Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management

*Sunil Kumar, Ranjit Kumar and Pankaj Sood*

## **Abstract**

Earthworm causes increase in availability of soil organic matter through degradation of dead matters by microbes, leaf litter and porocity of soil. Vermicompost is a non-thermophilic biodegradation process of waste organic material through the action of microorganism with earthworm. Vermicompost is rich in many nutrients including calcium, nitrates, phosphorus and soluble potassium, which are essentially required for plant growth. Different plant growth hormones like gibberellins, auxins and cytokinins are present in vermicompost, which has microbial origin. Nematodes are mostly small, colorless and microscopic organisms which remain under soil, fresh or marine water, plants or animals, and act as parasite in different conditions, while very few have direct effect on human. The nematodes which are parasitic on plants use plant tissues as their food. They have well developed spearing device, like a hypodermic needle called stylet. It is used to penetrate host cell membrane. Management of plant-parasitic-nematodes therefore is necessary and several means are adopted. Of which, use of bio-chemicals and organic compost have shown encouraging results and proved to be potential in suppressing the nematode population. Vermicompost plays an important role of soil fortification on growth characteristics, such as length, weight, root, shoot branches, number of leaves and metabolism of host plant against nematode infection. Vermicompost fortified plants showed increment in sugar, protein and lipid over untreated control. Increment of these metabolites helps treated plants to metabolically cope up the infection and promotes excessive plant growth. The vermicompost caused the mortality of nematodes by the release of nematicidal substances such as hydrogen sulfate, ammonia, and nitrite apart from promotion of the growth of nematode predatory fungi that attack their cysts. It favours rhizobacteria which produce toxic enzymes and toxins; or indirectly favors population of nematophagous microorganisms, bacteria, and fungi, which serve as food for predatory or omnivorous nematodes, or arthropods such as mites, which are selectively opposed to plant-parasitic nematodes.

**Keywords:** Vermicompost, nematode, nematophagous, *Meloidogynae*

## **1. Introduction**

The term vermicompost is derived from a latin word "vermes" meaning "worms" and the process of composting of organic material using earthworms is known as vermicomposting. Earthworms directly influences the microbial

community of soil and it maintains normal chemical and physical properties ofsoil, due to which it is popularly called the "farmer's friend".

Earthworm causes increase in availability of soil organic matter through degradation of dead matters by microbes, leaf litter and porocity of soil. Vermicompost is a non-thermophilic biodegradation process of waste organic material through the action of microorganism with earthworm. The product produced through vermicompost is highly fertile, very finesoilparticles with marked porosity, adequate aeration, low C: N ratios and high water-holding capacity [1]. The termed "drilosphere" is coined for microflora and microfaunain soil influenced by earthworms [2].

Due to decrease in land availability for cultivation, waste disposal and exponential increase in human population there is urgent need to improve crop production and waste disposal mechanism. Crop intensification has led to huge use of chemical fertilizers and pesticides which plays key role in ecological disturbances by destroying natural predators of crop pests, plant growth-promoting bacteria and other soil micro/macro flora and fauna. These pesticides pollute environment very adversely, necessitating demand for safe organic farming to protect us from adverse effect of these pollutants. Organic waste composting is a technique which converts organic wastes into useful composts, which could be used as biofertilizer for sustainable agriculture growth. Conventional composting through microbes is a thermophilic process, in which many microbes are lost due to excess temperature emitted during the composting process. While vermicomposting is a mesophilic process, which conserves all microbes and earthworm associated with it to provide associated beneficial effect for degradation of organic matter by preserving the diverse community of all beneficial microflora. Vermicompost provides more biologically active and nutritive biofertilizers in soil as earthworms transform different organic waste material into useful vermicompost material by grinding, churning and digesting these substancesin association with microbes which is essential in biogeochemical processes [3]. Earthworms enhance the beneficial microbes and suppresses harmfulmicrobes to convert different infectious hospital wastes into risk-free materials [4].

Vermicomposts are rich in many nutrients including calcium, nitrates, phosphorus and soluble potassium, which are essentially required for plant growth [5]. Different plant growth hormoneslike gibberellins, auxinsand cytokinins are also present in vermicompost, which has microbial origin.

Nematodes are mostly small, colorless and microscopic organism remain under soil, fresh or marine water, plants or animals They act as parasite in different conditions, while very few has direct effect on human. Almost 50 percent nematodes are living in marine environment while about 25 percent of the nematode species live in soil and fresh water feeding on different decomposer organism including bacteria and fungi, many small invertebrates and organic waste Only 15 percent of the nematode species are parasitic in nature, infecting animals, ranging from small insects, many invertebrates and man. Only almost 10 percent nematode species are plant parasite in nature.

The nematodes which are parasitic on plant use plant tissues as their food through well developed spearing device like a hypodermic needle called style used to penetrate host cell membrane. Plant-parasitic nematodes release an enzyme into a host plant cell through stylet for partial digestion of cell content before entry into gut. Nematode causes injury to plants in two ways involving their feeding mechanism. Few nematodes are ectoparasitic which utilizes different plant tissues outside the plant for their food, while few nematodes are endoparasitic which utilize inner part of plant tissues as their food. Few nematodes are migratory known as foliar nematodes which utilizes the leaves and buds of ferns, chrysanthemums, strawberries and many other ornamentals as their food. Foliar nematodes cause death of buds, distortion of leaf and formation of dark-brown to yellow lesions between major veins of the leaves.

*Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

Management of plant-parasitic nematodes therefore is necessary and several means are adopted. Of which use of bio-chemicals have shown encouraging results and proved to be potential in suppressing the nematode population. Vermicompost plays an important role of soil fortification on growth characteristics, such as length, weight, root, shoot branches, number of leaves and metabolism of host plant against nematode infection. Vermicompost fortified plants showed increment in sugar, protein and lipid over untreated control. Increment of these metabolites treated plants and metabolically cope up the infection and promote excessive plant growth. Use of Vermicompost as fertilizer also helps in suppression of plant diseases and pest as it provides better nutrient availability and greater strength, immunity, and resistance against infection. Compost and vermicompost are effective in eliminating root-knot nematodes (*Meloidogyne incognita*) in tomato plants. Almost 40 species of bacteria and 22 species of fungi were identified in soil treated with vermicompost, of 40 bacterial species majority were found under the genus like *Azotobacter*, *Bacillus*, *Rhizobium*, *Pseudomonas*, *Beigerinicka* and *Enterobactor* and in fungal the genus such as *Aspergillus*, *Rhizopus*, *Pencillum*, *MucorCladosporium*, and *Fusarium* were commonly found [6]. Arancon et al. [7] had also observed a reduction in plant-parasitic nematodes following the application of vermicompost.

## **2. Vermicompost**

#### **2.1 Nutritional composition**

The nutrient content obtained from vermicompost directly depends on the constituent of waste material where it feeds. It enhances levels of different material in casted soil than available mineral concentration due to microbial activity in its gut [8]. According to reports of Hand *et al*. [9] the earthworms enhance nitrogen mineralization in the soil, consequently resulting in more availability of nitrate in the soil. The vermicompost is also involved in reduction of organic carbon and carbon nitrogen ratio than in the normal composts. The combined earthworm and microorganism action lowered causes loss of different organic matter from the soil substrates as CO2 introduces 20–43% of total organic carbon material in soil the completion of vermicomposting period. Vermicompost also contains all essential nutrients including nitrates, phosphate, exchangeable calcium and soluble potassium which are quickly absorbed by plants (Edwards, 1998; [10]). Also observed more micro and macro nutrients in the vermicompost which are rich in the earthworm casts.

#### *2.1.1 C/N ratio*

The carbon and nitrogen (C/N) ratio is most important parameter during composting process which clearly indicates about the decomposition rate. Plants are able to take mineral nitrogen in the form of nitrates, only when carbon and nitrogen ratio falls below 20 [11]. The proper ratio of carbon and nitrogen is therefore required for the proper plant growth. Earthworms cause reduction in carbon level thereby increasing the nitrogen content in fresh organic matter.

#### *2.1.2 Nitrogen*

Nitrogen is very essential constituent of all amino acids and protein. Deficiency of nitrogen directly decreases the growth of plants leading to chlorosis, stunted and slow growth. According to Hand *et al*. [9] mineralization with nitrogen was highly facilitated in earthworm presence and it leads to deposition of nitrate in the soil.

## *2.1.3 Phosphorus*

Earthworms activity causes increase in total phosphorus concentration in soil in comparison to the food source available in soil. This clearly indicates that the vermicomposting causes increase in phosphorus level through the mineralization of phosphoric organic compounds [12, 13].

### *2.1.4 Iron (Fe)*

Iron (Fe) is also an important element required for growth and productivity of all plants. Only very trace amount of iron is required in comparison to other minerals by plant like carbon, oxygen, hydrogen, nitrogen, phosphorus, sulphur and potassium for proper plant growth. The iron functions like a cofactor, as it has a catalytic site for many essential enzymes activity which are even required for chlorophyll synthesis.

#### *2.1.5 Magnesium (Mg)*

It is a important component used in formation of chlorophyll, which play vital role in photosynthesis. It is also required for carbohydrate metabolism and acts as enzyme activator in nucleic acid synthesis. Magnesium serves as a carrier of phosphate compound in plants and also supports uptake of many essential elements into plant. It enhances production of oils and fats through the translocation of carbohydrates.

#### *2.1.6 Manganese (Mn)*

Manganese (Mn) plays vital role in nitrogen assimilation by, as enzyme activator. It is very important constituent of chlorophyll. Low plant manganese usually causes leaves to turn yellow due to reduced chlorophyll content. Organic soils usually contain intermediate amounts of manganese.

#### *2.1.7 Zinc (Zn)*

Low presence of zinc leads to high yield of crops. Zinc efficiency has been reported in many enzymatic activities of plants [14]. Zinc utilization mechanism in plant tissue is most important mechanism of zinc in plant tissues. Heavy metal bioaccumulation study showed that increased duration of vermicompost concentration of Zn and Cu decreases soil [15].

#### **2.2 Role of vermicompost in plant growth promotion**

Wide variety of plant species grows effectively in vermicompost rich soil, including many horticultural crops like tomato, cauliflower etc. [16], aubergine [17], garlic, pepper [18], strawberry, green gram and sweet corn [19]. Vermicompost is also very much effective on enhance production of many medicinal plants rich in aromatic compounds [20], cereals such as rice and sorghum [21], fruit crops such as papaya and banana, and ornamentals like geranium [22], petunia, marigolds and poinsettia. Effect of vermicompost was also observed in forest trees including eucalyptus, acacia and pine tree [23]. Vermicompost are very beneficial and used

#### *Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

as a partial or total substitute for chemical fertilizer in agriculture and artificial greenhouse potting media. Likewise, few studies show that water-extracts obtained from vermicompost, vermiwash were used as foliar sprays, which enhances growth of tomato plants [24], strawberries and sorghum. Vermicompost also stimulates seed germination in green gram and other plant species [25], tomato plants [26], pine trees and petunia. Vermicompost are used effectively for vegetative growth of leaf, stimulating growth of root and shoot [27]. These effects cause increase in root branching and leaf area and alterations in morphology of seedling plant [28]. Vermicompost stimulates flowering in plants, increasing flowers produced [29], and increase in fruit yield [30].

## **2.3 Bacterial diversity associated with earthworms**

A variety of bacterial species have been reported associated with earthworms/ vermicompost though the bacterial species varied with its isolation site including soil, intestine, and excrements. Almost 43 bacterial species were isolated from earthworm intestines and 25 obtained from fresh excrements of which, 9 were common. Among 40 bacteria species isolated from soil and intestine, 13 were shared species; 9 were gram-positive, and 6 Bacillus species were sporeforming. Comparison of soil and excrements bacteria revealed similarity of only 6 isolated species, of which three species were gram-positive and three species were gram-negative. *Brevundimonas diminuta* (α-Proteobacteria), *Kocuria palustris* (Actinobacteria) and D. acidovorans (β-Proteobacteria), were isolated from all three substrates. Comparison of bacteria isolated from the intestine of *Aporrectodea caliginosa*, *Lumbricus terrestris*, and *Eisenia fetida* earthwormsrevealed that the highest number of 43 bacterial taxa was isolated from *A. caliginosa* digestive tract; while from *L. terrestris* and *E. fetida*, 22 and 21 taxa were isolated respectively. Few members of bacteria were isolated from all earthworm species, which includes Bacteroidetes (classes Flavobacteria and Sphingobacteria), Actinobacteria, Proteobacteria (classes α-, β-, γ-) and Firmicutes (class Bacilli). Five bacterial species isolated from earthworm exhibited relatively low similarity between the sequenced 16S rRNA gene fragments (approx. 1490 nucleotides) and the genes of known bacterial taxa (93–97%), which includes Ochrobactrum sp. 341-2 (αProteobacteria), *Sphingobacterium* sp. 611-2 (Bacteroidetes), *Massilia* sp. 557-1 (β-Proteobacteria), *Leifsonia* sp. 555-1, and a Microbacteriaceae, isolate 521-1 (Actinobacteria).

Micromycetes were observed in digestive tracts of fasted earthworm species. The incubation temperature had no effect on the number of fungal CFU isolated from the intestines. Fungi isolated from the earthworms after 20 days of starvation, are *Bjerkandera adusta* and *Syspastospora parasitica* identified by light-colored sterile mycelia, as well as *Geotrichum candidum*, *Alternaria alternata*, *Acremonium murorum* (*A. murorum* var. *felina*), *A. versicolor*, *Aspergillus candidus*, *Rhizomucor racemosus*, *Mucor hiemalis*, *Cladosporium cladosporioides*, Fusarium (F*. oxysporum, Fusarium* sp.), and *Penicillium* spp.. The density of fungal colony in the air dry intestine was 103–104 CFU; this value is very close to the fungal populations density in soil mineral horizons. These fungi are most resistant to the conditions within earthworm digestive tract.

