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Biocontrol Agents of Phytonematodes

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Highlighting the use of biocontrol agents as an alternative to chemical pesticides in the management of plant parasitic nematodes, this book reviews the current progress and developments in the field. Tactful and successful exploitation of each biocontrol agent, i.e. nematophagous fungi, parasitic bacteria, predaceous mites, rhizobacteria, mycorrhiza and predaceous nematodes, has been described separately. The contributors are 23 eminent nematologists and their information has been compiled in 19 chapters.

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19 Chapters

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1: Impact of Phytonematodes on Agriculture Economy



Impact of Phytonematodes on

Agriculture Economy

Mahfouz M.M. Abd-Elgawad1* and Tarique Hassan Askary2

Phytopathology Department, National Research Centre, Giza, Egypt;


Division of Entomology, Sher-e-Kashmir University of Agricultural Sciences and Technology, Srinagar, Jammu and Kashmir, India


1.1  Introduction

­ roduction potential in the agricultural sector. p

Moreover, individuals and groups of mankind

It is well known that the 2008 global financial cannot save huge financial resources to continue crisis, considered by many economists to be the policy of securing reasonable development the worst financial crisis since the Great De- for other reasons widely known all over the pression of the 1930s, has played a key role in world – economic losses due to war damage hindering many small and large businesses, effected globally, new diseases which demand and causing a decline in consumer wealth ample costs to overcome, and non-optimal utiland downturn in economic activity creating ization of available resources. All these in one high unemployment, unfavourable condi- way or another minimize such resources which tions for new businesses, increase in prices of could be directed to fill in the gap of agriculgoods and services and low income per cap- tural produce. In addition, a continuous challenge ita. In this context, agriculture, as a far-reaching is to face an ever-increasing world population activity in terms of both economy and soci- with more and better food. Now, experts at ology throughout world civilization in the almost all levels in developing and more dehistory of mankind, has been adversely affected. veloped countries recognize the seriousness


2: Significance of Biocontrol Agents of Phytonematodes



Significance of Biocontrol Agents of Phytonematodes

Christian Joseph R. Cumagun1* and Mohammad Reza Moosavi2


Crop Protection Cluster, College of Agriculture, University of the

Philippines Los Banos, Philippines; 2Department of Plant Pathology,

Marvdasht Branch, Islamic Azad University, Marvdasht, Iran

2.1  Introduction

Plant parasitic nematodes (PPNs) pose a major constraint on world agriculture resulting in significant yield losses especially in the developing countries where suitable and effective control measures are unavailable (Webster, 1987;

Nicol et al., 2011). It is estimated that PPNs impose 8.8% and 14.6% annual losses to developed and developing countries, respectively

(Nicol et al., 2011), which are more or less equal to US$157 billion (Abad et al., 2008; Escudero and Lopez-Llorca, 2012), however the exact loss estimation of PPNs is too difficult (Schomaker and Been, 2006). Their microscopic size, underground existence and non-specific symptoms make their presence often undetec­ted; therefore, the diagnosis of nematode problems are frequently confused with nutritional deficiencies or other soil factors (Perry and Moens, 2011).


3: Nematophagous Fungi as Biocontrol Agents of Phytonematodes



Nematophagous Fungi as Biocontrol

Agents of Phytonematodes

Tarique Hassan Askary*

Division of Entomology, Sher-e-Kashmir University of Agricultural

Sciences and Technology, Srinagar, Jammu and Kashmir, India

3.1  Introduction

Plant parasitic nematodes are recognized a serious threat to crop production throughout the world. They cause significant damage to field crops (Luc et al., 2005), fruit and horticultural trees (Askary et al., 2000; Askary and

Haider, 2010). All crop plants are susceptible to at least one nematode species and it is considered that the damage potential of nematodes exists in all climates on any crop (Bridge and

Starr, 2007). Globally, agricultural losses due to plant parasitic nematodes have been estimated at US$358 billion annually (see Abd-Elgawad and Askary, Chapter 1, this volume). Plants infected with nematodes are often overlooked and mis-­diagnosed as the symptoms shown by the plants are not clear and are very much similar to fungal diseases or nutritional disorders. In some cases crop yield suppression occurs prior to the expression of explicit disease symptoms. The extent of damage caused to plants by these tiny creatures varies with the genera and species (Askary et al., 2012).


