Biodiversity of soil nematodes and their role in agriculture
Authors: Zakaullah Khan and Bharat H. Gawade
ICAR-National Bureau of Plant Genetic Resources, Pusa Camus, New Delhi 110012

Nematodes are microscopic, wormlike organisms and are one of the most abundant metazoans in soil; their population densities in soil may reach 10 millions of individuals per m². Nematodes can be classified into functional groups based on their feeding habits. In agricultural soils, the most common groups of nematodes are the bacterial-feeders, fungal-feeders, plant parasites, predators and omnivores. All these types of nematodes coexist in soil and contrary to their notorious image as hidden enemies of farmers; some nematode trophic groups play an important role in organic matter decomposition, mineral and nutrient cycling, and control of pests and diseases. They are excellent indicators of pollution, and metazoan models for basic studies in developmental biology, neurobiology, genetics, and aging, and for understanding the effects of nutrients on reproduction, development, and growth.

Role of nematodes in insects and slug control

Many species of nematodes are pathogenic to invertebrates and species from more than 30 families are pathogenic to insects. (Kaya, 1993).

Mermithidae:
Mermithids are large nematodes (1-30 cm long) that parasitize many invertebrate species including insects. The life cycle of a mermithid nematode starts with emergence of second stage juvenile (pre-parasite), which penetrates the host through the cuticle and enters into the haemocoel for nutrition. The insect host dies due to damage caused by the nematode. The death of the insect occurs due to exit hole made by the nematode. The post-parasitic stage enters soil or water where it matures, mates, and the female oviposits to complete the life cycle. The mermithid nematode, Romanomermis culicivorax, was once mass produced and sold commercially in 1970s for control of mosquitoes. However, the commercial success was short-lived. Filipjevimermis leipsandra, a parthenogenetic species, is another excellent biocontrol agent, which has been tested against Diabotrica balteata. In China, Ovamermis sinensis was successfully used for the control of Mythimna separata. The incidence of mermithid nematode parasitism on insects is observed frequently in moist and moderate temperature conditions such as in some rice (Oryza sativa)-growing regions. In rice fields, natural mermithid infection up to 12% has been reported on rice planthopper.

Steinernematidae and Heterorhabditidae:
The nematode species in these families are uniquely associated with symbiotic bacteria (Xenorhabdus sp and Photorhabdus sp) which cause septicemic death of the insects when carried by the nematodes into insect haemocoel. These nematodes have been successfully developed as biocontrol agents of insects, particularly of those living in soil and cryptic habitats. The infective juveniles carry the bacterium (Xenorhabdussp in Steinernema sp and Photorhabdus sp in Heterorhabditis sp) located primarily in the ventricular portion of the intestine (Steinernema sp) or in the intestine lumen (Heterorhabditis sp). Once a suitable host is found, the infective juveniles enter the host and release the bacteria in the haemolymph where they propagate and kill the host. Currently, S. carpocapsae, S. feltiae, S. glaseri, S. riobravis, S. scapterisci, Steinernema sp, H. bacteriophora, and H. megidis are available commercially in industrialized countries. These nematodes have a broad host range, are safe to non-targeted organisms, can be easily mass cultured in vitro and easily applied using standard spray equipment, have potential to establish and recycle in environment, are compatible with chemical pesticides, and can be genetically manipulated for desired traits such as host finding. The rice ecosystem is favorable for use of these nematodes for biocontrol of insect pests.

Role of nematodes in plant diseases control

There has been widespread interest in using predatory nematodes to control populations of plant parasitic nematodes (Khan and Kim, 2007; Stirling 2014). Yeates and Wardle (1996) introduced the dual function of predation by nematodes: Potential control of plant parasitic nematodes, and their important role in stimulating cycling of plant nutrients, which may enable plants to better withstand any nematode burden on their roots. The majority of predatory nematodes belong to the orders Mononchida, Dorylaimida, Diplogasterida and Aphelenchida and super families, Actinolaimoidea, Dorylaimoidea, Nygolaimoidea and families Ironidae, Monhysteridae, Oncholaimidae and Thalassogeneridae etc. They feed on soil microorganisms including plant parasitic nematodes.