#### **2.4 Role of vermicompost in nematode control**

The application of vermicompost resulting in reduction of free-living nematodes populations owing to, its adverse effects on these nematodes. The management of plant-parasitic nematodes is very difficult in comparison to management of other insect pests and pathogens. The plant-parasitic nematode generally resides in soil and attacks the underground parts of plants. While cyst nematode management faces a unique challenge owing to hard protecting cyst wall protects egg of gravid females. Prevention is the most common economical control method, because once any plant is parasitized by nematode, it is essential to destroy host for killing worm effectively. At present chemical nematicide is commonly used in controlling different types of plant-parasitic nematodes in the soil [31]. Frequent treatment of soil with different chemical is dangerous and adversely affects soil organisms, environment, as well as animal and human health. Gabour *et al*. [32] observed inhibitory effect of vermicompost application on the populations of the plant-parasitic nematode *Rotylenchulus reniformis*. In addition to vermicompost, recent studies have shown that the application of vermicompost tea has the potential to control plant-parasitic nematodes. In this sense, Edwards et al. [33] studied a significant suppression in the number of galls caused by *Meloidogyne hapla* in tomato when the plants were subjected to aerated vermicompost tea. The effects of vermicompost are likely on nematodes due to the mortality of nematodes by the release of nematicidal substances such as hydrogen sulfate, ammonia, and nitrite produced [34]. promotion of the growth of nematode predatory fungi that attack their cysts [35]; favoring of rhizobacteria that produce toxic enzymes and toxins [36]; or indirectly by favoring populations of nematophagous microorganisms, bacteria, and fungi, which serve as food for predatory or omnivorous nematodes, or arthropods such as mites, which are selectively opposed to plant-parasitic nematodes [37].

## **3. Mechanisms that mediate nematode control**

## **3.1 Crop rotation**

It reduces many soil-borne diseases and improves soil for agriculture. Many nematodes can reproduce, grow and survive on selected plants and not able to grow on other crops and hence die with practice of crop rotation. Repeatedly growing of single crop in particular field will enable any organism to reproduce successfully and increase their number. While introduction of crops which does not support nematode growth will prevent reproduction and growth of nematode and allow natural mortality factors to act on these to reduce their numbers. Through the planned rotation of crop and sequential alteration of crop, it is possible to reduce excessive growth of all pests of all of the major agriculture crops. Hairy indigo would reduce numbers of sting and rootknot nematodes and can be planted as a summer crop in between other crops. Pangola digitgrass a common agriculture crop of West Indies and Florida, which control burrowing and root-knot nematodes in vegetable lands. Use of crop rotation usually provides multiple benefits including mineralization of soil as well as effective pest control in agriculture field.

## **3.2 Crop root destruction**

Through destruction of root whole pest colony which resides on root are destroyed, and leads to decline in number of nematodes through increased mortality. This can stop nematode reproduction and should encourage their decline through normal mortality. Crop root systems are reservoir for many soil-borne diseases and nematodes. These small insects and nematodes can multiply on root system of crop whenever it will remain alive. Almost 10 folds increase in nematode concentration were observed when soil temperature were high. Even when soil temperatures are

*Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

declining, at least one additional generation of nematode were found. It was very good practice in nematode management to destroy root of previous crop to prevent growth and reproduction of nematode.

## **3.3 Flooding**

Flooding the agriculture land was also used to reduce numbers of soil infesting pests including plant-parasitic nematode. It is done through regular maintenance of high water level in field for many weeks in controlled manner. This high water level is maintained in field for two or three weeks followed by drying the soil and flooding again for two to three weeks is more effective way of controlling plant-parasitic root nematode. Flooding generally kills root nematodes by inhibition of nematode parasite with interaction to host plants for longer period.

### **3.4 Fallowing**

It is a process in which a field is left without any type of vegetation and plants for longer period; it leads to starvation of nematodes or other pests in absence of vegetation. Most soil pests and nematodes were decreased due to lack of food in the form of host plants. The field must be regularly cultivated to prevent growth of different weeds and it leads to proper cycling of drying and heating to different layers of soil.

### **3.5 Plant resistance**

Many plants are resistant to different types of pests, And their use in agriculture field is most effective and less expensive way of pest control strategy. But this method requires detailed knowledge on various resistant plants and pest categories and situation which does not support pest survival, but most of nematode resistant crop has resistant for only few nematode species and it would not be completely resistant to all species of nematode.

#### **3.6 Biological control**

Many biological agents like bacteria and fungi are nature well known enemies of nematodes. These do not support growth of nematode species when concentration of these bacteria and fungi are high. Many scientific studies on nematode are able to reduce nematode population with the help of these bacteria and fungi under laboratory conditions. But at field levels this is emerging field of research and success rate are not very high. However, the use of organic materials to the soil has been found reported to increase the availability of food for fungivorous and bacteriophage nematodes, increasing the competition between them with other groups.

## **4. Nematode associated with agricultural crops**

Nematode species varies greatly in different countries. Few nematode species are cosmopolitan, likespecies of *Meloidogyne* while many are geographically restricted to particular region e.g. different species of *Heterodera, Globodera,* etc*. Nacobbus*species are highly specific attacking only carrots. Some crops are infected with very few species of nematode pests while others are infected with wide range of nematode species. Crop like rice, maize and sugar cane are infected with variety of plantparasitic nematodes. Common plant-parasitic nematodes associated with different

agricultural crops are: *Meloidogyne, Heterodera, Globodera, Pratylenchus, Radopholus, Rotylenchulus, Tylenchorhynchus, Xiphinema, Longidorus, Paralongidorus, Aphelechoides, Ditylenchus* etc.

## **5. Nematode management through microbial biogents**

Nematode mainly attack underground parts of plant, due to which management of nematode are very difficult in comparison to other plant parasites [38]. At present synthetic nematicides are frequently used for management of plant-parasitic nematodes [39]. Although, nematicides are very efficient and fast acting, but are relatively unaffordable to many small scale farmers.

Application of organic amendments is one of the best practised alternative strategies for the management of plant-parasitic nematodes in the soil [40]. Organic amendments have shown beneficial effect on soil physical conditions, soil nutrients, and soil biological activity, thus improving plant health and reducing colonies of plant-parasitic nematode [41]. Integrated pest management (IPM) uses different strategies for the management of plant-parasitic nematode but the biological control would be the most effective and economical way of nematode management. Different groups of beneficial bacteria have been utilized for the management of plant-parasitic nematode in soil. Various fungi such as *Aspergillus*, *Paecilomyces*, *Trichoderma*, *Verticillium*, *Pochonia*, *Fusarium* and *Penicillium* have been reported to cause juvenile mortality and egg inhibition of nematodes. An increase in nematicidal potential of microorganisms were observed when such bacteria, fungi or other biocontrol agents are integrated with either organic amendments or nematicides for integrated control of nematodes [42, 43].

## **6. Ecological and economical importance of biomanagement**

The nematodes can survive in different environments including aquatic (such as fresh water, estuarine and marine water), terrestrial (as free living in the soil) and parasitic (either endoparasites and ectoparasites of animals and plants). Pokharel, and Larsen [44] and Pokharel., *et al*. [45], reported that soil nematodes are very important in protecting the organic nature of soil, Phytoparasitic nematodes on feed tissue of plants and reduce the growth and productivity of infected plants. Soil nematodes assist colonization of microbial substrates and nutrients mineralization in the soil. Metabolism in nematodes produce important nutrients like nitrogen and vitamins which speed up bacterial growth in the soil. Many nematodes feed on bacteria, fungi and protozoa within soil and acts like predatory or omnivorous nematodes it would improve cycling of nutrients and causes slow release of nutrients into soil. The free-living nematode in soil enhances mineralization of nutrient in soil. These nematode groups also feed different plant pathogen and few soil microbes including plant pathogens such as bacteria and fungi. Free-living nematodes can protect system crop by protecting nature of soil. The nematodes which attack insect pests are useful biological insecticide [46].

According to data of the American Phytopathological Society, nematodes have great economic benefits of both harmful and useful effect, most plant nematodes has a sharp needle-like structure found in mouth part called stylet. They is cause more than 15percent loss of crops per annum world-wide, equal to almost US\$78 billion. Majority of plant feeder nematodes found in the soil, feed on plants and reduce water and nutrient absorbed by the plants root, reducing their drought resistance ability. Some other nematodes transmit disease causing organisms like

#### *Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

viruses to plants while feeding. Large number of nematode species cause decomposition and recycling of nutrient by release of relevant nutrients for the plant growth.

From more than 4000 described plant-parasitic species of nematodes, only some cause economic losses in crops. Some of the major genera of phytoparasitic species of nematodes causing crop losses are *Xiphinema, Rotylenchulus, Pratylenchus, Meloidogyne, Hoplolaimus* and *Heterodera* [47]. The majority of soil nematodes are present in the rhizosphere of plant root area in the soil surrounding the root of plant where microbiological activity is exceptionally high.

## **7. Enrichment of beneficial microorganisms in vermicompost**

#### **7.1 Enrichment of vermicompost with bacteria**

Earthworm's gut microflora has high ability to increase plant nutrient availability. Earthworms highly influence the soil dynamics and chemical processes, by adding its litter and affecting the soil micro-flora activity [8]. Earthworms and microorganisms interaction seem to be very complex. Earthworms excretes plant growth-promoting substances and making soil fertile. Pseudomonas oxalaticus an oxalate-degrading bacterium was isolated from intestine of different species of earthworm and *Streptomyces lipmanii*from actinomycetes group was identified in the gut of *Eisenia lucens*. Scanning electron micrographs showed presence of endogenous microflora in guts of earthworms, *L. terrestris* and *Octolasion cyaneum*. Gut of *E. foetida* contained various anaerobic N2-fixing bacteria such as C*. Beijerinckii, Clostridium butyricum* and *C. paraputrificum*.

#### **7.2 Enrichment of vermicompost with fungi**

A total of 194 fungal entities comprising 117 mitosporic fungi, 45 ascomycetes, 15 zygomycetes, 14 SM morphotypes and three basidiomycete morphotypes were reported from the vermicompost. Mitosporic fungi including the ascomycetes in their anamorphic state are the most dominat. The thermotolerant fungus, Scedosporium state of *Pseudallescheria boydii* also display a significantly high load in vermicompost, However *Penecillium* and *Aspergillus* showed highest load in vermicompost.

## **8. Enrichment of vermicompost and agriculture benefits**

Vermicomposting is biotransforming process, stabilizing waste organic materials into humus by joint activity of microorganism and earthworms. Earthworms excrete casts which are partially digested waste materials, commonly known as castings or vermicast, and are homogeneous in composition of minerals than the source waste material. Vermicompost has very least levels of contaminants, and contains increased amount of minerals, plant hormones, symbiotic microbes and organic acids including fulvic and humic acids. Vermicomposting is a process of compost production by breeding, growing and maintaining earthworms population in soil. The earthworms cause biooxidation of waste by relentless turning, aeration, and fragmentation resulting in formation of homogeneous and stabilized humus in soil, which is useful for plant thus used as manure in agriculture field. Vermicomposting is very effective for maintenance of biodegradable household waste and Municipal Solid Waste at many places. Aerobically incubated extract of compost are now in high demand commercially for agriculture work. As being are rich in carbohydrate

and a protein source. It is known as 'compost teas' which is microbially very rich. The casting by earthworms consists of many nutrient including Nitrogen, Phosphorus, Potassium, Calcium and Magnisium.

### **9. Conservation of microbial biogents**

#### **9.1 Bacteria**

Bacteria are generally found in very diverse habitat including marine water, fresh water, soil and compost piles. Many bacteria are found in gastrointestinal tract of animal system. Few bacteria also reside in oxygen deficient conditions like in flooded soil. While most bacteria required well aerated soil. Many of bacteria grow and reproduce very rapidly in acidic and neutral soil conditions. Bacteria are first decomposer found in soil which initiates process of decomposition of different material in it. Through the process of decomposition bacteria makes different minerals available to plants. Phosphorus is also dissolved by bacteria and plants can utilize this dissolved phosphorus easily for their growth. Nitrogen fixing bacteria fixes nitrogen in soil for plants. Plants require large amount of nitrogen in agriculture soil for proper growth. It is well known fact that nitrogen present in atmosphere is neither consumed by animals nor plants for their nutrition and growth. Few nitrogen fixing bacteria has ability to convert these nitrogen gas into nitrate which is easily absorbed by plants. Plants use this nitrogen compound to form different types ofamino acids and proteins. This process of formation of nitrate compound through free nitrogen is called *nitrogen fixation*. Nitrogen-fixing bacteria generally reside in root nodules of plant to form mutually beneficial symbiotic associations with plants. Rhizobium bacteria reside in root nodule of different leguminous plant and fixes nitrogen present in air effectively while these bacteria uses sugars of plants for their energy source. Bacteria in alfalfa field can fix many hundreds pounds nitrogen per acre per year.

Pea plant fixes very less amount of nitrogen in field, it accounts for only 30 to 50 pounds per acre. Large molecules of lignin were broken down into very smaller in size through actinomycetes. Lignin is a complex and large molecule found in plant tissue, it protect cellulose from decomposition, bacteria acts on it and degrade it in to simpler form during the process of decomposition. Earthworms can also facilitate the dispersion of microorganisms by the excretion of their spores in the coprolites. However, the dispersion of nematophagous fungi by earthworms might be responsible for the reduction of the nematode populations in the substrates. The mechanisms by which vermicomposts and their aqueous extracts suppress plantparasitic nematodes after application to soil, are speculative. Larger predator–prey populations can also contribute to lower densities of plant-parasitic nematodes in vermicompost-treated soils [48]. Vermicomposts can increase the numbers of predatory or omnivorous nematodes or arthropods such as mites that selectively prey on plant-parasitic nematodes [48, 49]. Vermicomposts can promote the growth of nematode-trapping fungi and fungi that attack nematode cysts and may thereby influence the populations of plant-parasitic nematodes [35].

#### **9.2 Fungi**

Fungi are also important constituent of plant microorganism. Many fungi produce a number of antibiotics. Fungi also initiate the decomposition of waste as well as fresh organic residues. They act on surface of material, making it soft and available for other microorganism for initiating the decomposition of organic *Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

material. Decomposition of lignin also require fungal activity followed by bacterial decomposition process.

## **9.3 Algae**

Many algae, like crop plants, make sugars with the use of sunlight and carbon dioxide, which is used for energy need and formation of other complex molecules. Flooded soil and rice paddy field are rich in many species of algae. These algae grow on surface of wet soil and form mutually beneficial relationship with other organism for enhancing nitrification and mineralization process in soil. It also shows formation of lichens in agriculture field.

## **9.4 Protozoa**

Different species of protozoa use a variety of means for increased productivity of soil. Protozoan's feed on bacteria, fungi and other protozoa and waste materials. Protozoa acts like secondary consumers of organic materials. Protozoa consuming nitrogen rich organisms and excreting wastes rich in nitrogen element this is believed to be responsible for mineralizing much of the nitrogen in agricultural soils.

