch, berseem clover, rye, and peas are mainly used as green manures (Martín et al 2007; Bunch 1994). The use of green manure has a positive influence on certain soil characteristics. For example, soil nutrients susceptible to loss by drainage are retained. On the other hand, certain long-rooted manures capture nutrients from lower soil horizons and have the ability to transport them to the surface, which increases their availability for the development of metabolic processes of plants (Porcuna et al 2002).  

Green manures increase the amount of available organic matter in the soil for development of metabolic processes of native flowers and other plant species. Being in direct contact with the soil matrix, plant material is susceptible to microbial decomposition, which produces humic compounds that are able to increase the adsorption capacity of nutrients, promote drainage, aeration, and soil granulation. In addition, decomposition products serve as a substrate for those microorganisms responsible of biological transformation processes. These processes have a positive impact on the production of carbon dioxide, ammonia, nitrites, nitrates, and other simple compounds that are easily assimilated by plants for growth and development (Porcuna et al 2002; Alegre et al 2000; Plaster 2000; Bunch 1994).  

Finally, green manure applications can be combined with natural inputs to improve soil structure, minimize erosion, and increase water availability in the soil (i.e., trough evaporation reduction). For example, mineral fertilization with green manure increases yields per hectare and promotes development of mycorrhizal associations. It is also a source of essential nutrients and it is a way to foster development of AMF strains (Arbuscular Mycorrhizal Fungi) (Martin et al 2007). 

Microbial inoculants (MI) 

Microbial inoculants (MI) are substances or biological aggregates containing microbial populations as fermentation fungi, bacteria, and lactobacilli (Rolli 2007; Alfonso et al 2005). Their high nutritional content of salts allows reactions with organic matter in the soil, producing favorable substances for plant nutrition (e.g., vitamins, organic acids, chelated minerals, and antioxidants) (Welbaum et al 2004; Aranda et al 2005; Valencia et al 2001; Faggioli et al 2003). Microbial inoculants are capable to modify characteristics of the soil such as micro- and macro-flora and can improve biological balance (Berc et al 2005; Christry et al 2005). In addition, their antioxidant properties promote decomposition of organic matter and increase humus content in the soil matrix (Tognetti et al 2005; Suthar et al 2005). The latter has positive effects on plant growth, quality of harvests, and improvement of chemical, physical and biological stability of soils. 

With a rational use of MI, certain physical, chemical, and biological properties can be improved and suppression of biological diseases can be achieved (Plaster 2000; Reddy 2005; Tognetti et al 2005). In this regard: 

Seaweed extracts 

Seaweeds are mainly composed by trace, and major- and minor-elements helpful for plant nutrition. Other natural substances can also be found, whose effects are similar to those of certain growth regulators, vitamins, carbohydrates, proteins, and biocidal substances. They act against some pests, diseases, and chelating agents such as organic acids and mannitol (Canales 2001). The benefits of seaweed use in agriculture (greater efficiency and better fruit quality) may be evident from direct application of pure forms or its derivatives (Canales 2001; Canales 1999; Painter 1995). Species such as Ascophyllum nodosum contain macronutrients and micronutrients needed for cellular nutrition. Recent research has showed that vitamin supplements coming from these species can increase agricultural productivity and revenues. Similarly, it can promote availability of sugars, increase fruit size, minimize the time of cultivation, and help to obtain better shapes and tones of agricultural products (Canales 2001; Painter 1995). 

On the other hand, cyanobacteria (i.e., blue-green algae) are good at obtaining phosphates and micronutrients from media that may contain insoluble minerals. This ability gives them a level of superiority over other species, since they can supply essential nutrients for fertilizing soil and other substrates (Painter 1995). The Oregon State University evaluated the effects of applying seaweed extracts in apple orchards (i.e., apple trees). Two treatments were administered in areas of 1 acre. The first consisted on applying half pound of fungicides and herbicides, while the second on applying half pound of seaweed extracts. The authors concluded that 80% of orchards treated with seaweed extract produced fruits with better physical-chemical characteristics. Also 4% increases in yield per cultivated acre were reported by researchers (Eddy 1999). 