Several of commonly occurring mononchids feed extensively, though not exclusively, on plant parasitic and other nematodes. They may swallow their prey whole if it is of smaller size, or at times feed by cutting larger prey into pieces. Significant reductions in the population densities of potato cyst nematode, Globodera rostochiensis and root-knot nematode, Meloidogyne incognita in the presence of a mononchid predatory nematode, Prionchulus punctatus, in pot experiments have been reported. True predator-prey relationship existed between plant parasitic nematodes, Tylenchulus semipenetrans and Helicotylenchus dihystera with mononchid predator, Iotonchus tenuicaudatus in mandarin orange orchards. These reports indicated that mononchids are providing natural control of plant parasitic nematodes in soil. If their population can be manipulated in the field then they can be used as successful biocontrol candidates. Dorylaimids possess a hollow stylet, properly called as odontostyle with which they puncture the prey organisms suck food. The detection of a dorylaim predator, Eudorylaimus obtusicaudatus feeding on eggs inside cysts of Heterodera schachtii and an increase in the population of Thornia sp. in the presence of citrus nematodes but a decrease in their absence in pot trials have indicated their biocontrol potential against plant parasitic nematodes. The most advantageous and encouraging aspect of dorylaimids is that it is easy to maintain their populations simply by adding organic matter to agricultural fields. The diplogasterid predators posses a smaller buccal cavity than which armed with a dorsal tooth. They feed on nematodes, bacteria and other soil microorganisms. Diplogasterids are generally found abundantly in decomposing organic manure. They are the most readily cultured nematodes, being easily maintained on simple nutrient media containing bacteria. Fauzia et al. (1998) demonstrated the ability of Mononchoides longicaudatus to reduce root galling by root-knot nematodes in pot tests, resulting in improved vegetative growth and increased root mass. Further Khan and Kim (2005) reported that a pre-planting application of M. fortidens in potted field soil infested with root-knot nematode reduced the root galling on tomato plants and suppressed the nematode population. Bilgrami et al. (2008) have demonstrated that M. gaugleri reduced the population of naturally occurring plant parasitic nematodes in a turf grass field in USA.

The hyphal feeder nematodes' belong to the orders Tylenchida, Dorylaimida, and Aphelenchida. They have weak, hollow stylet for piercing the fungal hyphae and sucking the contents. The feeding habits of these nematodes sometimes protect plants from pathogenic fungi. For example, Aphelenchoides hamatus and A. hylurgi feed on plant pathogenic fungi and damping off disease of cucumber (Cucumis sativus) by Rhizoctonia solani is less severe in the presence of Aphelenchus avenae. In nature, the hyphal feeder nematode may be responsible for significant natural control of fungal pathogens. Like wise, bacterial feeder nematodes may reduce soilborne bacterial diseases by lowering the primary bacterial inoculum. Addition of organic matter to agricultural soils increases the populations of hyphal and bacterial feeder nematodes (Ishibashi and Kondo, 1986).

Role of nematodes in organic matter decomposition

The soil nematodes, especially bacterial- and fungal-feeding nematodes, can contribute to maintaining adequate levels of plant-available N in farming systems relying on organic sources of fertility (Ferris et al., 1998). The chemotropic bacteria convert the excretory product of nematodes (i.e., ammonia) to nitrate and nitrite compounds. The predominance of bacteriophagus nematodes in agricultural systems indicates faster rate of mineralization, decomposition, and nutrient turn over. Nematodes contribute directly to nutrient mineralization through their feeding interactions. Both bacterivore and fungivore nematodes mineralize N in soil (Ferris et al., 1998), bacterial-feeding nematodes consume N in the form of proteins and other N-containing compounds in bacterial tissues and release excess N in the form of ammonium, which is readily available for plant use. Indirectly, nematodes enhance decomposition and nutrient cycling by grazing and rejuvenating old, inactive bacterial and fungal colonies, and by spreading bacteria and fungi to newly available organic residues. Soil mineral N levels are increased by 20% or more by the feeding of bacterial- and fungal-feeding nematodes in microcosm experiments (Ferris et al., 1998).