## **Author details**

Sunil Kumar1 \*, Ranjit Kumar1 and Pankaj Sood<sup>2</sup>

1 Department of Animal Science, School of Life Science, Central University of Himachal Pradesh, Dharamshala, H.P., India

2 CSK Himachal Pradesh Krishi Vishvavidyalaya, Palampur, India

\*Address all correspondence to: sunilibes@gmail.com

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **References**

[1] Domínguez, J. & Edwards, C.A. (2010). Relationships between Composting and Vermicomposting: Relative Values of the Products, In: Vermiculture Technology: Earthworms, Organic Waste and Environmental Management, C.A. Edwards; N.Q. Arancon; R.L. Sherman, (Eds.), 1-14, CRC Press, ISBN 9781439809877

[2] Lavelle, P., & Pashanasi, B. (1989). Soil macrofauna and land management in Peruvian Amazonia (Yurimaguas, Loreto). Pedobiologia, 33, 283-291.

[3] Maboeta M S , Rensburg L.V.: Vermicomposting of industrially produced woodchips and sewage sludge utilizing Eisenia fetida, Ecotoxicol Environ Safety; 2003 Oct;56(2):265-270. doi: 10.1016/s0147-6513(02)00101-x.

[4] Mathur, U. B., Verma, L. K., & Srivastava, J. N. (2006). Effects of vermicomposting on microbiological flora of infected biomedical waste. Journal of ISHWM, 5(I), 21-26.

[5] Edwards, C.A. and Burrows, I. (1988) The potential of earthworms composts as plant growth media. In: Edward, C.A. and Neuhauser, E.F. Eds., 'Earthworms in Waste and Environmental Management', SPB Academic Publishing, The Hague, 2132.

[6] Singh and S. Sharma, "Composting of a crop residue through treatment with microorganisms and subsequent vermicomposting," Bioresource Technology, vol. 85, no. 2, pp. 107– 111, 2002.

[7] Arancon NQ, Edwards CA, Lee SS, Yardim E. Management of plantparasitic nematode populations by use of vermicomposts. Proceedings of Brighton Crop Protection Conference Pests and Diseases. 2002;8(B2):705-716

[8] Edwards, C.A. and Bohlen, P.J. (1996) Biology and Ecology of

Earthworms. 3rd Edition, Chapman & Hall, London

[9] Hand, P., Hayes, W.A., Frankland, J.C., Satchell, J.E., 1988. The vermicomposting of cow slurry. Pedobiologia 31, 199±209

[10] Atiyeh, R.M., Lee, S.S., Edwards, C.A., Arancon, N.Q., Metzger, J. (2002) The influence of humic acid derived from earthworm-processed organic waste on plant growth. Bioresource Technology 84, 7-14.

[11] Dash, MC. and B.K. Senapati 1985. Vermitechnology: potentiality of India.i earthworms for Vermicomposting and vermifeed. proc. Soil. Bio. Symp. Hisar, pp.61 - 69.

[12] Hartenstein R (1983) Assimilation by earthworm Eisenia fetida. In: Satchell JE (ed) Earthworm ecology. From Darwin to vermiculture. Chapman and Hall, London, pp. 297-308

[13] Mitchell A, Edwards CA (1997) The production of vermicompost using Eisenia fetida from cattle manure. Soil Biol Biochem 29:3-4

[14] Rengel Z. 2001. Genotypic differences in micronutrient use efficiency in crops. Communications in Soil Science and Plant Analysis 32: 1163-1186

[15] Hobbelen PH, Koolhaas JE, van Gestel CA. Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environ Pollut. 2006;144(2):639-646. doi:10.1016/j.envpol.2006.01.019

[16] Gutiérrez-Miceli, F.A., Santiago-Borraz, J., Montes Molina, J.A., Nafate, C.C., Abdud- Archila, M., Oliva Llaven, M.A., Rincón-Rosales, R. and

*Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

Deendoven L. (2007). Vermicompost as a soil supplement to improve growth, yield and fruit quality of tomato (Lycopersicum esculentum). Bioresource Technology 98, 2781-2786.

[17] Gajalakshmi,S. and Abbasi, S.A. (2004). Neem leaves as a source of fertilizer-cum-pesticide vermicompost. Bioresource Technology 92, 291-296.

[18] Arancon, N.Q., Edwards, C.A., Bierman, P., Metzger, J.D. and Lucht, C. (2005). Effects of vermicomposts produced from cattle manure, food waste and paper waste on the growth and yield of peppers in the field. Pedobiologia, 49, 297-306.

[19] Lazcano, C., Revilla P., Malvar, R.A. and Domínguez, J. (2011). Yield and fruit quality of four sweet corn hybrids (Zea mays) under conventional and integrated fertilization with vermicompost. Journal of the Science of Food and Agriculture.

[20] Prabha, M.L., Jayraay, I.A., Jayraay, R. and Rao, D.S. (2007). Effect of vermicompost on growth parameters of selected vegetable and medicinal plants. Asian Journal of microbiology, Biotechnology and Environmental Sciences, 9(2), 321-326.

[21] Bhattacharjee, G., Chaudhuri, P.S. and Datta, M. (2001). Response of paddy (Var. TRC-87- 251) crop on amendment of the field with different levels of vermicompost. Asian Journal of Microbiology, Biotechnology and Environmental Sciences, 3 (3), 191-196.

[22] Chand, S., Pande, P., Prasad, A., Anwar, M. and Patra, D.D. (2007). Influence of integrated supply of vermicompost and zinc-enriched compost with two graded levels of iron and zinc on the productivity of geranium. Communications in Soil Science and Plant Analysis, 38, 2581-2599.

[23] Donald, D.G.M. and Visser, L.B. (1989). Vermicompost as a possible growth medium for the production of commercial forest nursery stock. Appl. Plant Sci. 3, 110-113.

[24] Tejada, M., Gonzalez, J.L., Hernandez, M.T. and Garcia, C., (2008). Agricultural use of leachates obtained from two different vermicomposting processes, Bioresource Technology, 99, 6228-6232.

[25] Karmegam, N., Alagumalai, K. and Daniel, T. (1999). Effect of vermicompost on the growth and yield of green gram (*Phaseolus aureus* Roxb.). Tropical Agriculture 76, 143-146.

[26] Zaller, J.G. (2007). Vermicompost as a substitute for peat in potting media: Effects on germination, biomass allocation, yields and fruit quality of three tomato varieties. Scientia Horticulturae, 112, 191-199

[27] Edwards, C.A., Arancon, N.Q. and Greytak, S. (2006). Effects of vermicompost teas on plant growth and disease. BioCycle 47, 28-31.

[28] Lazcano, C., Arnold, J., Tato, A., Zaller, J.G. and Domínguez, J. (2009). Compost and vermicompost as nursery pot components: Effects on tomato plant growth and morphology. Spanish Journal of Agricultural Research 7, 944-951.

[29] Arancon, N.Q., Edwards, C.A., Babenko, A., Cannon, J., Galvis, P. and Metzger, J.D. (2008). Influences of vermicomposts, produced by earthworms and microorganisms from cattle manure, food waste and paper waste, on the germination, growth and flowering of petunias in the greenhouse, Applied Soil Ecology 39, 91-99.

[30] Singh, R., Sharma, R.R., Kumar, S., Gupta, R.K. and Patil, R.T. (2008). Vermicompost substitution influences growth, physiological disorders, fruit

yield and quality of strawberry (Fragaria x ananassa Duch.). Bioresource Technology, 99, 8507-8511.

[31] Haydock, P. P. J., Woods, S. R., Grove, I. G., and Hare, M. C. (2013). "Chemical control of nematodes," in Plant Nematology, eds R. N. Perry and M. Moens (Wallingord: CABI), 259-279.

[32] Gabour EI, Marahatta SP, Lau J-W. Vermicomposting: A potential management approach for the reniform nematode, Rotylenchulus reniformis. Nematropica. 2015;45(1):285-287

[33] Edwards CA, Arancon NQ, Emerson E, Pulliam R. Suppression of plant-parasitic nematodes and arthropod pests by vermicompost teas. Biocycle. 2007;48(12):1-6

[34] Rodríguez-Kábana R. Organic and inorganic nitrogen amendments to soil as nematode suppressants. Journal of Nematology. 1986;18(2):129-135

[35] Kerry B. Fungal parasites of cysts nematodes. In: Edwards CA, Stinner BR, Stinner D, Rabatin S, editors. Biological Interaction in Soils. Amsterdam: Elsevier; 1998. pp. 293-306

[36] Siddiqui ZA, Mahmood I. Role of bacteria in the management of plantparasitic nematodes: A review. Bioresource Technology. 1999;69(2):167-179

[37] Bilgrami L. Evaluation of the predation abilities of the mite *Hypoaspis calcuttaensis*, predaceous on plant and soil nematodes. Fundamental & Applied Nematology. 1997;20:96-97

[38] Sikora, R.A. & Fernandez, E. 2005. Nematode parasites of vegetables. In: Luc, M., Sikora, R.A. & Bridge, J. (Eds). Plant-parasitic nematodes in subtropical and tropical agriculture. CABI Publishing, Wallingford, UK, 319-392 pp.

[39] Akhtar, M. & Malik, A. 2000. Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: A review. Bioresource Technology 74, 35-47.

[40] Agyarko, K. & Asante, J.S. 2005. Nematode dynamics in soil amended with neem leaves and poultry manure. Asian Journal of Plant Sciences 4, 426-428.

[41] Oka, Y., Nacar, S., Putievsky, E., Ravid, U., Yaniv, Z. & Spiegel, Y. 2000. Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90, 710-715.

[42] Ashraf, M.S. & Khan, T.A. 2007. Efficacy of *Gliocladium virens* and *Talaromyces flavus* with and without organic amendments against Meloidogyne javanica infecting eggplant. Asian Journal of Plant Pathology 1, 18-21.

[43] Radwan, M.A., Abu-Elamayem, M.M., Kassem, M.I. & El-Maadawy, E.K. 2004. Management of Meloidogyne incognita rootknot nematode by integration with either organic amendments or carbofuran. Pakistan Journal of Nematology 22, 135-142.

[44] Pokharel RR and HJ Larsen. "The importance and management of phytoparasitic nematodes in western Colorado fruit orchards". Journal of nematology 39 (2007): 96.

[45] Pokharel RR., et al. "Plant-parasitic nematodes, soil and root health in Colorado onion fields". In: Godin, R. (ed.). Western Colorado Research Center, Colorado State University. Annual report (2009): 39-44.

[46] Frank S Hay. The American Phytopathological Society (APS). Nematodes the good, the bad and the ugly. University of Tasmania (2019).

*Role of Microbial Enriched Vermicompost in Plant-Parasitic Nematode Management DOI: http://dx.doi.org/10.5772/intechopen.97934*

[47] Koenning S., et al. "Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994". Journal of Nematology 31 (1999): 587-618.

[48] Renčo M., Sasanelli N., D'Addabbo T., Papajová I. 2010. Soil nematode community changes associated with composts amendment. Nematology 12 (5): 681-692.

[49] Bilgrami A.L. 1996. Evaluation of the predation abilities of the mite *Hypoaspis calcuttaensis*, predaceous on plant and soil nematodes. Fundamental & Applied Nematology 20: 96-98

## **Chapter 4**

## Plant Parasitic Nematodes: A Major Constraint in Fruit Production

*Nishi Keshari and Gurram Mallikarjun*

## **Abstract**

The plant parasitic nematodes are one of the major limiting factors in fruit trees specially in citrus, banana, papaya, jackfruit, guava etc. The root knot nematodes are the major problem amongst all those nematodes infecting on these trees. Besides, directly causing a huge losses, they are also inviting the secondary plant pathogens, like fungi, bacteria, viruses etc. amongst which, the wilt fungus, *Fusarium* species increase the severity of the diseases. This complex disease is becoming much severe in banana and guava recent years. In citrus also, the citrus nematodes, *Tylenchulus semipenetrans*, is causing havoc by slow decline disease and it is becoming a major problem in horticultural nurseries because these nurseries are a hot spot of citrus nematodes. So, unknowingly these nematodes get spread to different places. The management of these nematodes by simple, cheap and eco friendly methods, is very important as it will decrease the monetary pressure on cultivators as well as it helps in improving environmental pollution.

**Keywords:** plant parasitic nematodes, fruits, *Meloidogyne* spp., *Tylenchulus semipenetrans*, *Pratylenchus* spp.

## **1. Introduction**

Plant parasitic nematodes cause considerable economic losses in fruit crops. The main loss is the destruction of roots which hinders the movement of nutrients and water through the vascular system, so, there is drastic reduction in fruit or bunch weights, the quality of fruits is deteriorated and there is a drastic reduction in plant numbers. Furthermore, roots damaged by nematodes are easy prey to fungi and bacteria which invade the infected roots and feed on them and thus roots decay rapidly. The root-knot nematode, *Meloidogyne incognita*; the burrowing nematode, *Radopholus similis* and citrus nematode, *Tylenchulus semipenetrans* are the major nematode pests that infect these fruit crops. Around 30–40% loss in yield is due to these nematodes. The nematode infestation in fruit crops not only aggravate disease complexes but also breaks down disease resistance in certain varieties of fruit crops. These nematodes mainly spread through infested planting material to other uninfested sites. For an instance, in banana, paring or trimming of suckers is carried out before planting which is usually not adequate to eliminate deep infections in the suckers. The residual nematode population builds up and disseminates when they enter the irrigation system. Other routes of their dispersal include soil adhering to tractor tyres, shoes of labour and tillage implements. The major fruit crops which suffer severe nematode infestation, are discussed here.

## **2. Citrus**

Citrus is grown in more than 125 countries in a belt between 35° latitude north or south of the equator. The citrus is generally consumed as fresh fruit, approximately 68% of the world's citrus production, and in international trade, about 11% of total production is used [1]. *Citrus* spp. are naturally deep-rooted plants [2, 3], and optimum growth requires deep, well-drained soils. The first nematode discovered in citrus, was, *Meloidogyne* sp. which parasitized the citrus in Florida in 1889 but people were unaware about these nematodes. Again in 1913, Thomas discovered the citrus nematode infecting citrus in California. Nathan Cobb had reported it as a new species, *T. semipenetrans*, and this was the causal agent of mottling disease in citrus in California, later identified as 'slow decline' because the trees declined in vigour but very slowly about in 10–15 years. *T. semipenetrans* has been found in every citrus-growing region of the world since its discovery [4]. Field infestations within United States, infect 50–90% of citrus orchards in Arizona, California, Florida, and Texas, as well as local vineyards in California [4–6]. The major economic nematodes causing diseases in citrus, are *T. semipenetrans*, *Pratylenchus* spp. and *Meloidogyne* spp.