Vermicomposting

Vermicomposting is a biological fertilization technique consisting on the use of earthworms’ metabolism to produce humus with high nutrients content. To apply it, organic waste is required (e.g., manure, fruit peel, crop residues). The organic material passes through the digestive tract of worms, where it is transformed into a material rich in microorganisms, macro-, and micro-nutrients. Based on that process, a chemical and biological stable fertilizer is obtained (Berc et al 2004, Chhotu 2008; Reddy 2005). Use, storage, transport, and application of vermicompost in soils are of particular interest for those soils with nutritional shortages. This technique can be developed and applied successfully at both small and large-scale in various environments or under controlled laboratory conditions. 

Most common earthworm species used in vermiculture are: Eisenia foetida (i.e., Red California) and Eudrilus eugeniae (i.e., African Red) (Berc et al 2004; Chhotu 2008). The former presents advantages related to its rapid rate of reproduction under conditions of high temperature (above 40 ° C), high densities tolerance (10,000 to 50,000 worm/m2), and resistance to large variations in temperature, pH and moisture. In addition, this species have the ability to thrive in different substrates, under variable conditions. Therefore, Eisenia foetida is the most used worm in vermiculture (Tognetti et al 2005). On the other hand, Eudrilus eugeniae is a rapidly growing worm, prolific, but difficult to manage, since removal from the substrate is much more complex than that of Eisenia foetida (Chhotu 2008). 

Recently, effectiveness of vermicomposting in Havana, Cuba, has been proved (Berc et al 2005; Rosset 1998). The research study conducted by Berc et al (2005) addressed the need to increase productivity and reduce adverse environmental impacts caused by indiscriminate use of chemical fertilizers and pesticides to get better agrarian practices in their geographical area. The authors emphasized on the need of taking advantage from climatic (e.g., solar radiation, rainfall, multi-year average temperature), economic (e.g., agricultural potential), and social (e.g. availability of cheap labor) conditions to incorporate vermicomposting techniques and identify their advantages, disadvantages, and limits. The authors got yields exceeding 1.5 tones of humus in a year (in tropical zones) from three tons of organic substrate and 1 m3 of treated soil. Humus resulting from the process exhibited physical, chemical, and microbiological properties suitable for application on local soils with nutrients deficiencies such as phosphorus (P), nitrogen (N), and potassium (K) (Berc et al 2005; Roberts et al 2007). 

Efficiency and benefits of biological fertilization  

In the past two decades, agricultural activities based on conservative agriculture (CA) have become largely visible in the world. These have produced favorable results on agricultural productivity and sustainability of agriculture, for both traditional and extensive techniques. 

Development of research focused on biological fertilization has increased over the last ten to fifteen years. The increasing number of annual publications in international journals such as Scientia Horticulturae, Crop Production, Food Science and Technology, and Bioresource Technology indicates a widespread interest on the subject. In addition, professionals and specialized personnel are being required to solve different issues around the globe concerning mass production and environmentally friendly practices. 

In the next section of this paper, some national and international researches based on the use of biological fertilizers for agricultural production are presented and discussed. 

Alegre and Morales (2000) conducted a research on the East coast of Peru, evaluating the influence of green manures (cowpea and Crotolaria sp.), varying doses of cattle manure and pea compost over performance of potato crops. Yields of 55 t/ha (i.e., tones per hectare), 53 t/ha, 47.7 t/ha, 43.3 t/ha, and 33.3t/ha were obtained. These productivity values were not reported previously for that same species in the study area. The latter mentioned verifies the efficiency of biologic fertilizers in agricultural production. On the other hand, some physicochemical properties of the soil were improved and environmental impacts (caused by the continuous use of chemical fertilizers) were gradually mitigated. 