4: Nematophagous Fungi: Ecology, Diversity and Geographical Distribution



Nematophagous Fungi: Ecology,

Diversity and Geographical Distribution

Mrinal Kanti Dasgupta1* and Matiyar Rahaman Khan2

Visva-Bharati; Palli-Siksha Bhavana (Institute of Agriculture), Department of

Plant Protection, Sriniketan, India; 2Department of Agricultural

Entomology, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, India


4.1  Introduction

An organism lives in a state of dynamic

­equilibrium with the environment. Interactions of an organism with members of its community are intraspecific and interspecific. The ecosystem comprises the biotic community and the non-living environment and is the basic functional unit, as it includes both the organism and the environment, each influencing the properties of the other and both necessary for the survival and maintenance of life. Climate is the primary environmental factor influencing the nature of flora and fauna in a  region. The climatic components are temperature, rainfall and relative humidity. The physical, chemical and biological conditions of soil are secondary to the climate. But they all determine the population, seasonality and determine the survival and population fluctuations of soil micro- and meso-biota in particular.


5: Nematophagous Fungi: Virulence Mechanisms



Nematophagous Fungi: Virulence


Pedro Luiz Martins Soares,1* Rafael Bernal de Carvalho,1

Paulo Roberto Pala Martinelli,1 Vanessa dos Santos Paes,1

Arlete Jose da Silveira,2 Jaime Maia dos Santos,1

Bruno Flavio Figueiredo Barbosa1 and Rivanildo Junior Ferreira1


Department of Plant Protection, UNESP, Jaboticabal,

São Paulo, Brazil; 2Department of Agrarian and Environmental Sciences,

State University of Santa Cruz, Ilheus-Bahia, Brazil

5.1  Introduction

may transform a conducive soil from suppressive soils; and collaborates to the integrated

Plant-parasitic nematodes cause physiological handling of nematode management in sustainchanges and injuries that reduce the absorp- able agriculture (Soares, 2006). tion and transportation of water and nutriBiological control aims to reduce the nema­ ents to the plant, affecting their development, tode population or their capacity to feed on or productivity and even product quality. They cause damage to plants through the action of cause an estimated loss of US$358 billion one or more living organism that occur naturally annually on a worldwide basis (see Abd-­ in the soil, or through the manipulation of the


6: Nematophagous Fungi: Formulation, Mass Production and Application Technology



Nematophagous Fungi: Formulation,

Mass Production and Application


Paulo Roberto Pala Martinelli,1* Pedro Luiz Martins Soares,1

Jaime Maia dos Santos1 and Arlete Jose da Silveira2


Department of Plant Protection, UNESP Jaboticabal, São Paulo, Brazil;


Department of Agrarian and Environmental Sciences, State University of Santa Cruz, Ilheus-Bahia, Brazil

6.1  Introduction

A successful plant-parasitic nematode (PPN) management requires a combination of management tactics, such as exclusion measures, crop rotation, use of antagonistic plants, resistant varieties and chemical and biological methods. Among these, the biological method of nematode management by using nematophagous fungi has drawn considerable attention by researchers all over the world (Barron,

1977; Fattah, 1988; Maia et al., 2001; Bernardo,

2002; Corbani, 2002; Martinelli et al., 2012a,b).

These carnivorous fungi are the most studied organisms for the management of nematodes.

The first report of fungi parasitizing nematodes was reported by Zopf (1888), and the first attempt of using these microorganisms in nematode control was taken by Cobb in


7: Nematophagous Fungi: Commercialization



Nematophagous Fungi:


Mohammad Reza Moosavi1* and Tarique Hassan Askary2


Department of Plant Pathology, Marvdasht Branch, Islamic

Azad University, Marvdasht, Iran; 2Division of Entomology,

Sher-e-Kashmir University of Agricultural Sciences and

Technology, Srinagar, Jammu and Kashmir, India

7.1  Introduction

It is estimated that about 842 million people, or 12% of the global population, did not have enough food to satisfy their dietary energy requirements in 2011–13. This means that approximately one in eight people in the world are likely to have suffered from chronic starvation (FAO et al., 2013). Plant diseases are considered a significant threat to increasing agricultural productivity since they can cause serious losses and in turn endanger food security (Strange and Scott, 2005). At least 12% of worldwide food production is lost due to plant-parasitic nematodes (PPNs)

(Nicol et al., 2011) and this quantity is too high to be ignored. Therefore, it becomes mandatory to decrease the level of damage caused by PPNs to agricultural and horticultural crops, though it is a daunting task and difficult to achieve. Management of PPNs has been principally based on application of chemical nematicides but there is a need to substitute chemicals with other effective methods. The efficient synthetic nematicides are not affordable by a lot of growers or have generally been taken off the market due to concerns about the environmental hazards and human