## **2.1 Citrus nematode (***T. semipenetrans***)**

In world, Cobb in [7] first described its distribution, morphology and life history. In India, it was first reported by Siddiqi [8] at Aligarh, Uttar Pradesh. About 80% of the citrus trees were reported to be infected with this nematode. This slow decline further results in 'die back' disease in most of the citrus trees in India and is a major problem that is estimated at 8.7–12.2%. The citrus nematodes are found highly in number when the citrus orchards are established in the soil which is finelytextured or sandy having high organic matter content. Nematode reproduction was positively favoured when there are fluctuations in soil salinity from high to low, while sandy soils poor in organic matter, hinder population increase [9]. In Florida and California (USA), there is 24–60% of *T*. *semipenetrans* infection in citrus orchards while it is 70–90% in commercial orchards of Brazil and Spain [10]. This shows that the citrus nematodes can infect under extreme range of environmental conditions. Unfortunately, infected nursery seedlings which are the main infection material transported from one to another, are not easily detected by the personnel involved in that business just because of unawareness [10]. If the infection is not severe, the roots show only lesions but, during severe infection, the sloughing of root cortex appears and roots die finally. Nematode infection increases the levels of the cell-damaging enzymes [11].

## **2.2 Symptoms**


## **2.3 Life cycle**

*T. semipenetrans* exhibits sexual dimorphism, i.e., different shape of male and female individuals at both the juvenile and adult stage. The life cycle duration is of 6–8 weeks from egg to egg [12]. The *T*. *semipenetrans* biology and ecology have been extensively studied [10]. The egg hatching takes place in 12–14 days at 24°C. The male larvae after second stage, do not feed and become mature in 7 days whereas the female takes 14 days to find the feeding site on the root and start feeding and moulting. The female juveniles can survive more than 2 years in the absence of roots [13]. The life cycle was of 14 weeks on *Poncirus trifoliate*, 10 weeks on *Ruta bracteosa* and 7 weeks on *Citrus aurantianum* and *C. limettoides* [14]. The mature males are vermiform and mobile found in the soil or in the egg masses. Therefore, the feeding apparatus (stylet and oesophagus) of adult males is poorly developed and may be difficult to observe. *T. semipenetrans* is a sexually reproducing species that can occasionally reproduce by facultative parthenogenesis without the need of males. The mature females and their eggs are found attached to roots which are protected by soil particles that sticks to gelatinous matrix. The females are swollen and enlarged posteriorly often protruding on the root surface in a finger like protrusions while elongated and not swollen anteriorly generally embedded and hidden in cortical parenchyma. After hatching at optimum temperature, i.e., at 25°C, females lay eggs after 6 weeks, on the root surface in a gelatinous egg mass secreted from the excretory pore.

## **2.4 Histopathology**

The second stage larvae enter the root surface and start feeding on the mature part. After moulting, the immature females penetrate deeper in the cortex region and their neck becomes longer to feed inside. The posterior portion remains outside of the root. They establish a feeding site around their stylet where the cortical cells change into food sink by reaction of dorsal oesophageal gland secretions. These are called 'nurse cells' which provide food to the developing females. The nurse cells are thick-walled cells with modified cell organelles like enlarged nucleus and nucleolus. These cells have no vacuoles. The cells are gradually destroyed by their feeding and hence the plants can not draw food and water for their growth, so change in development proceeds which finally results in poor vigour.

#### **2.5 Host range**

Unlike many nematodes, *T. semipenetrans* has a restricted host range. Many plants belonging to Rutaceae family, were found as hosts of this nematode. It was reported that from 23 countries, 29 species of *Citrus*, 21 citrus hybrids and 11 other species as the hosts [15]. Except these plants, it was also reported to attack on other plants like *Andropogon rhizomatus*, *Panicum* spp., Olive (*Olea* spp.), grapevines (*Vitis* spp.), Persimmon (*Diospyrous lotus*), Pear (*Pyrus communis*), *Calodendrum capense*, climbing hemp weed (*Mikania batatifolia*) and Lilac (*Syringa vulgaris*) [16–19]. Parvatha Reddy and Singh [20] reported that the citrus nematode also attacked grapes and loquats. It can parasitize more than 75 plant species belonging to rutaceous species (especially citrus and their close relatives) which are its suitable hosts [13]. Till now, there have been no reports of *T. semipenetrans* infecting herbaceous plants [17]. El-Mohamedy et al. [21] reported numerous citrus varieties from Egypt, Washington Navel, Valencia orange, Mandarins group varieties (*C*. *reticulata*), lemon (*C. aurantifolia*), and Balady orange (*C*. *sinensis*), Grapefruit (*C*. × *paradisi*), Sour orange (*C. aurantium*), and Kumquat (*C*. *japonica*) infected with this nematode [22, 23].

#### **2.6 Complex disease**

The citrus nematode also interacts with other plant pathogens and increase the severity of the disease. The wilt fungus, *Fusarium oxysporum* and *F. solani* with citrus nematode caused the death of citrus trees. The interaction between *T*. *semipenetrans* with such microorganisms occurs in inconsistent ways. It can reduce the infection of roots by *Phytophthora nicotianae* after the infection to citrus seedlings and it can also increase the virulence of *Fusarium solani* [10]. It was reported that the high population level of nematodes when interacted with *F. semitectum*, got synergistic effect on the infected citrus seedlings [24]. *Fusarium* spp. can be pathogenic on citrus roots alone [25] or in combination with nematodes [26], which leads to the great destruction of the feeder roots. The loss of feeder roots due to feeding of nematodes results in increase of drought stress and decrease of soil nutrient uptake, leading to chlorosis and loss of leaves. Affected trees do not die, but have an unthrifty appearance and yield fewer, smaller fruits than uninfested trees.

#### **2.7 Nematode spread**

The major cause for the spread of this nematode is because of distribution of infested planting material from the horticultural nurseries. Once the infested soil is taken with the planting material to distant places, it will spread this nematode to new sites. The other spreading agents are human and animals with the infested soil on their feet, agricultural implements, and water. They can survive in the soil for long periods in the absence of host that enables them to infect after a long time also. The main source of infection in the citrus plant, are, infected seedlings, organic

#### *Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

fertilizers, plant materials, irrigation, and machinery which are affecting growth and yield in the newly planted area [27]. In Egypt, which is a highly ranked citrus producing country [27], the citrus orchards were incorporated with the soil brought from silty soil from the Nile Valley for mulching and improving the soil quality but that soil was nematode infested, so the disease incidence got aggravated [28]. So, with time, the nematode spread their populations in that soil and the losses increased [27]. Soil moisture is often inversely related to population growth of *T. semipenetrans* [29–31].

## **2.8 Management**

## *2.8.1 Preventive measures*

The most important and effective method is to take every effort to avoid the use of infested planting materials and contaminated farm implements when new plantations have to be established. In the orchard, proper drainage and light should be there and shade should be avoided as far as possible. New nurseries should not be established near the old citrus orchards. All sanitation practices should be taken to avoid nematode infestations. Use of certified nematode-free material for planting, is also very important. If there is established infection, the citrus orchard should be rotated with annual crops for 1–3 years before replanting helps to reduce citrus nematode populations. For intercropping, Marigold is an excellent crop which has repellent action and reduces the population of nematodes in citrus [32].

## *2.8.2 Biological measures*

Application of *Pseudomonas fluorescens* @ 20 g/tree. *Paecilomyces lilacinus* parasitize nematode eggs and females, reduces the number of plant parasitic nematodes in soil, *T. semipenetrans*. Park et al. [33] reported that *P. lilacinus* could produce leucino toxin and other nematicidal compounds. *Trichoderma* spp. play major roles in controlling plant diseases in roots and soil. The *Trichoderma* spp. have antagonistic activities to be used as effective biological control agents for many plant diseases which are caused by soil borne fungi and nematodes [34]. Although *Bacillus subtilis* was reported as a bio-agent against soil borne fungi [35] some strains of *B. subtilis* exhibited enormous potential as bioagent in the management of nematodes [36]. *B. subtilis* produces antibiotics as bacterocin and subitisin [37, 38]. Streptomycetes are the major group of actinomycetes producing secondary metabolites that could decrease the invasive juveniles of root-knot nematodes. Streptomyces is known for its chitinolytic activity which produces more extracellular chitinase [39]. Some species of streptomycetes release compounds like antibiotic that inhibit the growth of plant-pathogenic fungi [40] and plant parasitic nematodes [41]. Qingfei et al. stated that *Streptomyces* spp. produce lytic enzymes and nematicidal compounds and can be one of candidates for bio-agents against nematodes. Le Roux et al. [42] demonstrated that *P. lilacinum* individually controlled *T. semipenetrans* Cobb on mandarin and rough lemon effectively, but when the fungus was combined with oil-cakes, the results were more significant.

## *2.8.3 Chemical measures*

In heavy infestation, many nematicides have successfully been used to lower down the population of *T. semipenetrans* on citrus in many locations. The soil treatments with soil solarization and nematicides is highly beneficial in both replanting conditions and already established orchards. Pre-plant application of carbofuran 3 G @

100 g/tree, was found highly beneficial. The nematicide application often increases the citrus yield [10]. Nemastop (natural oils) as commercial nematicide, play very important role in controlling nematodes. The effect of Nemastop on the nematode might be due to alkyl cysteine sulphoxides which released a mixture of volatile alkyl thiols and sulphides [43]. Whereas, Nemaphos belonging to organophosphate group [44] showed a highly performance systemic nematicide. When halogenated hydrocarbons are used as pre-plant soil fumigants, these can effectively control *T. semipenetrans* for many years [45–48]. However, to maintain the low population and higher yield, one has to apply the chemicals repeatedly. In the first year of treatment, the effect will be little on yield and fruit quality but the efficacy to increase the growth and yield parameters can be observed in the following year [49–51].

Oxime carbamates (aldicarb, oxamyl, Carbofuran) and organophosphates (fenamiphos, ethoprophos and cadusaphos) are the two main groups of nematicides which are available in the market for the management of citrus nematode. Of these, granular formulation of Cadusaphos has shown greater efficacy against the *T. semipenetrans* [52–55]. Irrigation is generally recommended before nematicide application for better results.

#### *2.8.4 Resistant rootstocks*

The use of resistant root stock is the best method to avoid the disease if available. It was reported by many workers that the use of resistant (Swingle citrumelo) rootstocks and certified propagative material which are free from nematode parasites of citrus, are promising cultivars for preventing the loss caused by *T. semipenetrans* to citrus [56–58]. In Florida, this approach has significantly reduced the spread of this parasite, making the land free from nematode infestations [59]. In California vineyards, resistant (Ramsey) or moderately resistant (vinfera Dog Ridge) grape rootstocks were used successfully [60] (McKenry, personal communication). To get sustainable agriculture, planting of nematode certified citrus and grape rootstocks, is an excellent practice that should be adopted for other fruit crops also which are susceptible to nematode infections. Resistance-breaking biotypes were developed on Swingle citrumelo [61]. The commercially resistant rootstock, Swingle citrumelo is common in Florida and combined with regulation program of the citrus nematode, has decreased the spread of *T*. *semipenetrans* dramatically [62]. Using a resistant rootstock is recommended whether or not nematodes are present. Trifoliate orange is known to be tolerant to citrus nematode.

#### *2.8.5 Soil solarization*

Soil solarization is an effective method to disinfest the upper soil layers by moistening the soil and covering with a clear plastic sheet in regions with hot and dry summer months. This method is highly beneficial to manage the population of insects, soil borne pathogens, weed seeds and nematodes by altering the physical, chemical, and biological properties of the soil. In South Africa, solarization has not shown promising and there was inconsistent suppression of the citrus nematode and tree growth [63], which may be because these nematodes are found deep within the soil profile and so, are not affected by solarization that is most effective for the upper soil layers [64].

#### *2.8.6 Steam treatment*

Steam treatment of soil is widely used for the control of nematodes in planting material and is shown very effective. In this method, the soil is heated up to 70°C, mainly by means of aerated steam. It is very useful and economical for disinfestation of nursery beds. Steam treatment of vermiculite or tuff stones is usually effective but is more difficult for peat soils due to their high water content [65]. The dipping of planting material in hot water is also effective but here the temperature of water should be taken care of, otherwise the germination may get affected. Bare root dipping of citrus seedling in hot water at 45°C for 25 min [66] or 50°C for 10–20 min [67] was found to be effective without any adverse effect on the germination.

## **2.9 Lesion nematodes (***Pratylenchus* **spp.)**

There are three species of *Pratylenchus* which can affect citrus i.e., *P*. *coffeae*, *P*. *brachyurus*, and *P*. *vulnus*. All are reported from Egyptian citrus orchards [68]. The most pathogenic species is *P*. *coffeae* [10]. Lesion nematodes, being a migratory endoparasites, cause infection mainly in the feeder roots during their movement by penetrating the cortical tissue, but they do not invade the vascular tissues. After their infection, the secondary organisms infect the root tissues and then the vascular tissues also got infected. *P. coffeae* is obligatorily amphimictic, all stages infective with males feeding in the roots [69]. Its reproduction is highest at high (26–30°C) soil temperatures. At those temperatures, the life cycle is completed in less than a month, and it can achieve densities of up to 10,000 nematodes/g root [70] and persist in soil roots for at least 4 months. This leads to root weight reduction by half and growth reduction ranging from 49 to 80% in young trees in field conditions. A 3-fold to 20-fold differences between infected and non-infected trees was observed in terms of the numbers of fruit [71]. Commercial rootstocks resistant to *P. coffeae* are yet to be identified. A lesion nematode, *P. coffeae*, was detected on citrus in Sao Paulo State, Brazil and found to infest about 1% of the nurseries and orchards [72].

The biology of *P. brachyurus* is similar to that of *P. coffeae.* [13]. It has been established as a pathogen of citrus seedlings across several soil types. [73]. After controlling *P. brachyurus* with aldicarb, yields of Valencia orange trees grafted on rough lemon were increased, and plants sustained reduced frost damage in the winter [51]. Some studies failed to note the fact that *P. vulnus* has been found associated with citrus plants in Egypt [10, 13, 68]. This species is capable of causing significant damage to citrus seedlings but has not been reported to damage mature plants [74]. Biology, population growth rates, and root damage are similar to those described for *P*. *coffeae* [13]. Several *Pratylenchus* species have been identified in Egyptian citrus orchards based on field studies [68].