Singh and Sharma (2003) evaluated the growth of kidney bean plots fertilized with vermicompost from degraded municipal solid waste. The researchers used Eisenia foetida earthworms. The study was conducted in New Delhi by the Indian Institute of Technology. The results showed that the combination of microbial inoculants (i.e., P. sajor-caju, T. Haezianum and A. Chrocooccum) with vermicomposting has a positive effect on the growth of kidney bean crops. The significant role played by fungi on the degradation rate of solid waste and the significant involvement of bacteria in the atmospheric fixation of nitrogen and subsequent transformation into more available forms were emphasized by the authors. 

Rajendran and Devaraj (2004) reported 40% increases in the levels of phosphorus (P) and nitrogen (N) through the use of the microbial species: Azospirillum, Phosphobacterion, MA and Frankia, during the growth process of Australian pine (Casuarina equisetifolia). The authors concluded that the growth phase of the pine is positively affected by incorporating microbial inoculants on the substrate. 

In addition, Berc et al (2004) identified that worm from the genus Eisenia foetida (i.e., Red California) used to fertilize crops such as tobacco, cacao, coffee, and rice have a high potential for agricultural development in tropical areas. Specifically, the authors reported 30% yield improvements by using the mentioned species on potato, banana, tomato, garlic, coffee, and cocoa crops. Similarly, the amount of chemical fertilizers used was reduced by 40%. 

Alfonso et al (2005) used mineral fertilizers to improve yield performance on tomato crops. The authors reported water savings close to 25%, pesticide use savings of 40%, and 25 to 30% reduction of mineral fertilizers use. Furthermore, increases of 10% yield per hectare were observed for crops treated with Arbuscular Mycorrhizal (AM). The resistance of plants to the action of pathogenic microorganisms was higher with the use of AM. 

Treatment of cows’ feces through anaerobic and aerobic digestion has been used as a strategy for biological control of fungal species in crops, as reported by Kupper et al (2006). The authors used a bio-fertilizer obtained from biological digestion of feces to control the growth of Guignardia citricarpa sp., which, for years, incorporated black spots on the peel of citrus fruits like orange, tangerine, and lemon. It was concluded that compost manure coming from cattle is useful for biological control and obtaining of better fruits, suitable for sale and consumption. 

Padilla et al (2006) reported increases close to 36% in the production of melons from the incorporation of arbuscular mycorrhizae (AM) in crops. Besides that, 100% saving in the use of phosphate fertilizers, 20% saving on potassium fertilization and nitrogen, 25% saving of water, and 100% reduction in fungicide use were obtained during the research study. In this sense, the authors concluded that polyethylene padding techniques, along with microbial inoculants (i.e., probiotics) in the cultivation of melons, can increase proportions of mycorrhizae in the soil and favorably influence the elimination of pathogenic fungi (e.g., Alternaria , Fusarium and Rhizoctonia). 

Classen et al (2007) quantified the effect of vermicomposting from pig excreta on growth process of turnips. The researchers assessed the influence of rainfall regimes and the amount of bio-fertilizers applied on the yield per acre. As a result of the experimental design, increases in the size of turnip leaves and higher growth rates were reported. Fresh fruits size obtained by using the technique was superior to that of the control treatment. The authors concluded that productivity increased by a factor between 2 and 5, suggesting benefits for the application of vermicomposting on tropical areas.  

Responses on the photosynthetic process of coffee plants by addition of organic fertilizers have been evaluated by Gordillo et al (2008). The authors used photo acoustic techniques to compare the photosynthetic activity of plants treated with chemical fertilizers and others with bio-fertilizers (i.e., from microbial type). The procedure consisted in applying white light, from an artificial xenon lamp, on two 7-months-age coffee plant treatments to evaluate the production of oxygen (O2) and energy storage. For assessment and monitoring purposes, photo acoustic and pressure detectors were used. The first treatment received chemical fertilizers, while the second received organic fertilizers. According to the authors, organic fertilizers encourage and accelerate photosynthetic activity, allowing it to be faster and minimizing stress in plants. The authors concluded that biological products for fertilization of coffee are a sustainable and a clean alternative that can be replicated in different geographical areas. 