Role of nematodes in nutrient cycling

Nitrogen Cycle: It is estimated that 60% of nitrogen ingested by the total nematode community comes from bacteria, 15% from fungi, and 25% from plant roots. The bacteriophagus nematodes and amoeba together account for over 83% of nitrogen mineralization. The nematodes have been related to increased plant production owing to increased nitrogen availability.

Sulfur Cycle: The primary effect of nematodes on sulfur cycling and biogeochemical cycling is through interactions with sulfur-oxidizing bacteria. An efficient anaerobic trophic food web exists near natural oil and petroleum sources. The hydrogen sulfide produced is oxidized by Beggiatoa species of sulfur-reducing bacteria. The bacteriophagus nematodes feed on these bacteria and are the key intermediaries between the bacterial and macrofaunal predation.

Phosphorus Cycle: Increased mineralization of carbon, nitrogen, and phosphorus owing to grazing by free-living nematodes has been studied but the exact mechanisms are not yet known.

The beneficial role of nematodes in agro-ecosystems has not received much attention as of plant parasitic group. But the presence of many groups of beneficial nematodes in to soil is vitally important in soil ecosystem process. The insect parasitic nematodes have been used for controlling the insect pests in industrialized countries but not in the developing countries. Predatory nematodes used to manage plant parasitic nematodes especially in greenhouses and pot cultures. The contributions of nematodes to organic matter decomposition and nutrient recycling, deserve much greater attention of scientific community world wide.

Literature cited

Bilgrami, A.L., Brey, C. and Gaugler, R. (2008). First field release of a predatory nematode, Mononchoides gaugleri (Nematoda: Diplogasterida), to control plant-parasitic nematodes. Nematology 10: 143-146.

Fauzia, J., Jairajpuri, M.S. and Khan, Z. (1998). Biocontrol potential of Mononchoides longicaudatus on Meloidogyne incognita on tomato plants. International Journal of Nematology 8: 89-91.

Ferris, H., Venette, R. C. van der Meulen, H. R. and Lau, S.S. (1998). Nitrogen mineralization by bacterial-feeding nematodes: Verification and measurement. Plant and Soil 203: 159â€"171.

Ishibashi, N. and Kondo, E. (1986). Steinernema feltiae (DD 136) and S. glaseri: Persistence in soil and bark compost and their influence on native nematodes. Journal of Nematology 18:310-336.

Kaya, H.K. (1993). Entomogenous and entomopathogenic nematodes in biological control. Pages 565-591 in Plant parasitic nematodes in temperate agriculture (Evans, K., Trudgill, D.L., and Webster, J.M., eds.). Wallingford, UK: CAB International.

Khan, Z. and Kim, Y.H. (2007). A review on the role of predatory soil nematodes in the biological control of plant parasitic nematodes. Applied Soil Ecology 35: 370-379.

Khan, Z. and Kim, Y.H. (2005). The predatory nematode, Mononchoides fortidense (Nematoda: Diplogasterida), suppresses the root-knot nematode, Meloidogyne arenaria, in potted field soil. Biological Control 35: 78-82.

Stirling, G.R. (2014). Biological control of plant-parasitic nematodes: soil ecosystem management in sustainable agriculture. Wallingford, UK: CAB International, 496 pp.

Yeates, G.W. and Wardle, D.A. (1996). Nematodes as predators and prey: relationships to biological control and soil processes. Pedobiologia 40: 43-50

About Author / Additional Info:
Senior Scientist (Nematology), Division of Plant Quarantine, Indian Council of Agricultural Research (ICAR)-National Bureau of Plant Genetic Resources (NBPGR), Pusa Campus, New Delhi-110012.