**Host range:** *Citrus limon*, *C. sinensis*, *C. reticulata*, banana [75] and *Citrus jambhiri* [76].

### *2.9.1 Management*

**Chemical:** Fensulfothion or phenamiphos @ 4.4 kg a. i./ha and aldicarb or carbofuran @ 4 kg a. i./ha [77].

**Resistant root stocks**: Trifoliate orange (*Poncirus trifoliata*), Rubiboux 70-A5, hybrids of *Microcitrus australis* x *M. australasica.*

#### *2.9.2 Root knot nematodes (*Meloidogyne *spp.)*

Root knot nematodes attacking citrus trees, are not reported much and is little in distribution [10]. Only a few locations in world, have been found to be infested with this nematode. A pathogenic root knot nematode species (known as Asiatic pyroid citrus nematode) recorded from Taiwan and New Delhi could cause elongated galls on citrus roots [13]. It can complete its life cycle on several citrus and other plant species. The common species are *Meloidogyne incognita*, *M*. *javanica*, and *M*.

*arenaria* reported to infect roots of Troyer citrange and sour orange, causing small galls, but their multiplication is not recorded [78]. *M. indica* was reported from citrus tree at some locations in India [79].

### *2.9.3 Symptoms*


#### *2.9.4 Management*

**Chemical methods:** Seedling dip treatment with carbosulfan @ 500 ppm for 6 h can effectively control root knot nematodes.

**Organic amendments**: Mustard cake, farm yard manure and poultry manure @ 2.5 kg/plant were found effective against root knot nematode and increasing the plant growth.

**Host resistance:** Resistant rootstocks, like, Rangpur lime 8784, Sour orange Tirupati, Citrumello 4479, Rangpur 8748, Rangpur lime chethalli, Trifoliate orange chethalli, Nasnaran, Hazara Australia, Rangpur lime Kirumakki, Pramalini and Anand Selection were moderately resistant.

## **3. Guava**

The common guava (*Psidium guajava* L.) is indigenous to tropical America. It is a popular fruit generally consumed as fresh fruit but also processed as jam, paste, puree, canned shells and juice for round the year use. It is grown throughout the tropics and subtropics and is of commercial importance in more than 60 countries [81]. This fruit tree also suffers many nematode infections. Mostly root knot nematodes were reported from guava roots and after infection, the roots are predisposed to wilt fungus which is common wilt disease causing pathogen found in guava. This interaction resulted increased disease severity. Khan et al. [82] observed greater damage to guava with both *Helicotylenchus dihystera* and *Fusarium oxysporum* than with the nematode alone. In India, *Hoplolaimus indicus* was found to be a pathogen of guava [83, 84] and *Tylenchorhynchus cylindricus*, in numbers of up to 2000 nematodes/100 cm3 of soil, was found associated with damaged guava trees in Iran [85]. In the past two decades, the

*Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

root-knot nematodes, *Meloidogyne* spp. Göldi, have been reported on some species of the tropical fruit trees grown in the region [86]. Gomes et al. [87] demonstrated that guava trees infected with *M. mayaguensis* had deficiencies in nitrogen, potassium, phosphorus, calcium, and magnesium, and that these mineral deficiencies were proportionally related to the severity of root galling and root decay, which eventually led to the death of guava trees within a few months. Recently a new species, *M. enterolobii* has been found to be widely associated with many guava trees.

## **3.1 Symptoms**


#### **3.2 Spread**

In guava, grafts are often produced in polythene bags with a substrate mixture (sand + soil + FYM or other organic manure). In most cases the substrate mixtures harbour the aforementioned nematodes as well as other harmful fungi and bacteria. Generally, nurserymen do not treat the soil combination used in the production of fruit seedlings or grafts in their nurseries. As a reason, before applying the substrate, it should be treated with biopesticides.

#### **3.3 Management**

### *3.3.1 Prevention*

Nematode free plants should be used for new planting and the orchard should be planted in nematode free soil. The soil used for the preparation of new plants should be sterilized. The equipment should be sterilised before using.

#### *3.3.2 Deep summer ploughing*

The soil for the planting of new guava plants, should be deeply ploughed during hot summer months. It should be repeated twice or thrice at 15 days interval.

#### *3.3.3 Biological method*

For biological control, many fungal and bacterial bioagents are used for the management of nematodes. The fungal bioagents, *Purpureocillium lilacinum* and *Verticillium clamydosporium* were found as the most potent fungal parasites that can effectively control *Meloidogyne* spp. on many host plants [89]. Another fungal bioagent, *Trichoderma harzianum* effectively suppressed the population of the root-knot nematode, *M. enterolobii* in both soil and roots of guava in Thailand [90]. In Saudi Arabia, Al-Hazmi et al. [91] found a heavy colonization of the cysts of *Heterodera avenae* Woll. with the fungus, *Verticillium clamydosporium.* Rao [92] who reported that the fungus, *P. lilacinum* and the bacteria, *P. fluorescens* enriched the farm yard manure, fairly controlled the reniform nematode, *R. reniformis* and the root knot nematodes.

#### *3.3.4 Organic and inorganic nitrogenous amendments*

These amendments are useful both for managing plant parasitic nematodes as well as to improve the soil fertility [93]. At rates as low as 300–400 mg/kg soil, urea and ammonia were found to be effective in controlling plant parasitic nematodes [94]. Guava decline disease, a disease complex caused by *M. mayaguensis* in association with the fungus, *Fusarium solani*, has been successfully managed in a commercial guava plantations, with significant yield gains obtained by the use of cow manure and poultry compost [95]. Urea and nitrogenous fertilizer are considered to be good nematicides when applied at levels as low as 300–400 mg/kg soil because due to root infections, the roots become unable to take the minerals and nutrients [94, 96–98]. Previously it was also reported that organic and inorganic nitrogen amendments had a nematicidal effect against plant parasitic nematodes [93, 94, 99]. Gomes et al. [95] reported that the guava canopy when treated with organic soil amendments, particularly poultry compost and cow manure, gave better control of the root knot nematode, *M. mayaguensis*. Organic soil amendments not only promote the growth of soil microorganisms that are antagonistic to plant parasitic nematodes but also release specific toxic compounds during their decomposition that may have nematicidal effects against nematodes [99]. These organic amendments also improve crop nutrition and growth which lead to increased tolerance of plants against plant-parasitic nematodes [100].

#### **3.4 Production of healthy rootstocks/grafts**

Enriched substrates should be used for producing healthy grafts or rootstocks of fruit crops. A mixture of enriched FYM can be produced by mixing one ton of soil mixture consisting red soil and sand in equal proportions with 500 kg of FYM which is added with 2 kg each of *P. fluorescens* 1% W. P., *Trichoderma harzianum* 1% W. P., *Paecilomyces lilacinus* 1% W.P. + 50 kg neem or pongamia cake +5 kg carbofuran or phorate.

#### **3.5 Spraying or drenching the nursery seedlings or grafts with bio-pesticides**

The nursery seedlings or grafts can be treated by dissolving 5 g or 5 ml/l of water once in 10 days.

#### **3.6 Management of nematodes in the main field**

#### *3.6.1 Soil application*

Before planting the saplings of guava, the land should be thoroughly ploughed and soil should be brought to fine tilth. Then recommended doses of fertilisers

#### *Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

should be added because the vigour plants resist the nematode attack. Now carbofuran or phorate @ 20 kg–25 kg + 200 g neem/pongamia/mahua cake per acre should be added to reduce the initial population of nematodes. The optimum moisture should be maintained in the beds which is necessary for proper decomposition of organic matter. In case of organic farming, during the land preparation, application of two tons of FYM or 500 kg of neem cake/pongamia cake or one ton of enriched vermicompost with *P. fluorescens* + *Trichoderma harzianum* + *Paecilomyces lilacinus*.

## *3.6.2 Process of enrichment of FYM*

For enrichment of FYM, 2 kg each of *P. fluorescens, Trichoderma harzianum* and *Paecilomyces lilacinus* formulation should be mixed with one ton of well decomposed FYM under shade and covered with mulch. An optimum of 25–30% moisture should be maintained for a period of 15 days. This mixture should be thoroughly mixed once in a week to promote maximum multiplication along with even growth of the microorganisms in the entire lot of FYM.

## *3.6.3 Process of enrichment of neem cake*

Neem cake can be enriched by mixing with 2 kg each of *P. fluorescens*, *Trichoderma harzianum* and *Paecilomyces lilacinus* with one ton of neem cake under shade and covered with mulch. For next 15 days, an optimum moisture of 25–30% has to be maintained followed by thorough mixing once in a week to ensure maximum multiplication & uniform growth of the microorganisms in the entire lot of neem cake.

## *3.6.4 Process of enrichment of vermicompost*

Similarly, vermicompost can be enriched by mixing with 2 kg each of *P. fluorescens*, *Trichoderma harzianum* and *Paecilomyces lilacinus* with one ton of vermicompost under shade and covered with mulch. For next 15 days, an optimum moisture of 25–30% has to be maintained followed by thorough mixing once in a week to ensure maximum multiplication & even spread of the microorganisms in the entire lot of vermicompost.

## *3.6.5 Application of bio-pesticides at the time of planting*

At the time of planting, application of bio-pesticide enriched FYM @ 3 kg or enriched neem cake @ 250 g or enriched vermicompost @ 500 g/plant at an interval of six months.

## *3.6.6 Spraying*

Spraying plants with organic formulation containing *P. fluorescens* & *Trichoderma harzianum* at regular 30-day intervals at a dosage of 5 g/l or 5 ml/l.

#### *3.6.7 Drenching or application through drip irrigation system*

Drenching of the above biopesticide @ 5 g/l or 5 ml/l at regular interval of 30 days.

## **4. Banana**

It is also one of the important fruit crops in India, cultivated over 0.83 million ha, constituting about 44.3% of total fruit production. Generally, the farmers and cultivators grow banana as cash crop and do the intensive cultivation on a commercial scale and as monoculture in the same field. This system invited several pests and diseases to this crop. Among these major biotic stresses, plant parasitic nematodes are causing severe losses in banana production not only individually but also with the interaction of wilt fungi, *Fusarium oxysporum f.* sp*. cubense* [101]. The major nematode causing economic yield loss globally, is the burrowing nematode, *Radopholus similis* (Cobb, 1893) Thorne, 1949. Other nematode species that are found in banana cultivation along with *R. similis*, are, lesion nematode (*Pratylenchus coffeae*), spiral nematode (*Helicotylenchus multicinctus*) and *Meloidogyne* spp. In South Africa, 34 plant parasitic nematode species have been found associated with banana [102] (SAPPNS1). Likewise, *Meloidogyne incognita* (Kofoid and White, 1919) Chitwood, 1949, *Meloidogyne javanica* (Treub, 1885) Chitwood, 1949 and *Meloidogyne arenaria* (Neal, 1889) Chitwood, 1949 are most commonly reported root knot nematode species found in association with local banana cultivars in Zimbabwe [103]. Root knot nematodes were the most abundant and together with spiral nematodes constituted 72% of the total plant parasitic nematode complex [104]. The root knot nematodes become larger in size in banana root tissue as the root tissues are thicker. These nematodes attack root and corm tissues causing damage which results in long vegetative growth cycle, late fruiting, production of small bunches, less fruiting and finally toppling of the plants. The spiral nematodes produce root lesions in the corm which attract the secondary pathogen, fungi and bacteria, that aggravate the damage of the root system [105]. Root knot nematodes are present in almost all banana plantations [106]. The general perception is that these nematode pests can cause severe damage to young plants, resulting in suboptimal growth and yield.

### **4.1 Host range**

Both *M. incognita* and *M. javanica* has a wide host range of cultivated crops including most broad leaf weed species. To effectively control root-knot nematodes in bananas, special attention should be paid to weeding during fallowing or crop selection for rotation [107].

## **4.2 Losses**

The diseases in banana are caused by 3–4 nematodes so, the quantification of the damage by individual species is, therefore, not possible. Willers [108] estimated that these pests caused a direct loss of 19% in total production of the crop.

## **4.3 Symptoms caused by burrowing nematode,** *R. similis*

The origin of burrowing nematode is believed to be from Australia and New Zealand [109] from where recently new species have been described. The relative increase in worldwide distribution is mainly due to transfer of infected planting material domestically as well as internationally. The importation of banana cultivar Cavendish which is susceptible to nematode attack is often correlated with the wide distribution of *R. similis*. It is assumed that *R. similis* was introduced in Latin America and the Caribbean, on the cv. Gros Michel where it subsequently infested the more susceptible Cavendish cultivar [110]. In a study, 55 out of 57 burrowing nematode isolates, collected from Australia, Cameroon, Central America, Cuba, Dominican Republic, Florida, Guadeloupe, Hawaii, Nigeria, Honduras, Indonesia, Ivory Coast, Puerto Rico, SA and Uganda were morphologically similar to *R. similis*.

The following are the symptoms:


## *4.3.1 Management*


## **Symptoms caused by Lesion nematode**, *Pratylenchus coffeae*


• Reduction in size and number of leaves and in bunch weight.

**Symptoms caused by Root knot nematodes**, *Meloidogyne* spp. and Reniform nematode, *Rotylenchulus reniformis*


## *4.3.2 Management*


## *4.3.3* Helicotylenchus *spp. (Spiral nematodes)*

Spiral nematodes are one of the most common group of nematodes infesting banana which include *H. multicinctus* (Cobb, 1893) Golden, 1956, *Helicotylenchus dihystera* (Cobb, 1893) Sher, 1961, and *Helicotylenchus erythrinae* (Zimmermann, 1904) Golden, 1956 [103, 106]. A survey of commercial banana plantations showed that species of *Helicotylenchus* (mainly *H. multicinctus*) were present in 95% of all the samples which had highest overall average [106]. These results were similar to previous studies. *H. multicinctus* was recorded in most of the soil and root samples collected in a survey [116]. Gowen and Quénéhervé [101] suggested that

*H. multicinctus* is often the major parasitic nematode on banana where temperature and rainfall conditions are suboptimal for the crop.

## *4.3.4 Damage*

The above-ground symptoms are not specific and resemble damage caused by other nematode pests of banana. Symptoms of damage inflicted by *H. multicinctus* include discolouration of the root epidermis where small reddish lesions can be observed in the superficial cortical region also in rhizome tissue of infected plants along with reduction in the number of lateral roots [103]. Under severe infestations, the smaller lesions enlarge and coalesce leading to extensive necrosis in the outer cortical region of root and even root dieback sets in [117]. Toppling of plants can be observed due to poor anchorage under severe infestation [105]. No distinct biotypes or races have been reported in *H. multicinctus* [101].