Gharib et al (2008) evaluated the potential application of compost and bio-fertilizers in oregano crops (Majorana hortensis L). Researchers created a microbial inoculum with a mixture of Azospirillum brasiliense, Azotobacter chroococcum, Bacillus polymyxa, and B. circulans. Main results indicated that combined use of bio-fertilizer on crops provides better yield performance, higher by a factor of two, and better physical characteristics of individual plants than those from nitrogen fixing bacteria or compost extracts. The authors concluded that inoculation of oregano (marjoram) with 15% and 30% compost extracts and bio-fertilizer mixtures has beneficial effects on plant growth, fat content, and dry matter production, as a result of hormonal stimulation and addition of combined forms of nitrogen (N). 

Sierra and Moreno (2008) investigated the feasibility of bio-fertilizers prototypes based on native bacteria from rice crops (Oryza sativa). The research used complex mixtures of nitrogen-fixing bacteria with humic substances (Polyethylene Glycol, Carbopol®), and chelates. The formulations rate of application was considered for a 3-month treatment period. The authors reported 10% increases in yield production of the mixtures, passing from 7,625 kg/ha to 8,500 kg/ha. Main outcomes deal with the importance of bio-fertilizers to get higher revenues and increase productivity, in order to obtain, progressively, a sustainable agricultural development. 

The effect of applying commercial bio-fertilizers from microbial type, phosphoric, and Cerealien® in tangerine crops was evaluated by Mohamedy and Ahmed (2009). The research consisted on the application of varying doses of bio-fertilizers solely or combined in mandarin crops. The response variables took into account were: type and size of fruit and presence of root diseases (i.e., rotting of the roots). According to the authors, the use of biological fertilizers, combined with humic acids, can reduce the incidence of disease on the roots by 20%, as well as increase productivity by 15% and improve physical characteristics of tangerine fruits. 

Bocchi and Malgioglio (2010) used aquatic cyanobacteria Azolla-Anabaena as fertilizer in rice paddies of northern Italy. This species have been frequently used in rice crops in different regions of the world, especially in Asia (e.g., Thailand, China, Indonesia, and India). To monitor the process, dynamics of plant growth, resistance/tolerance to low temperatures, and presence of herbicides in the soil were taken into account. The research allowed obtaining yields close to 40 kg nitrogen/ha during a 3-month period and verifying increases in growth rate of rice. Furthermore, higher resistance of Milan species (named by authors) to the presence of herbicide Propanil was evidenced. 

Thenmozhi et al (2010) quantified the increase in biomass production and growth of Amaranthus and hard pea species by using bio-fertilizers (i.e., mix of biogas, vermicomposting, microbial inoculants Azospirillum and Pseudomonas, and a combination of them). Sole or combined additions of organic fertilizers were evaluated and the main outcomes were that the application of organic fertilizers in combination is much more efficient than individually in terms of plant growth. Moreover, the use of biogas and vermicompost permitted to identify better growth of plants (i.e., with larger leaves and healthier roots) and biomass production in a 20-days period. 


Conclusions and recommendations


Acknowledgements

The authors offer special acknowledgements to the Research Group on Hazardous and Solid Waste (GIRPSU, for its Spanish spelling) and Research Group on Soil, Environment and Society at the University of Magdalena. Also, thanks are due to Eng. Adriana Mera for her invaluable help during her stay at the University of Magdalena, as director of GIRPSU. Similarly, gratitude is expressed to engineer Alvaro Castillo Miranda for his support at the head of the research group and management of the Environmental and Sanitary Engineering program at the University of Magdalena. 


References

Alegre C y Morales F 2000 Concepción y manejo del suelo en agroecología. Lima, Perú. 