8: Nematophagous Fungi: Regulations and Safety




Nematophagous Fungi: Regulations and Safety

Tabo Mubyana-John1* and Joanne Taylor2

Department of Biological Sciences, University of Botswana, Gaborone,

­Botswana; 2Royal Botanic Garden Edinburgh, Edinburgh, UK

8.1  Introduction

Biocontrol of phytonematodes involves the use of biopesticides (also known as biocontrol agents; BCA), which, in the case of nematodes, are mainly their natural fungal predators

(Stirling and Smith, 1998). Historically, phytonematodes were controlled using soil chemical fumigants such as methyl bromide, dazomet,

1,3-dichloropropene, telone, metam sodium and chloropicrin (Bell et al., 1998; Sardanelli and Elision, 2005). However, recently there has been a shift from chemical control to biological methods of controlling nematodes due to several reasons. These include general awareness of the environmental pollution ­aspects associated with chemical control and banning of the use of methyl bromide (Chaves, 2003) and other organochlorides implicated in the depletion of the ozone layer (Sikora, 2002).


9: Nematophagous Bacteria as Biocontrol Agents of Phytonematodes



Nematophagous Bacteria as Biocontrol

Agents of Phytonematodes

Mohamed F.M. Eissa* and Mahfouz M.M. Abd-Elgawad

Phytopathology Department, National Research Centre, Giza, Egypt

9.1  Introduction

Plant-parasitic nematodes (PPN) are a severe constraint to agricultural production worldwide, in turn impacting international trade, social and economic development (Perry and

Maurice, 2013). A great deal of research has been done on phytonematodes and their hosts including many horticultural and field crops in tropical, subtropical (e.g. Luc et al., 2005), temperate (e.g. Evans et al., 1993) and other regions (e.g. Perry and Maurice, 2013). The nematodes can damage their host plants directly, act as vectors of viruses, or form disease complexes with other pathogens. In addition, nematode penetration of infected plants may facilitate subsequent infestation by ­secondary pathogens such as fungi and bacteria (Powell, 1971). Yet, due to their often subterranean habit and microscopic size, phyto­nematodes usually remain invisible to the naked eye (Ngangbam and Devi, 2012), which complicates their control. Monetary estimates of global annual yield losses caused by the nematodes demonstrated staggering figures whether in the past (e.g. Sasser and


10: Nematophagous Bacteria: Virulence Mechanisms



Nematophagous Bacteria: Virulence


Fernando da Silva Rocha1* and Jorge Teodoro de Souza2

Laboratory of Phytopathology, Federal University of Minas Gerais,

Montes Claros, Brazil; 2Department of Phytopathology, Lavras Federal

University, Lavras, Minas Gerais, Brazil


10.1  Introduction

Bacteria may affect nematode populations by a series of direct mechanisms, including para­ sitism and antibiosis and indirectly by inter­ fering with the recognition of host plants, inducing systemic resistance and improving plant health (Tian et al., 2007). Bacteria may be classified as antagonists, parasites and sym­ bionts, according to their ecological associ­ ation with nematodes. Antagonistic bacteria are saprophytes that may use nematodes as a source of nutrients under certain conditions, but are not dependent on them for survival.

These bacteria kill nematodes through the production of toxins, enzymes, volatile com­ pounds and antibiotics. On the other hand, obligate parasitic bacteria and symbionts depend on the nematode host for survival and have evolved a biotrophic lifestyle with little or no production of enzymes and toxic compounds.


11 Nematophagous Bacteria: Survival Biology



Nematophagous Bacteria:

Survival Biology

Fabio Ramos Alves1* and Ricardo Moreira de Souza2

Department of Vegetable Production, Federal University of Espirito Santo,

Alegre, Brazil; 2Laboratory of Entomology and Phytopathology,

Centre for Agricultural Sciences and Technology, State University of

North Fluminense Darcy Ribeiro, Rio de Janeiro, Brazil


11.1  Introduction

Plant-parasitic nematodes play an important role among the pathogens that cause serious damage directly to the plants and indirectly to the growers. Their destructive action on the root system or aerial part affects the absorption and translocation of nutrients to the plant, altering its physiology and predisposing it to other complex diseases and environmental stresses (Paula et al., 2011). The great majority of plant-parasitic nematodes pass at least part of their life cycle in the soil, and their activity is influenced by the variation of physical (temperature, humidity and aeration), chemical (defensives and fertilizers) and physiological (Alves and Campos, 2003; Ferraz et al.,


12: Nematophagous Bacteria: Field Application and Commercialization



Nematophagous Bacteria: Field

Application and Commercialization


Mahfouz M.M. Abd-Elgawad1* and Ioannis K. Vagelas2

Phytopathology Department, National Research Centre, Giza, Egypt;