## *4.3.5 Host range*

*H. multicinctus* hosts range from most edible banana and plantain to various alterative host plants, such as pigweed (*Amaranthus* spp.), purslane (*Portulaca oleracea*) and ornamentals [101].

## *4.3.6 Nature of damage*

Most damaging spiral nematode species spend most of their life cycle in root tissues of banana. Their buccal cavity is equipped with a hollow stylet which helps in puncturing and feeding the inner contents of cells. They multiply and build their population as high as a million in corm and root tissues and they alter the physical and functional integrity of the tissues. Nematodes disrupt nutrient and water uptake results in delay of growth and finally banana plants topple down. They destruct the primary roots so poor anchorage develops and that results in toppling of the plants.

## *4.3.7 Loss*

In banana, the majority of the losses caused by *R. similis* infection is due to mass destruction of primary roots and could be present throughout entire root system, including the rhizome leading to poor anchorage [118]. During windy conditions, the plants with bunches often topple off due to heavy weight and poor anchorage, Hence the name "Toppling disease". The nematodes move laterally in cortical region and colonize the cavities caused by parasitic and saprophytic fungi which results in greater lesion formation thus, leading to indirect disruption of stele which otherwise is rare. When this occurs, the entire root beyond the initial nematode entry site becomes functionless [103].

## *4.3.8 Host range*

Duchame and Birchfield [119] established the existence of a *R. similis* biotype that also attacked citrus, it was confirmed that the *R. similis* did not attack citrus [120, 121]. An experiment to determine the host status was conducted to study the reaction of banana plants which were planted in *R. similis* infested soil. Out of 100 plants tested, only 20 were found to be able to act as host for *R. similis* [120, 121]. However, in field conditions, no record of *R. similis* was found to be associated with banana in both the National Collection of Nematodes (NCN) and South African Plant Parasitic Nematode Survey (SAPPNS) records.

### **4.4 Lesion nematodes (***Pratylenchus* **spp.)**

The lesion nematodes which are well represented in South African region, have a limited distribution in banana plantations. Two species of lesion nematodes which are most frequently found in South Africa plantations include *Pratylenchus coffeae* (Zimmerman, 1898) Filipjev and Schuurmans Stekhoven, 1941 and *Pratylenchus brachyurus* (Godfrey, 1929) Filipjev and Schuurmans Stekhoven, 1941 with the former one being more frequently encountered [116]. *Pratylenchus coffeae* was very effective in limiting the spread of *R. similis* in local banana-growing areas as the combination of legislative measures with the development of tissue culture based propagative material for producing nematode free plants, limited the spread of *R. similis* and *P. coffeae.* Tissue culture plants are developed in the laboratory using healthy planting material are free of pests and diseases. Before these plants are distributed to the producers, they have to be tested and declared virus free which is generally found in 25.9% of root and soil samples in commercial plantations [106]. Despite, these pests are widely distributed throughout the banana-producing areas, samples from several individual plantations had no lesion nematodes. The lesion nematode population in commercial banana plantations, varied from 0 to 1400 nematodes in 30 g/root. A survey was conducted in rural areas producing banana had shown that lesion nematodes were present in all areas where *P. coffeae* constituted only 3.2% of the nematode pest complex present in banana roots and 7.6% in soil samples [116].

#### **4.5 Damage**

The symptoms of damage caused by *P. coffeae* are very similar to those caused by *R. similis* as both are migratory endoparasites*.* They cause stunting of the plants, slow growth in vegetative phase, reduced number of leaves, lower bunch weight and reduce life span of plantations. There was reports of *P. coffeae* infections on banana plantations [107] which rendered the whole plantations unproductive.

#### *4.5.1 Host range*

The grapevine, citrus and veld (dune thicket, grasses) are the well-known hosts of *Pratylenchus coffeae* although it has a wide host range including many broad leaf weed species [101, 102] and information from both NCN and SAPPNS databases).

#### **4.6 Management strategies**

#### *4.6.1 Legislation*

In South Africa, when *R. similis* was discovered in banana under severe infection, the Government passed a legislation to prevent the spread of this nematode in new areas. This legislation is named as, "The Agricultural Pest Act 36 of 1983 [122]". According to this legislation, for the transport of planting material from one area to another area, a permit is required during transportation. In this act, the propagation materials are identified as suckers, rhizomes and setts. The tissue culture plants are the best technique to get rid of this nematode, because these plants are healthy and do not carry any plant pathogens but eventhough, a permit is required when any nursery is established there.

#### *4.6.2 Preparation of plant material*

In most developed countries, nematode free banana planting material is exclusively produced from tissue culture-based methods for commercial purposes.

#### *Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

However, in underdeveloped countries particularly in rural areas, suckers and rhizomes are still being used to produce propagative material especially where tissue culture-based methods are lacking. This results in spread of plant parasitic nematodes to healthy soil from infected sites. In such cases, paring is recommended where visible lesions caused by nematode pests and banana weevil is removed so that only white rhizome tissue remains. In many African countries especially in South Africa paring is generally followed by hot water treatment for a specific period of time to kill remaining nematode population and found to be effective in managing nematode pests. Once the rhizomes are treated, they must be planted in nematode free soil and for that the soil should be tested in nematological laboratory. This could be obtained by using one or combinations of the following strategies, like, keeping the field fallow for a certain period, organic amendments, soil sterilisation through heat by using transparent plastic cover for several weeks or planting the suckers in virgin soil. The soil sterilisation is not that much feasible in a large area as the use of polythene to a large area is not practical because of high input cost.

## *4.6.3 Cultural control*

Cultural methods are the cheap and easily followed method and also eco friendly. These methods include, fallowing for at least six months, is very useful [123, 124] as this is generally used as monocropping and because of this practice, nematode population build up and cannot be controlled through any method. Another method under this is, crop rotation with selected cover crops before banana cultivation that helps in reducing the nematode population so that the new suckers will not get the infection from very beginning like, Milne and Keetch [121] tested several cover crops and reported that radish (*Raphanus sativus*) and *Tagetes patula* reduced populations of *R. similis* after 5 months compared to that of ethylene dibromide (EDB) fumigation. Rotation with Buffalo grass (*Megathyrsus maximus* var. *trichoglum*; syn *Panicum maximum*) and purple bean (*Phaseolus atropurpureus*) also reported to control *R. similis* and *Meloidogyne* spp. Sugarcane crop (*Saccharum* hybrid) eliminated *R. similis* after 10 weeks [118]. The third method is intercropping. Intercropping is the cultivation of some particular crops with the main crops to manage the nematodes. These crops may be coffee (*Coffea arabica*), vegetables, maize (*Zea mays*) and cassava (*Manihot esculenta*). The next method is incorporation of organic manures in large volume. These manures after decomposition, release some phenolic compounds which are harmful for the nematode survival [125]. Application of 15 tons chicken manure/ha or 30 tons cattle manure/ha is generally recommended before planting banana [118]. The organic amendments have multiple beneficial effects like, increase in plant growth by improving soil structure and fertility, improvement in plant resistance and the stimulation of micro-organisms, which act as natural enemies of nematodes [125]. In cases of severe nematode infections, treatment of banana plants with a nematicide is recommended.

## **4.7 Clean propagative materials**

## *4.7.1 Banana tissue culture*

To prevent the spread of pests and disease, use of tissue culture banana planting material is one of the best methods to avoid the nematode infection. The tissue cultured propagating material is grown in such a media that it is free from any disease. So, this is an important practice to get rid of any pathogen or nematode. Using these materials, the spread of nematodes and other pathogens is controlled from diseased

field to healthy field. In Hawaii, most of the banana fields are infested with plantparasitic nematodes [126], micro-propagation from disease free materials using sterile techniques, offers a good way to obtain nematode free planting materials.

#### *4.7.2 Hot-water treatment*

A hot water dip has been successfully used to control burrowing nematodes and root knot nematodes in anthurium and ginger, respectively. Although, various temperature-time combinations ranging from 5 min @ 50°C to 25 min @ 55°C are recommended by researchers across the world, CTAHR researchers recommend soaking of banana suckers at 50°C for 10 min for disinfestion.

#### *4.7.3 Modified solarization*

Soil solarization involves heating the soil using natural solar radiation beneath a transparent plastic sheet to reach lethal temperatures for soilborne pests. The method is effective against a range of soil inhabiting pests, pathogens and nematodes which live in the top 4 inches (10 cm) of soil. The nematodes in the deep layers escape from the lethal temperature attained by this method.

#### *4.7.4 Biological control*

Many biocontrol agents like, fungal and bacterial bioagents are beneficial for the management of nematode pests of banana. In 1998, Daneel et al. [127] has demonstrated the efficacy of the soil fungus, *Purpureocillium lilacinum* (syn *Paecilomyces lilacinus*) for the control of banana nematode pests including *R. similis* and *Meloidogyne* spp. This bioproduct was also responsible for reducing the period of growth from flowering to harvesting which is helpful in escaping the nematode problems. This product was used at a dosage rate of 2 × 109 spores/g in suspension at 2–4 g/mat, depending on the severity of nematode infestation [128]. It was registered for use in South Africa on banana. *P. lilacinus* is a common soil fungus used as biocontrol agents that has been isolated from many different habitats around the world. It acts as a facultative egg pathogen of sedentary nematodes and also an important option to control juvenile and adult burrowing nematodes in banana. Mendoza et al. [129] reported that this nematode antagonistic fungus may be used as an integrated approach to control plant parasitic nematodes of banana.

#### *4.7.5 Corm destruction*

Since the most damaging stages of nematodes spend a considerable amount of their life cycle inside roots, killing of banana plants using a non-selective herbicide i.e., Glyphosate simultaneously kills the obligate endoparasitic stages of the nematodes Thus greatly improving the potential of successive fallow to lower the nematode populations without using nematicides [130].

#### *4.7.6 Cover-cropping*

Since banana is a perennial crop, and farmers take the benefit of ratoon crop also within the same planting cost, it is difficult to manage nematodes over a longer period of time because the endoparasites are nearly impossible to manage even through chemicals. In this condition, growing of cover crop may become an option for the management. These cover crops release some chemicals which are having allelopathic compounds that are deleterious for the nematodes. Allelopathy is a

*Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

biological phenomenon by which an organism produces one or more biochemicals that negatively affect the growth, survival, and reproduction of other organisms. The plants like, marigold (*Tagetes* spp.), sunhemp (*Crotalaria juncea*), rapeseed (*Brassica napus*, [131]), velvet bean (*Mucuna pruriens*, [132]), sorghum-sudan grass (*Sorghum bicolor* × *Sorghum arundinaceum* var. *Sudanense,* [133]), are reported as cover crops having allelopathy against plant parasitic nematodes. Among all these crops, marigold was found the best in banana cropping system and the allelopathy differs with different species of nematodes and marigold and also the soil temperature has the influence over it [134].

#### **4.8 Production of healthy seedlings of banana**

For the preparation of healthy banana suckers, a mixture of soil with biocontrol formulations and organic cakes can be prepared and used for hardening the seedlings. This mixture may include two kg each of *P. fluorescens* 1% W. P., *Trichoderma harzianum* 1% W. P. and *Purpureocillium lilacinus* 1% W. P. + five kg of carbofuran or phorate or 25 kg of neem cake or pongamia cake for preparing one ton of final mixture.

#### **4.9 Chemical control**

Conventionally, synthetic derived nematicides have been widely used for nematode control on banana. Although fumigants have been highly effective [135], such products are not used in banana production mainly due to high input costs and now these are banned also to be used in agriculture. The carbamates and the organophosphates are used regularly in the banana cultivation as pre and post application. These chemicals are used as granular or liquid formulations. During application, these are sprayed around the base of pseudostems or suckers. In South Africa, a chemical, Furfuraldehyde is registered for banana and it can be used when the population of nematodes is below economic damage level [128]. Because of unawareness and hidden mode of life cycle of plant parasitic nematodes, they are not given so much importance although they cause sufficient loss in the yield. Therefore, it is recommended that nematode samples are taken annually for nematode population estimation and that nematicides are only applied to reduce nematode pest populations likely to limit yield or cause long term yield decline. Although pre plant treatments such as soil fumigation with Telone II® (1,3-dicloropropene) are very effective in suppressing nematode populations, such treatments are short lived compared to the life of a banana plot. The following treatments should be done to manage the nematodes in banana:


9.Regular spot applications with nematicides.

## **4.10 Practices that maintain productivity and vigour**


## **5. Conclusions**

In banana cultivation, plant parasitic nematodes are not causing much damage or the loss and is not that much economical but there is yield reduction and the production cost increases very high when compared to the yield. Nowadays in banana cultivation, tissue culture propagation became a common practice, so, after planting in an orchard, there is rare chance of getting infection of plant parasitic nematodes in the first year. The cultivators also become very aware about the monitoring and testing the soils before planting and after planting every year. After getting tested from the designated authorities, they follow the recommendations given by them. Thus, these producers manage effectively the infestation of nematode problems. But, we have to be very careful and always be ready with some alternative management practices that could be followed if found any severe infection. The need for the management is more necessary in small holding farmers and growers because of their small holding size.