Alfonso E, Leyva A y Hernández A 2005 Microorganismos benéficos como biofertilizantes eficientes para el cultivo de tomate (Lycopersicon esculentum, Mill).Revista Colombiana de Biotecnologia 2(2): 47-54. Available online at http://www.revistas.unal.edu.co/index.php/biotecnologia/article/view/498/891 

Álvarez C, Scianca C, Barraco M y Klappenbach J 2007  Impacto de fertilizantes biológicos sobre la productividad del cultivo de girasol. Córdoba, Argentina: Instituto Nacional de Tecnología Agropecuaria. 6 p. Available online at http://www.crinigan.com/ensayos/girasol/INTA%20Villegas%200607.pdf 

Aranda E, Sampedro I, Martín J, Delgado M A, Arriagada C, García-Romera I y Ocampo J A 2005 Disminución por hongos saprobios de la fitotoxicidad del alpeorujo seco y extractado. Optimización de su uso como fertilizante biológico y para control de hongos fitopatógenos. CAO01-008. Granada, España. Available online at http://www.expoliva.com/expoliva2005/simposium/comunicaciones/OLI-57.pdf 

AraujoY, Luizao F and Barros E 2004 Effect of earthworm addition on soil nitrogen availability, microbial biomass and litter decomposition in mesocosms. Biology and Fertility of Soils 39(3): 146-152. Available online at http://www.springerlink.com/content/efuh7rcdgvtg07am/ 

Aseri G K, Jain N, Panwar J, Rao AV, Meghwal P R 2008 Bio-fertilizer s improve plant growth, fruit yield, nutrition, metabolism and rhizosphere enzyme activities of Pomegranate (Punica granatum L.) in Indian Thar Desert. Scientia Horticulturae 117(2): 130-135. 

Benitez J, Vaneph S y Bot A 2002 Plantando conceptos y cosechando buenos resultados. Leisa Revista de Agroecología 18(3): 6-9. 

Berc J, Muñiz O and Calero B 2004 Vermiculture offers a new agricultural paradigm. Biocycle 45(6): 56-57. 

Bocchi S and Malgioglio A 2010 Azolla-Anabaena as a bio-fertilizer for rice paddy fields in the Po valley, a temperate rice area in northern Italy. International Journal of Agronomy. Volume 2010. 1-5. Available online at http://www.hindawi.com/journals/ija/2010/152158/ 

Bunch R 1994 El uso de abonos verdes por agricultores campesinos: lo que hemos aprendido hasta la fecha.  Informe técnico N°3. 2ª ed. Honduras: Fundación Interamericana. Available online at http://www.cidicco.hn/archivospdf/Inftecnico3.pdf   

Canales-López B 1999 Enzimas-algas: posibilidades de su uso para estimular la producción agrícola y mejorar los suelos. Terra Latinoamericana 17(3): 271-276. Available online at www.chapingo.mx/terra/contenido/17/3/art271-276.pdf

Canales-López B 2001 Uso de los derivados de algas marinas en la producción de papa. Tomate, chile y tomatillo: Resultados de investigación. Ponencia. Buenavista, Saltillo, Coahuila, 29 de octubre del 2001. Available online at http://www.uaaan.mx/academic/Horticultura/Memhort01/Ponencia_03.pdf 

Celis J, Sandoval M, Zagal E y Briones M 2006 Effect of sewage sludge and salmon wastes applied to a Patagonian soil on lettuce (Lactuca Sativa L.) germination. Journal of Soil Science and Plant Nutrition 6(3): 13-25. Available online at http://www.scielo.cl/scielo.php?pid=S0718-27912006000300002&script=sci_arttext 

Chen J H 2008 The combined use of chemical and organic fertilizers and/or bio-fertilizer for crop growth and soil fertility. International workshop on sustained management of the soil-rhizosphere system for efficient crop production and fertilizer use. Taiwan: National Chung Hsing University. Available online at http://www.agnet.org/library/tb/174/ 

Chhotu J and Fulekar M 2008 Vermicomposting of vegetal waste: a biophysicochemical process based on hydro-operating reactor. African Journal of Biotechnology 7(20): 3723-3730. Available online at http://www.ajol.info/index.php/ajb/article/viewFile/59420/47714 

Chirinos J,  Leal A y Montilla J 2006 Uso de insumos biológicos como alternativa para la agricultura sostenible en la zona sur del Estado Anzoátegui. Revista Digital Ceniap Hoy 11: 1-7. Available online at http://cadenahortofruticola.org/admin/tecno/76uso_insumos_biologicos_alternativa_agricultura_sostenible.pdf  

Christry M and Ramaligam R 2005 Vermicomposting of sago industrial solid waste using epigeic earthworm Eudrilus eugeniae and macronutrients analysis of vermicompost. Asian Journal of Microbiology Biotechnology and Environmental Sciences 7(3): 377-381. 