Technological Education Institute of Larissa, Department of Plant

Production, Larissa, Greece

12.1  Introduction

In our world there is an uncountable variety of nematodes, which are usually classified into feeding types according to their main sources of nutrition. Kimpinski and Sturz (2003) considered them as the most numerous multicellular animals on earth. Among their major groups are plant-parasitic nematodes (PPNs), which can cause considerable losses to a wide variety of economically important crops (see

Abd-Elgawad and Askary, Chapter 1, this volume). Chemical control is a widely used option for PPN management. However, chemical nematicides are now being reappraised with a clear aim at the avoidance of their hazards to  human beings. It is widely known that many such chemicals demonstrated environmental hazards, high costs, limited availability in numerous countries, or their reduced effectiveness following repeated applications.


13: Novel Bacteria Species in Nematode Biocontrol



Novel Bacteria Species in Nematode


Ioannis K. Vagelas*

Technological Education Institute of Larissa,

Department of Plant Production, Larissa, Greece

13.1  Introduction

Plant parasitic nematodes (PPN), especially the root-knot nematodes (RKN), are considered a limiting factor in crop production, causing considerable annual losses among a wide variety of crops grown in the world

(Sasser and Freckman, 1987). Among the different PPNs, Meloidogyne spp. are of much significance. Multiple invasions of plant roots by Meloidogyne spp. cause poor development of root system, interfering primarily with water and nutrient absorption. It is clear that

Meloidogyne spp. can reduce yields substantially, particularly where susceptible crops are grown intensively without fallow periods

(Sasser, 1980; Sasser and Freckman, 1987).

Among the different methods used to control PPNs, the main three are: (i) the cultural method (e.g. fallow, crop rotation, sanitation, manuring, water management, trap and resistant crops); (ii) the chemical method (soil fumigants and non-fumigants); and (iii) the biological method. The cultural method, which implies crop rotation with non-host plants, can be an effective method to reduce nematode population densities but non-host crops


14: Mites as Biocontrol Agents of Phytonematodes



Mites as Biocontrol Agents of


Uri Gerson*

Department of Entomology, The Robert H. Smith Faculty of Agriculture,

Food and Environment, Rehovot, Israel

14.1  Introduction

Reductions in the extent of nematode damage to plants, which may occur without human intervention, are usually attributed to certain biota that decrease nematode numbers in what are termed suppressive soils. These have been reported from all over the world and include some of the best documented cases of natural, effective biological control of nematodes (Kerry,

1997; Sánchez-Moreno and Ferris, 2007). The biological control (BC) of plant nematodes

(phytonematodes) has been defined (Sayre and

Walter, 1991; Stirling, 1991) as reductions in nematode populations and/or their damage through the activities of organisms other than nematode-resistant host plants. Stirling (2011) later proposed a broader, more ecologicallyminded definition, that BC is the action of soil organisms in maintaining nematode population densities at lower average levels than would occur in their absence. Biological control is usually understood to be a scientific as well as a practical approach (and a management tool) in reducing pest numbers and/or their economic, medical and/or veterinary damage, through the activities of other organisms. When it is applied to arthropod pests, BC consists of three strategies, or modes, namely introductions


15: Plant Growth-promoting Rhizobacteria as Biocontrol Agents of Phytonematodes



Plant Growth-promoting

Rhizobacteria as Biocontrol

Agents of Phytonematodes

Abdul Hamid Wani*

Department of Botany, University of Kashmir,

Jammu and Kashmir, India

15.1  Introduction

Plant-parasitic nematodes (PPN) or phytonematodes are invertebrate obligate parasite of a large number of plants. There are about 197 genera containing 4300 species of phytonematodes. The important genera of PPN include: Meloidogyne, root-knot nematodes; Pratylenchus, lesion nematode; Heterodera and Globodera, cyst nematodes;

Tylenchulus, citrus nematode; Xiphinema, dagger nematode; Radopholus, burrowing nematode;

­Rotylenchulus, reniform nematode; Helicotylenchus, spiral nematode; and Belonolaimus, sting nematode. Root-knot nematodes, Meloidogyne spp. have been found all over the world and are known to cause huge losses to crops of economic importance (Taylor and Sasser, 1978). About

90 species of root-knot nematode have been reported, but four of them, Meloidogyne incognita,

Meloidogyne hapla, Meloidogyne arenaria and


16: Arbuscular Mycorrhizal Fungi as Biocontrol Agents of Phytonematodes



Arbuscular Mycorrhizal Fungi as

Biocontrol Agents of Phytonematodes

Chellappa Sankaranarayanan*

Division of Crop Protection, Sugarcane Breeding Institute,

Coimbatore, India

16.1  Introduction

endomycorrhiza or arbuscular mycorrhiza, ericoid mycorrhiza, arbutoid mycorrhiza, monoThe symbiotic associations between the plant tropoid mycorrhiza, ect-endomycorrhiza, and roots and fungi are referred to as ‘Mycorrhizae’. orchidaceous mycorrhiza.