## **Author details**

Nishi Keshari\* and Gurram Mallikarjun Department of Nematology, Dr. Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar, India

\*Address all correspondence to: nishinema@gmail.com

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

## **References**

[1] Anonymous. Citrus Fruit Fresh and Processed Annual Statistics 2002. Rome, Italy: Food and Agriculture Organization of the United Nations; 2002

[2] Ford HW. The influence of rootstock and tree age on root distribution of citrus. Proceedings of the American Society for Horticultural Science. 1954;**63**:137-172

[3] Ford HW. Root distribution in relation to the water table. Proceedings of the Florida State Horticultural Society. 1954;**67**:30-33

[4] Duncan LW. Nematode parasites of citrus. In: Luc M, Sikora RA, Bridge J, editors. Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Wallingford, UK: CAB International; 2005. pp. 437-466

[5] Heald CM, O'Bannon JH. Citrus Declines Caused by Nematodes. V. Slow Decline. Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Nematology Circular No. 143; 1987

[6] Van Gundy SD, Meagher JW. Citrus nematode (*Tylenchulus semipenetrans*) problems worldwide. In: 1977 International Citrus Congress; Orlando, Florida. 1977

[7] Cobb NA. The citrus root knot nematode. Journal of Agricultural Research. 1914;**2**:217-230

[8] Siddiqi MR. Occurrence of the citrus nematode, *Tylenchulus semipenetrans* Cobb, 1913, and the reniform nematode, *Rotylenchulus reniformis* in India (Abstr.). In: Proceedings of 48th Indian Science Congress Part III. 1961. p. 504

[9] Timmer LW, Garnsey SM, Broadbent P. Diseases of citrus. In: Diseases of Tropical Fruit Crops. Wallingford, UK: CAB International; 2003. pp. 163-196

[10] Shokoohi E, Duncan LW. Nematode parasites of citrus. In: Sikora R, Timper P, Coyne D, editors. Plant-Parasitic Nematodes in tropical & Subtropical Agriculture. 3rd ed. St. Albans, UK: CAB International; 2018. pp. 446-476

[11] Abd-Elgawad MMM, Abou-Deif MH, Hammam MMA, Abd-El-Khair H, Koura FFH, Abd El-Wahab AE, et al. Effect of infection with *Tylenchulus semipenetrans* on enzymatic activities in citrus. International Journal of Engineering and Innovative Technology. 2015;**4**(12):43-48

[12] Van Gundy SD. The life history of the citrus nematode, *Tylenchulus semipenetrans* Cobb. Nematologica. 1958;**3**(4):283-294

[13] Duncan LW. Managing nematodes in citrus orchards. In: Ciancio A, Mukerji KG, editors. Integrated Management of Fruit Crops and Forest Nematodes. Springer Netherlands: Springer Science+Business Media B.V; 2009. pp. 135-173. DOI: 10.1007/978- 1-4020-9858-1

[14] Cohn E. The development of the citrus nematode on some of its hosts. Nematologica. 1965;**11**:593-600

[15] Vilardebo A, Luc M. Slow decline of citrus caused by the nematode, *Tylenchulus semipenetrans*. Fruits. 1961;**16**:261-261

[16] Baines RC, Miyakawa T, Cameron JW, Small RH. Infectivity of two biotypes of the citrus nematode on citrus and on some other hosts. Journal of Nematology. 1969;**1**:150-159

[17] Inserra RN, Duncan LW, O'Bannon JH, Fuller SA. Citrus Nematode Biotypes and Resistant Citrus Rootstocks in Florida. Nematology Circular No. 205. Florida Department of Agriculture and Consumer Services, Division of Plant Industry; 1994

[18] Stokes DE. *Andropogon rhizomatus* parasitized by a strain of *Tylenchulus semipenetrans* not parasitic to four citrus rootstocks. Plant Disease Reporter. 1969;**53**:882-885

[19] Thorne G. Principles of Nematology. New York, NY: McGraw-Hill Book Company, Inc.; 1961

[20] Parvatha Reddy P, Singh DB. Evaluating the reaction of some species and varieties of *Citrus* and *Poncirus* to the citrus nematode. Indian Journal of Nematology. 1978;**8**:82-84

[21] El-Mohamedy RSR, Hammam MMA, Abd-El-Kareem F, Abd-Elgawad MMM. Biological soil treatment to control *Fusarium solani* and *Tylenchulus semipenetrans* on sour orange seedlings under greenhouse conditions. International Journal of ChemTech Research. 2016;**9**(7):73-85

[22] Abobatta WF. Citrus varieties in Egypt: An impression. International Research Journal of Applied Sciences. 2019;**1**:63-66

[23] Hammam MMA, El-Mohamedy RSR, Abd-El-Kareem F, Abd-Elgawad MMM. Evaluation of soil amended with bioagents and compost alone or in combination for controlling citrus nematode *Tylenchulus semipenetrans* and fusarium dry root rot on Volkamer lime under greenhouse conditions. International Journal of ChemTech Research. 2016;**9**(7):86-96

[24] Safdar A, Javed N, Khan SA, Safdar H, Haq IU, Abbas H, et al. Synergistic effect of a fungus, *Fusarium semitectum*, and a nematode, *Tylenchulus semipenetrans*, on citrus decline. Pakistan Journal of Zoology. 2013;**45**(3):643-651

[25] Nemec S, Phelps D, Baker R. Effects of dihydrofusarubin and isomarticin from *Fusarium solani* on carbohydrate status and metabolism of rough lemon seedlings. Phytopathology. 1989;**79**(6):700-705

[26] Labuschange N, van der Vegte FA, Koteze J.M. Interaction between *Fusarium solani* and *Tylenchulus semipenetrans* on citrus roots. Phytophylactica. 1989;**21**(1):29-33

[27] Abd-Elgawad MMM, Koura FFH, Montasser SA, Hammam MMA. Distribution and losses of *Tylenchulus semipenetrans* in citrus orchards on reclaimed land in Egypt. Nematology. 2016;**18**:1141-1150. Available from: http://journals.indexcopernicus.com/ EgyptianJournalof Agronematology, p8230,3.html

[28] Abd-Elgawad MMM, McSorley R. Movement of citrus nematode-infested material onto virgin land: Detection, current status and solutions with cost-benefit analysis for Egypt. Egypt Journal of Agronematology. 2009;**7**(1): 35-48

[29] Duncan LW, Graham JH, Timmer LW. Seasonal patterns associated with *Tylenchulus semipenetrans* and *Phytophthora parasitica* in the citrus rhizosphere. Phytopathology. 1993;**83**:573-581

[30] Galeano M. Dinamica di popolazione di *Tylenchulus semipenetrans* e della nematofauna di vita libera nella rizosfera di agrumi in Spagna. Supplemento Nematologia Mediterranea. 2002;**30**: 49-53

[31] Sorribas FJ, Verdejo-Lucas S, Forner JB, Alcaide A, Pons J, Ornat C. Seasonality of *Tylenchulus semipenetrans* Cobb and *Pasteuria* sp. in citrus orchards in Spain. Supplement to the Journal of Nematology. 2000;**32**(4S):622-632

[32] Siddiqui MA, Alam MM. Toxicity of different plant parts of *Tagetes lucida* to plant parasitic nematodes. Indian Journal of Nematology. 1988;**18**:181-185

[33] Park JO, Hargreaves JRE, McConville J, Stirling GR, Ghisal-berti EL, Sivasithamparam K. Production of *Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

leucinostatins and nematicidal activity of Australian isolates of *Paecilomyces lilacinus* (Thom) Samson. Letters in Applied Microbiology. 2004;**38**:271-276

[34] Mclean KL, Dodd SL, Sleight BE, Hill RA, Stewart A. Comparison of the behavior of a transformed hygromycin resistant strain of *Trichoderma viride* with the wild type strain. New Zealand Plant Protection. 2004;**57**:72-76

[35] Ali Ayat M. Control of strawberry fungal diseases under organic agriculture system [Ph.D. thesis]. Egypt: Fac. Agric. Cairo Univ.; 2013. 124 p

[36] Huang XW, Zhao NH, Zhang KQ. Extracellular enzymes serving as virulence factors in nematophagous fungi involved in infection of the host. Research Microbiology. 2005;**115**:811-816

[37] Huang Y, Xu C, Ma L, Zhang K, Duan C, Mo M. Characterization of volatiles produced from Bacillus megateriumYFM3.25 and their nematicidal activity against *Meloidogyne incognita*. European Journal of Plant Pathology. 2009;**26**:417-422

[38] Khan MR, Kounsar K, Hamid A. Effect of certain rhizobacteria and antagonistic fungi on root-knot nodulation and root knot nematode disease of green gram. Nematologia Mediterranea. 2002;**30**(1):85-89

[39] Mahadevan B, Crawford DL. Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzyme and Microbial Technology. 1997;**20**:489-493

[40] Nemec S, Datnoff LE, Strandberg J. Efficacy of biocontrol agents in planting mixes to colonize plant roots and control root diseases of vegetables and citrus. Crop Protection. 1996;**15**:735-742

[41] Dicklow MB, Acosta N, Zuckerman BM. A novel *Streptomyces* species for controlling plant parasitic nematodes. Journal of Chemical Ecology. 1993;**19**:159-173. DOI: 10.1007/ BF00993686

[42] Le Roux HF, Pretorius MC, Huisman L. Citrusnematode IPM in Southern Africa. Proceedings of the International Society of Citriculture. 2000;**2**:823-827

[43] Coley-Smith JR. Some interaction in soil between plants, sclerotium forming fungi and other microorganisms. In: Friend J, Threlfall DR, editors. Biochemical aspects of Plant Parasite Relationships. London, New York, San Fracisco: Academic Press; 1976. pp. 11-23

[44] Giannakou IO, Karpouzas DG, Anastasiades I, Tsiropoulos NG, Georgiadou A. Factors affecting the efficacy of non-fumigant nematicides for controlling root-knot nematodes. Pest Management Science. 2005;**61**:961-972

[45] Le Roux HF, Ware AB, Pretorius MC. Comparative efficacy of preplant fumigation and postplant chemical treatment of replant citrus trees in orchards infested with *Tylenchulus semipenetrans*. Plant Disease. 1998;**82**:1323-1327

[46] O'Bannon JH, Tarjan AC. Preplant fumigation forcitrus nematode control in Florida. Journal of Nematology. 1973;**5**:88-95

[47] Reynolds HW, O'Bannon JH. Factors influencing the citrus nematode and its control on citrus replants in Arizona. Nematologica. 1963;**9**:337-340

[48] Sorribas FJ, Verdejo-Lucas S, Galeano M, Pastor J, Or-nat C. Effect of 1,3-dichloropropene and rootstocks alone and incombination on *Tylenchulus semipenetrans* and citrus tree growth in areplant management program. Nematropica. 2003;**34**:149-158

[49] Davis RM, Heald CM, Timmer LW. Chemical control of the citrus nematode on grapefruit. Journal of the Rio GrandeValley Horticultural Society. 1982;**35**:59-61

[50] Van Gundy S, Garabedian S, Nigh EL. Alternatives to DBCP for citrus nematode control. Proceedings of the International Society of Citriculture. 1982;**1**:387-390

[51] Wheaton TA, Childers CC, Timmer LW, Duncan LW, Nikdel S. Effects of aldicarb on yield, fruit quality, and tree condition on Florida citrus. Proceedings of the Florida State Horticultural Society. 1985;**98**:6-10

[52] Le Roux HF, Ware AB. Accelerated degradation ofsome soil-applied nematicides in a South African citrus orchard. Pro-ceedings International Society of Citriculture. 1996;**1**:593-596

[53] McClure MA, Schmitt ME. Control of citrus nema-tode, *Tylenchulus semipenetrans*, with cadusafos. Supplement to Journal of Nematology. 1996;**28**:624-628

[54] Philis J. Effect of citrus nematode control on the yield and fruit quality of grapefruit in Cyprus. Miscellaneous Report. 1997;**66**:3-6

[55] Walker GE, Morey BG. Effects of chemicals andmicrobial antagonists on nematodes and fungal pathogens of citrus roots. Australian Journal of Experimental Agriculture. 1999;**39**: 629-637

[56] Galeano M, Verdejo-Lucans S, Sorribas FJ, Ornat C, Forner JB, Alcaide A. New citrus selections from Cleopatra mandarin x *Poncirus trifoliate* with resistance to *Tylenchulus semipenetrans* Cobb. Nematology. 2003;**5**:227-234

[57] Kaplan DT. Characterization of citrus rootstock responses to *Tylenchulus semipenetrans* (Cobb). Journal of Nematology. 1981;**13**:492-498

[58] Ling P, Duncan LW, Deng Z, Dunn D, Hu X, Huang S, et al. Inheritance of citrus nematode resistance and its linkage with molecular markers. Theoretical Applied Genetics. 2000;**100**:1010-1017

[59] Lee RF, Lehman PS, Navarro L. Nursery practices and certification programs for budwood and rootstocks. In: Citrus Health Management. St. Paul, MN: APS Press; 1999. pp. 35-46

[60] Edwards M. Resistance and tolerance of grapevine rootstocks to plant-parasitic nematodes in vineyards in North-East Victoria. Australian Journal of Experimental Agriculture. 1989;**29**:129-131

[61] Duncan LW, Inserra RN, O'Bannon JH, El-Morshedy MM. Reproduction of a Florida population of *Tylenchulus semipenetrans* on resistant citrus rootstocks. Plant Disease. 1994;**78**:1067-1071

[62] Lehman PS. Role of plant protection organizations in nematode management. XIX Congress of Brazilian Society of Nematology; Rio Quente, Brazil; 1996. pp. 137-148

[63] Cronjé C, Le Roux HF, Truter M, Van Heerden I, Phillips H. Long-term effect of preplant soil solarisation on growth of replant citrus trees in South Africa. African Plant Protection. 2002;**8**:41-49

[64] Stapleton JJ, Elmore CL, DeVay JE. Solarization and biofumigation help disinfest soil. California Agriculture. 2000;**54**:42-45

[65] Tjamos EC, Grinstein A, Gamliel A. Disinfestation of soil and growth media. In: Albajes R, Gullino ML, van Lenteren JC, Elad Y, editors. Integrated Pest and Disease Management in Greenhouse Crops. Dordrecht, The Netherlands: Kluwer Academic; 1999. pp. 139-149

*Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

[66] Baines RC, Klotz LJ, Clarke OF, DeWolfe TA. Hot water treatment of orange trees for eradication of citrus nematode. California Citrograph. 1949;**34**:482-484

[67] Silva HP, Montero AR, Feraz LCCB. Trata-mento hidrote ́rmico de mudas de cı ́tricos para a erradicaçãode *Tylenchulus semipenetrans*. Nematologia Brasileira. 1987;**11**:143-152

[68] Ibrahim IKA, Mokbel AA, Handoo ZA. Current status of phytoparasitic nematodes and their host plants in Egypt. Nematropica. 2010;**40**: 239-262

[69] Inserra RN, Duncan LW, Troccoli A, Dunn D, Maia SosSantos J, Vovlas N. *Pratylenchus jaehni* sp. n. from citrus in Brazil and a redescription of *P. coffeae*. Nematology. 2001;**3**:653-665

[70] O'Bannon JH, Tomerlin AT. Population studies on two species of *Pratylenchus* on citrus. Journal of Nematology. 1969;**1**:299-300

[71] O'Bannon JH, Tomerlin AT. Citrus tree decline caused by *Pratylenchus coffeae*. Journal of Nematology. 1973;**5**:311-316

[72] De Campos AS, dos Santos JM, Duncan LW. Nematodes of citrus in open nurseries and orchards in Sao Paulo State, Brazil. Nematology. 2002;**4**:263-264