Classen J, Rice M and Sherman R 2007 The effects of vermicompost on field turnips and rainfall runoff. Compost Science & Utilization. 15(1): 34-39. 

Coker C 2006 Environmental remediation by composting. Biocycle 47(2):18-23 Available online at http://www.brownbearcorp.com/testimonials/Environmental%20Remediation%20by%20Composting.pdf 

Corpoica, Gobernación de Antioquia y FAO 2007 Manual de buenas prácticas agrícolas en la producción de fríjol voluble. Medellín: FAO. 168 p. Available online at http://www.fao.org.co/manualfrijol.pdf 

Dáguer G P 2003 Gestión de biosólidos en Colombia. Congreso Internacional de ACODAL “Sociedad, Ambiente y Futuro”. Santiago de Cali, Colombia, 29-31 de octubre 2003. Available online at http://www.bvsde.paho.org/bvsaar/fulltext/biosolidos.pdf 

Eddy D 1999 Eye on micronutrients: There are plenty of materials you can use to fertilize your crops. Here’s a look at what’s hot. American Vegetable Grower 47(1): 48-49. 

Faggioli V, Cazorla C, Vigna A y Berti M 2003 Fertilizantes biológicos en maíz.: ensayo de inoculación con cepas de Azospirillum brasilense y Pseudomonas fluorescens. Córdoba, Argentina: Instituto Nacional de Tecnología Agropecuaria. Available online at  http://www.inta.gov.ar/mjuarez/info/documentos/Suelos/fertbio07.pdf 

Fresco L 2003 Fertilize the plant, not the soil. UN Chronicle 40(3): p. 62 

Fundases y Asocolflores 2005 Biofertilizantes como alternativa nutricional en ornamentales. Revista Virtual Pro. Available online at http://www.revistavirtualpro.com/revista/index.php?ed=2006-10-01&pag=11 

Gharib FA, Moussa L A and Massoud O N 2008 Effect of compost and bio-fertilizer s on growth, yield and essential oil of sweet marjoram (Majorana hortensis) plant. International Journal of Agriculture & Biology 10(4): 381-387. Available online at http://www.fspublishers.org/ijab/past-issues/IJABVOL_10_NO_4/4.pdf 

González F, Escamilla E y Luna A 2002 Una estrategia para lograr la sustentabilidad campesina. La recuperación del suelo. Leisa Revista de Agroecología 18(3):17-19. Available online at http://subscriptions.leisa.info/index.php?url=getblob.php&o_id=67124&a_id=211&a_seq=0 

Gordillo F, Zárate F, Mejía C, Rivera L Y, Ariza H 2008 Análisis de la actividad fotosintética de plantas de café utilizando la técnica fotoacústica. Revista Colombiana de Física. 40(1): 186-189. Available online at http://revcolfis.org/publicaciones/vol40_1/4001186.pdf 

Guerra B E 2008 Micorriza arbuscular. Recurso microbiológico en la agricultura sostenible. Tecnología en Marcha 21(1): 191-201. Available online at http://www.tec.ac.cr/sitios/Vicerrectoria/vie/editorial_tecnologica/Revista_Tecnologia_Marcha/pdf/tecnologia_marcha_21-1/191-201.pdf 

Jurado-Guerra P, Luna M and Barretero R 2004 Beneficial use of biosolids as organic fertilizers in arid and semiarid rangelands. Técnica Pecuaria en México 42(3): 379-395. Available online at http://www.tecnicapecuaria.org.mx/journal/publicacion04.php?IdPublicacion=438 

Kowalchuk G A, Naoumenko Z S, Derikx J L, Felske A, Stephen J R and Arkhipchenko I A 1999 Molecular analysis of ammonia-oxidizing bacteria of the β-subdivision of the class proteobacteria in compost and composted materials. Applied and Environmental Microbiology 65(2): 396-403. 