The term mycorrhiza from the Greek (mykes =

Arbuscular mycorrhizal fungi (AMF), mushroom or fungus and rhiza = root) can also previously known as vesicular-arbuscular mycorbe defined as ‘a mutualistic symbiosis between rhizae (VAM), are mutualistic symbiotic associplant and fungus, localized in a root or root-like ations between the roots of most vascular plants structure in which energy moves primarily and a small group of fungi belonging to the from plant to fungus and inorganic resources new phylum Glomeromycota (Schussler et al., move from fungus to plant’. These symbiotic 2001). AMF are characterized by the presence relationships are characterized by two-way of intercellular or intracellular hyphae, arbusmovements of essential nutrients such as move- cules which are branched hyphae involved ment of carbon from plant to the fungus and in nutrient exchange (Fig. 16.1), extra-radicle movement of inorganic nutrients from fungus mycelium that connect the root to the soil, to plant, which are critical symbiotical link- and spores that are formed in the extra-radicle ages between the soil, root and plant. Mycor- mycelium. Some fungal species also form rhizal fungi in infertile soil help in uptake of intra-radicle structures referred to as vesicles nutrients, which results in improvement of plant (enlarged portions of hyphae that are filled with growth. Mycorrhizal plants are always com- lipid bodies) (Fig. 16.2). Taxonomically, AMF petitive and are able to withstand unfavourable belong to the phylum Glomeromycota, class environmental conditions compared to non-­ Glomeromycetes, orders Archaeosporales, Parmycorrhizal plants. The vast majority of land aglomerales, Diversisporales and Glomerales. plants form symbiotic associations with fungi and Eight genera of AMF have been recognized, an estimated 95% of all plant species belong to mainly on the basis of morphological characdiverse genera that characteristically form mycor- ters of asexual spores (Schussler et al., 2001). rhizae. On the basis of morphology and anatomy, These are Glomus, Paraglomus, Sclerocystis, only seven types of mycorrhizae have come into Scutellospora, Gigaspora, Acaulospora, Archaeospora general use so far. These are: ectomycorrhiza, and Entrophospora, including ­approximately


17: Predatory Nematodes as Biocontrol Agents of Phytonematodes



Predatory Nematodes as Biocontrol

Agents of Phytonematodes

Young Ho Kim*

Department of Agricultural Biotechnology and Research Institute of

Agriculture and Life Sciences, Seoul National University, Korea

17.1  Introduction

Nematodes are multicellular triploblastic

­invertebrates with a pseudocoel that belong to the phylum Nematoda of the kingdom

­Animalia. They are ubiquitous in nature, inhabiting a very broad range of environments largely as marine or terrestrial inhabitants.

Among their terrestrial forms, soil nematodes are very small (generally 0.3–0.5 mm long as adults) wormlike animals with a high diversity

(commonly >30 taxa) predominating over all other soil animals in species as well as in number (commonly millions per square metre;

Yeates, 1979; Bernard, 1992).

Soil nematodes feed on soil organisms

­belonging to a broad range of groups. Based on feeding behaviour, they can be classified into different trophic groups, such as bacterial feeders, fungal feeders, algal feeders, animal predators, omnivores and plant parasites (Freckman and Caswell, 1985; Yeates and Bongers, 1999).


18: Factors Affecting Commercial Success of Biocontrol Agents of Phytonematodes



Factors Affecting Commercial

Success of Biocontrol Agents of



Mohammad Reza Moosavi1* and Rasoul Zare2

Department of Plant Pathology, Marvdasht Branch, Islamic Azad University,

Marvdasht, Iran; 2Department of Botany, Iranian Research Institute of Plant

Protection, Tehran, Iran

18.1  Introduction

Phytonematodes represent a global threat to agricultural production either as causing yield loss or quality loss, both included in the concept of crop loss. To date, approximately

4100 species of phytonematodes have been described that can cause various plant diseases (Decraemer and Hunt, 2006). They are of considerable importance and their deleterious impacts on crops have great economic and social effects. Total annual losses caused by phytonematodes in developing and developed countries are estimated to be about

14.6 and 8.8%, respectively (Nicol et  al.,

2011), that is approximately equal to US$157 billion (Abad et al., 2008; Escudero and

Lopez-Llorca, 2012).

Management of phytonematodes is


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