[73] Tomerlin AT, O'Bannon JH. Effect of *Radopholus similis* and *Pratylenchus brachyurus* on citrus seedlings in three soils. Soil and Crop Science Society of Florida Proceedings. 1974;**33**:95-97

[74] Inserra RN, Vovlas N. Effects of *Pratylenchus vulnus* on the growth of sour orange. Journal of Nematology. 1977;**9**:154-157

[75] Siddiqi MR. Studies on nematode root rot of citrus in Uttar Pradesh, India. Proceedings of Zoological society, Calcutta. 1964;**17**:67-75

[76] Radewald JD, O'Bannon JH, Tomerlin AT. Anatomical studies of *Citrus jambhiri* roots infected by *Pratylenchus coffeae*. Journal of Nematology. 1971;**3**: 409-416

[77] Baghel PPS, Bhatti DS. Evaluation of pesticides for the control of phytonematodes on citrus. In: Third Nematology Symposium. Solan: Himachal Pradesh Agricultural University; 1983. pp. 38-39

[78] Van Gundy SD, Thomason IJ, Rackham RL. The reaction of three *Citrus* spp*.* to three *Meloidogyne* spp. Plant Disease Reporter. 1959;**43**:970-971

[79] Whitehead AG. Taxonomy of *Meloidogyne* (Nematoda: Heteroderidae) with descriptions of four new species. Transactions of the Zoological Society of London. 1968;**31**:263-401

[80] Patel D, Patel BA, Patel SK, Patel RL, Patel RG. Root knot nematode, *Meloidogyne indica* on kagzi lime in North Gujarat. Indian Journal of Nematology. 1999;**29**:185-205

[81] Lazan H, Ali ZM. Guava. In: Shaw PE, Chan HT Jr, Nagy S, editors. Tropical and Subtropical Fruits. Auburndale, Florida: AgScience, Inc.; 1998. pp. 446-485

[82] Khan RM, Kumar S, Reddy PP. Role of plant parasitic nematode(s) and fungi in guava wilt. Pest Management in Horticultural Ecosystems. 2001;**7**:152-161

[83] Mahto Y, Edward JC. Studies on pathogenicity, host parasite relationship and histopathological changes of some important fruit trees due to predominant phytonematode associated with them (Part 1). Allahabad Farmer. 1979;**50**:403

[84] Nigam K, Verma RS, Verma AK, Sinha V. Pathogenicity of Hoplolaimus spp. Daday, 1905 to guava (*Psidium gujava*). Advances in Agricultural Research in India. 1995;**3**:158-160

[85] Abivardi C. A stylet nematode, *Tylenchorhynchus cylindricus* Cobb 1913, infesting the common guava, *Psidium guajava* L. in Iran. Nematologia Mediterranea. 1973;**1**:139-140

[86] Mokbel AA. Nematodes and their associated host plants cultivated in Jazanprovince, Southwest Saudi Arabia. Egyptian Journal of Experimental Biology (Zoology). 2014;**10**:35-39

[87] Gomes VM, Souza RM, Silva MM, Dolinski C. Nutritional status of guava (*Psidium guajava* L.) plants parasitized by *Meloidogyne mayaguensis*. Nematologia Brasileira. 2008;**32**:154-160

[88] Cetintas R, Kaur R, Brito JA, Mendes ML, Nyczepir AP, Dickson DW. Pathogenicity and reproductive potential of *Meloidogyne mayaguensis* and *M. floridensis* compared with three common *Meloidogyne* species. Nematropica. 2007;**37**:21-31

[89] Rao MS. Papaya seedlings colonized by the bio-agents, *Trichoderma harzianum* and *Pseudomonas fluorescens* to control root-knot nematodes. Nematologia Mediterranea. 2007;**35**:199-203

[90] Jindapunnapat K, Chinnasri B, Kwankuae S. Biological control of root knot nematodes (*Meloidogyne enterolobii*) in guava by the fungus, *Trichoderma harzianum*. Journal of Developments in Sustainable Agriculture. 2013;**8**:110-118

[91] Al-Hazmi AS, Dawabah AAM, Al-Nadhari SN. *Verticillium chlamydosporium*, a fungal parasite of the cereal cyst nematode (*Heterodera avenae*) in the Saudifields. In: The 4th International Cereal Nematodes Initiative Workshop. 22-24 Aug., 2013. Beijing: Friendship Hotel; 2013

[92] Rao MS. Effect of combinations of bio-pesticides on the management of nematodes on *Carica papaya* L. Acta Horticulturae. 2010;**1**:459-464

[93] Oka Y. Mechanisms of nematode suppression by organic soilamendments—A review. Applied Soil Ecology. 2010;**44**:101-115

[94] Rodriguez-Kabana R. Organic and inorganic nitrogen amendments to soilas nematode suppressants. Journal of Nematology. 1986;**18**:129-135

[95] Gomes VM, Souza RM, Corrêa FM, Dolinski C. Management of *Meloidogyne mayaguensis* in commercial guava orchards with chemical fertilization and organic amendments. Nematologia Brasileira. 2010;**34**:23-30

[96] Alam MM. In: Nemtol PJ, editor. Effect of Ammonia on the Population of Plant Parasitic Nematodes and Growth of Some Vegetables. Vol. 10. 1992. pp. 133-137

[97] Al-Hazmi AS, Dawabah AAM. Effect of urea and certain NPK fertilizers onthe cereal cyst nematode (*Heterodera avenae*) on wheat. Saudi Journal of Biological Sciences. 2014;**21**:191-196

[98] Al-Hazmi AS, Dawabah AAM, Al-Nadhari SN, Al-Yahya FA. Comparativeefficacy of different approaches to managing *Meloidogyne incognita* on green bean. Saudi Journal of Biological Sciences. 2017;**24**: 149-154

[99] Akhtar M, Malik A. Roles of organic soil amendments and soil organisms inthe biological control of plantparasitic nematodes: A review. Bioresource Technology. 2000;**74**:35-47

[100] McSorley R. Overview of organic amendments for management of plant-parasitic nematodes, with case studies from Florida. Journal of Nematology. 2011;**43**:69-81

[101] Gowen S, Quénéhervé P. Nematode parasites of bananas and plantains. In: Luc M, Sikora RA, Bridge J, editors. Plant Parasitic Nematodes in

#### *Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

Subtropical and Tropical Agriculture. Wallingford: AB International; 2005. pp. 611-643

[102] Kleynhans KPN, Van den Berg E, Swart A. Plant nematodes in South Africa. Plant Protection Research Institute Handbook No 8. Pretoria: Agricultural Research Council–Plant Protection Research Institute; 1996

[103] Jones RK, Milne DL. Nematode pests of bananas. In: Keetch DP, Heyns J, editors. Nematology in Southern Africa. Science Bulletin No. 400. Pretoria: Department of Agriculture and Fisheries; 1982. pp. 30-37

[104] De Jager K, Daneel MS, Desmet M, et al. Pathogenicity and distribution studies to determine threshold levels for nematodes on banana. Banana Growers Association of South Africa. 1999;**3**:72-77

[105] Gowen SR, Queneherve P. Nematode parasites of bananas, plantains and abaca. In: Plant Parasitic Nematodes of Subtropical and Tropical Agriculture. Walligford, UK: CAB International; 1990. pp. 431-460

[106] Daneel MS, De Jager K, Van den Bergh I, et al. Occurrence and pathogenicity of plant-parasitic nematodes on commonly grown banana cultivars in South Africa. Nematropica. 2015;**45**:118-127

[107] Willers P, Daneel MS, De Jager K. Banana. In: Van den Berg MA, De Villiers EA, Joubert PH, editors. Pest and Beneficial Arthropods of Tropical and Non-Citrus Subtropical Crops in South Africa. Nelspruit: Agricultural Research Council–Institute for Tropical and Subtropical Crops; 2001. pp. 34-43

[108] Willers P. Nematologiese navorsing in subtropiese bedrywe. Neltropica Bull. 1998;**299**:12-13

[109] Sher SA. Revision of the Genus *Radopholus* Thome, 1949 (Nematoda, Tylenchoidea). Proceedings of the Helminthological Society of Washington. 1968;**35**:219-237

[110] Marin DH, Sutton TB, Barker KR. Dissemination of bananas in Latin America and the Caribbean and its relationship to the occurrence of *Radopholus similis*. Plant Disease. 1998;**82**:964-974

[111] Milne DL, Kuhne FA. Nematodes attack bananas. Farming in South Africa. 1968;**44**:5-9

[112] Rabie EC. Die invloed van *Meloidogyne javanica* en *M. incognita* op die voorkoms van Valspanamasiekte by piesangs [MSc dissertation]. Pretoria: University of Pretoria; 1991

[113] Jonathan EI, Gajendran G, Manuel WW. Management of *Meloidogyne incognita* and *Helicotylenchus multicinctus* in banana with organic amendments. Nematologia Mediterranea. 2000;**28**:103-105

[114] Kim J, Seo SM, Lee SG, Shin SC, Park IK. Nematicidal activity of plant essential oils and components from coriander *(Coriandrum sativum*), oriental sweetgum (*Liquidambar orientalis*), and valerian (*Valeriana wallichii*) essential oils against pinewood nematode (*Bursaphelenchus xylophilus*). Journal of Agricultural and Food Chemistry. 2008;**56**(16):7316-7320

[115] Seenivasan N. Bio-efficacy of anti-nemic plants against root knot nematode in medicinal coleus. Journal of Eco-Friendly Agriculture. 2011;**6**(1):92-96

[116] Daneel MS, Dillen N, Husselman J, et al. Results of a survey on nematodes of *Musa* in household gardens in South Africa and Swaziland. InfoMusa. 2003;**12**:8-11

[117] Quénéhervé P, Cadet P. Localisation des nematodes dans les rhizomes du

bananier cv Poyo. Revue de Nématologie. 1985;**8**:3-8

[118] De Villiers EA, Daneel MS, Schoeman PS. Pests. In: Robinson JC, De Villiers EA, editors. The Cultivation of Banana. Nelspruit: Ingwe Print; 2007. pp. 194-219

[119] Duchame EP, Birchfield W. Physiologic races of the burrowing nematode. Phytopathology. 1956;**46**: 615-616

[120] Keetch DP. Some host plants of the burrowing eelworm, *Radopholus similis* (Cobb) in Natal. Phytophylactica. 1972;**4**:51-58

[121] Milne DL, Keetch DP. Some observations on the host plant relationships of *Radopholus similis* in Natal. Nematropica. 1976;**6**:13-17

[122] NDA. 2015. Available from: http:// www.nda.agric.za/docs/NPPOZA/ Agricultural%20Pests%20Act.pdf

[123] Loos CA. Eradication of the burrowing nematode, *Radopholus similis*, from bananas. Plant Disease Report. 1961;**45**:457-461

[124] Tarjan AC. Longevity of *Radopholus similis* (Cobb) in host free soil. Nematologica. 1961;**6**:170-175

[125] Stirling GR. Biological Control of Plant Parasitic Nematodes. Progress, Problems and Prospects. Wallingford: CAB International; 1991

[126] Wang K-H, Hooks CRR. Survey of nematodes on banana in Hawaii and methods used for their control. In: CTAHR Cooperative Extension Service PD-69. 7 pp. 2009. Available from: http:// www.ctahr.hawaii.edu/oc/freepubs/pdf/ PD-69.pdf

[127] Daneel MS, De Jager K, Dreyer S. PL Plus is an environmentally friendly nematicide for banana nematodes. Neltropica Bulletin. 1998;**300**:32-34

[128] Van Zyl K. A guide to crop pest management in South Africa. A compendium of acaricides, insecticides, nematicides, molluscicides, avicides and rodenticides. In: A Crop Life Compendium. 1st ed. Pinetown: VR Print; 2013

[129] Mendoza A, Sikora RA, Kiewnick S. Efficacy of *Paecilomyces lilacinus* strain 251 for the control of *Radopholus similis* in banana. Communications in Agricultural and Applied Biological Sciences. 2004;**69**:365-372

[130] Chabrier C, Quénéhervé P. Control of the burrowing nematode (*Radopholus similis* Cobb) on banana, impact of the banana field destruction method on the efficiency of the fallowing fallow. Crop Protection. 2003;**22**:121-127

[131] Wang KH, Sipes BS, Schmitt DP. Suppression of *Rotylenchulus reniformis* by *Crotalaria juncea*, *Brassica napus*, and *Target erecta*. Nematropica. 2001;**31**: 237-251

[132] Zasada IA, Klassen W, Meyer SLF, Codallo M, Abdul-Baki AA. Velvetbean (*Mucuna pruriens*) extracts: Impact on *Meloidogyne incognita* survival and on *Lycopersicon esculentum* and *Lactuca sativa* germination and growth. Pest Management Science. 2006;**62**:1122-1127

[133] Widmer TL, Abawi GS. Mechanism of suppression of *Meloidogyne hapla* and its damage by a green manure of Sudan grass. Plant Disease. 2000;**84**:562-568

[134] Ploeg AT, Maris PC. Effect of temperature on suppression of *Meloidogyne incognita* by *Tagetes* cultivars. Journal of Nematology. 1999;**31**:709-714

[135] Keetch DP, Reynolds RE, Mitchell JA. An evaluation of pre- and post–plant nematicides for the control of plant parasitic nematodes on bananas. Citrus and Subtropical Fruits Journal. 1976;**506**:5-7

*Plant Parasitic Nematodes: A Major Constraint in Fruit Production DOI: http://dx.doi.org/10.5772/intechopen.101696*

[136] Sikora RA, Schuster RP. Novel approaches to nematode IPM. In: Frison EA, Gold CS, Karamura EB, Sikora RA, editors. Mobilizing IPM for Sustainable Banana Production in Africa. Montpellier, France: INIBAP; 1998. pp. 127-136

[137] Felde AZ, Pocasangre L, Sikora R. The potential use of microbial communities inside suppressive banana plants to increase root health and suppression of the burrowing nematode, *Radopholus similis*. In: Proceeding of the International Symposium—Banana Root Systems, Towards a Better Understanding for its Productive Management; 3-5 November 2003; Costa Rica. Corbana– INIBAP; 2004

[138] Niere B, Gold CS, Coyne D. Can fungal endophytes control soilborne pests in banana? In: Sikora RA, Gowen S, Hauschild R, Kiewnick S, editors. Multitrophic Interactions in Soil and Integrated Control, IOBC/WPRS Bulletin. Vol. 27. 2004. pp. 203-210

## **Chapter 5**