Kupper K C, Bettiol W, de Goes A, de Souza P S, Bellotte J A M 2006  Bio-fertilizer  for control of Guignardia citricarpa, the causal agent of citrus black spot. Crop Protection 25(6): 569-573. 

López -Gutiérrez J 2001 Micorrizas arbusculares y actividades enzimáticas en la rizósfera de Trachypogon plumosus Ness en tres sabanas de suelos ácidos. Acta Biológica Venezuelica 21(2): 49-57. 

Luévano A y Velázquez N E 2001 Ejemplo singular en los agronegocios. Estiércol vacuno: de problema ambiental a excelente recurso. Revista Mexicana de Agronegocios. Año 5 Vol. 9: 306-320. Available online at http://redalyc.uaemex.mx/pdf/141/14100905.pdf 

Martín G, Costa Rouws J, Urquiaga S and Rivera R A 2007 Crop rotation of Canavalia ensiformis green manure of maize and arbuscular mycorrhize in an eutric rodic nitisol of Cuba. Agronomía tropical 57(4):313-321. Available online at http://www.scielo.org.ve/pdf/at/v57n4/art07.pdf 

Mills T 2006 Composting cafeteria residuals with earthworm. Biocycle 47:54-55. Available online at http://www.redorbit.com/news/science/413042/composting_cafeteria_residuals_with_earthworms 

Mohamedy E and Ahmed M A 2009 Effect of bio-fertilizer s and humic acid on control of dry root rot disease and improvement yield quality of mandarin (Citrus reticulate Blanco). Research Journal of Agriculture and Biological Sciences 5(2):127-137. Available online at http://www.aensionline.com/rjabs/rjabs/2009/127-137.pdf 

Morte A, Gutiérrez A, Dreyer B, Torrente P y Honrubia M 2003 Biofertilizantes de última generación. Retrieved April 27, 2008, from http://www.carm.es/web/integra.servlets.Blob/AsuncionMorte.pdf?ARCHIVO=AsuncionMorte.pdf&TABLA=ARCHIVOS&CAMPOCLAVE=IDARCHIVO&VALORCLAVE=20940&CAMPOIMAGEN=ARCHIVO&IDTIPO=60&RASTRO=c503$m4632  

Padilla E, Sánchez JA, Troncoso R, Sánchez A y Esqueda M 2006 Efecto de biofertilizantes en cultivo de melón acolchado con polietileno. Revista Fitotecnia Mexicana 29(4): 321-329. 

Painter T J 1995 Bio-fertilizer s: exceptional calcium binding affinity of a sheath proteoglycan from the blue-green soil alga Nostoc calcicola. Carbohydrate Polymers 26(3): 231-233. 

Peigné J and Girardin P 2004 Environmental impacts of farm-scale composting practices. Water Air Soil Pollution 153(1-4): 45-68. Available online at http://www.springerlink.com/content/pgq62022070766nv/ 

Petiot C and Guardia A 2004 Composting in a Laboratory Reactor: A review. Compost Science & Utilization 12(1): 69-79. 

Plaster E 2000 La ciencia del suelo y su manejo. Madrid: Thompson Editores. p. 248. 

Porcuna J L, Arnau J, Jímenez A, Ocon C and Zacares V 2002 Agroecología y agricultura ecológica: Hacia una reconstrucción de la soberanía alimentaria. Valencia, España. 3p.  

Rajendran K y Devaraj P 2004 Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with bio-fertilizer s in farm land. Biomass and Bioenergy 26(3): 235 –249. 

Reddy K and Shantaram M 2005 Potentiality of earthworms in composting of sugarcane byproducts. Asian Journal of Microbiology Biotechnology and Environmental Sciences 7(3): 483-487. 

Rivera-Cruz M, Trujillo A, Córdova G, Kohler J, Caravaca F, Roldán A 2008 Poultry manure and banana waste are effective bio-fertilizer  carriers for promoting plant growth and soil sustainability in banana crops. Soil Biology & Biochemistry 40(12):3092-3095. 

Roberts P, Edwards-Jones G, and Jones D L 2007 Yield responses of wheat (Triticum aestivum) to vermicompost. Compost Science & Utilization 15(1): 6-15. 

Rojas J y Moreno N 2008 Producción y formulación de prototipos de un biofertilizante a partir de bacterias nativas asociadas al cultivo de arroz (Oryza sativa). Revista Colombiana de Biotecnología. 10(2): 50-62. Available online at http://redalyc.uaemex.mx/pdf/776/77610207.pdf 

Rolli U 2007 Microorganismos efectivos EM en la agricultura. Retrieved March 3rd, 2009 from http://www.emmexico.com/agricultura.pdf 

Rosset P 1998 Alternative Agriculture Works: the case of Cuba. Monthly Review 50(3):137-146. 

Salinas J R, Díaz A, Garza E y Garza I 2005 Efectos de la labranza y biofertilización en propiedades del suelo que afectan la sostenibilidad de la producción de fríjol. Ciencia y Tecnología Alimentaria 5(1): 30-34. Available online at http://redalyc.uaemex.mx/src/inicio/ArtPdfRed.jsp?iCve=72450105# 

Sessitsch A, Howieson J G, Perret X, Antoun H and Martínez-Romero E 2002 Advances in Rhizobium research. Critical Reviews in Plant Sciences 21(4): 323-328. Available online at http://www.bashanfoundation.org/hani/hanirhizobiumresearch.pdf 

Singh A and Sharma S 2003 Effect of microbial inocula on mixed solid waste composting, vermicomposting and plant response. Compost Science & Utilization 11(3): 190-199. 

Stamford N P, Santos P R, Santos C E S, Freitas A D S, Dias S H L, and Lira Jr M A 2007 Agronomic  effectiveness  of  bio-fertilizer s  with phosphate rock, sulphur and Acidithiobacillus for yam bean grown on a Brazilian tableland acidic soil. Bioresource Technology 98(6):1311-1318. 

Suthar S 2005 Vermicomposting of kitchen waste by using Eisenia foetida (Savigny). Asian Journal of Microbiology Biotechnology and Environmental Sciences 7(3): 541-544. 

Thenmozhi R, Rejina K, Madhusudhanan K and Nagasathya J 2010 Study on effectiveness of various bio-fertilizers on the growth & biomass production of selected vegetables. Research Journal of Agriculture and Biological Sciences 6(3): 296-301. Available online at http://www.aensionline.com/rjabs/rjabs/2010/296-301.pdf        

Tognetti C et al 2005 Composting vs. vermicomposting: A comparison of end product quality. Compost Science & Utilization 3(1): 6-13. 

Tognetti C, Laos F, Mazzarino M J and Hernández M T 2005 Composting vs. vermicomposting: A comparison of end product quality. Compost Science & Utilization 3(1): 6-13. 

Valencia E y Peña J 2001 El suelo y sus habitantes microbianos: consideraciones ecológicas. Avance y perspectiva 20: 401-406. Available online at http://www.mundoverde.com.ec/pages/MIcroorganismosSuelo.pdf 

Vanegas R 2003 La transición: la búsqueda del cambio hacia sistemas sustentables de producción agropecuaria. Foro Agrario «Sistemas Agrícolas Sustentables». Quito: Universidad Central del Ecuador. p. 18-19. 

Welbaum G, Sturz A, Dong Z and Nowak J 2004 Managing soil microorganisms to improve productivity of Agro-ecosystems. Critical Reviews in Plant Sciences 23(2): 175-193. 


Received 26 December 2011; Accepted 25 February 2012; Published 4 March 2012

Go to top