Abstract
Biological control can be a safe alternative to detrimental chemical nematicides if its persistence and performance increase to a satisfactory level. But at present, no biocontrol agent (BCA) can provide adequate nematode control when applied alone. One approach to improve their controlling importance is to use them in integration with one or more compatible practices that enhance BCAs’ population, diversity, durability and efficacy. This goal may be achieved by combined use of BCAs with measures aiming at manipulating the soil environment in favour of BCAs, reducing nematode population and enhancing BCAs’ activity. Here a brief outline of some measures for controlling phytonematode is illustrated with extra attention to those that can be applied combinedly with biological control. Their advantages and disadvantages as well as their effects on altering biocontrol activity are demonstrated along with selected examples of each tactic. The reviewed strategies in combination with biocontrol are using host plant resistance (tolerance, resistance and induced resistance); agronomic practices (rotation, trap crops, antagonistic crops, cover crops, fallow, flooding, organic amendments and tillage); decrease in phytonematode populations (soil solarisation, biofumigation and chemical nematicides); and application more than one BCA. Finally, the future paths of integrated nematode management are designed.
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10.1 Introduction
Food production currently suffers an unprecedented pressure due to increase in the global population and inability to feed the world. It seems that the pressure will be exceedingly increased over the coming years when the population projected to reach 9.3 billion in 2050 (FAO, IFAD and WFP 2013). So, the most important challenge for agricultural industry is to provide more food in spite of diminishing fertile land, water supply and energy resources (Godfray et al. 2010; Gomiero et al. 2011; Ansari and Mahmood 2017a; Ansari and Mahmood 2019a, b). More food can be imagined in three main ways: cultivate more land; intensify the frequency of cropping; and increase the harvested yield in a given area. Several studies have evaluated the contribution of these three ways to the increase in universal food production. In a study, the contribution of more harvested yield, cultivation more land and intensified agriculture to enhancement of world food supply during 1960–1999 was estimated as 78%, 15% and 5%, respectively (Bruinsma 2003). One of the most important components of yield improvement is reducing the damage of the pests to agricultural plants. The estimated amount of losses to global agricultural production implies that plant diseases are a problem of great significance. They cause a serious threat to agricultural productivity and sustainability, and may endanger food security (Strange and Scott 2005). Phytonematodes are a group of plant pathogens whose importance is progressively understood in the last few decades. It is estimated that they now impose about 12% loss to global food production (Nicol et al. 2011). However, it should not be forgotten that indigenous phytonematodes in traditional cropping are not normally an agricultural problem. They usually turn into noxious pests in consequence of alteration in the cropping system, agricultural practices, climate, or being introduced to new regions (Sikora et al. 2005). There is a serious need to control the phytonematodes; however, the task is not easy to achieve. Many approaches can be employed to either increase the plant resistance/tolerance to phytonematodes or reduce nematode populations below its economic injury level. The main controlling method is now based on chemical nematicides which should be apparently substituted with other safer methods (Moosavi and Askary 2015). Biological control offers a safe opportunity for nematode control and many organisms have been identified with hostile activity against phytonematodes (Moosavi and Zare 2015). However, it has been recently shown that phytonematodes can defend themselves by producing antimicrobial peptides whose secretion is regulated by the nematode immunity system (Liang et al. 2019). One strategy to improve the general levels of phytonematode biocontrol is to manipulate the environment in favour of resident microbiota so enhanced their diversity and populations. In spite of its great potential, biological control takes little or no part in present phytonematode management programmes (Stirling 2014). This may be partly due to our insufficient understanding about the traits involved in efficacy of biocontrol agents (BCAs) which in turn leads to inconsistency of their effectiveness. It seems that, at least for now, no BCA can provide sufficient nematode control when implemented by itself. Therefore, a successful nematode-biocontrol programme needs more approaches than the application of a BCA (Viaene et al. 2013). Using BCAs in an integrated programme can improve their performance against phytonematodes. The main principle of integrated pest management (IPM) is to decrease the pest population under damage threshold by using an integration of measures. These measures are chosen according to our information about pest and plant biology, environmental factors and ecological principles (Stirling 1999). Decrease in phytonematode damage in an IPM programme can be achieved by practices targeting either reducing nematode population or enhancing BCAs’ activity (Hildalgo-Diaz and Kerry 2008). This chapter tries to illustrate the measures which can be used in integration with BCAs to enhance nematode control.
10.2 Using Host Plant Tolerance/Resistance
Resistant cultivars present an efficient, environmentally safe, persistent and inexpensive tactic for phytonematode control (Koenning et al. 2001; Castagnone-Sereno 2002; Starr et al. 2013) but with one disadvantage that is effective only when the soil is infested with one (important) species (Hildalgo-Diaz and Kerry 2008). This restriction is because of specificity in resistance which acts against one species of phytonematodes or even more specifically against one race of a species without any effect on other existing parasitic species (Roberts 2002). Therefore, a number of researchers believe that resistance could not be a worldwide solution to phytonematode management. Tolerant cultivars are able to endure severe pathogen infection and produce an acceptable yield (Agrios 2005). The tolerant host plants do not restrict the development of phytonematodes, so their population densities increase during growing season but the yield does not remarkably reduce (Dalmasso et al. 1992). The extent of yield loss corresponds to phytonematode initial population densities (Sikora et al. 2005). Integration of host plant tolerance or resistance with other controlling measures such as biological control could positively increase the efficacy of nematode management.
10.2.1 Host Plant Tolerance
Planting tolerant hosts in combination with BCAs makes the controlling programme of phytonematodes more efficient. The tolerant host could produce acceptable yield while robust BCAs reduce nematode populations. This will decrease the residual nematode population density in soil and consequently the initial nematode population for the next successive crop. On the other hand, decline in females’ fecundity on tolerant host might delay the occurrence or selection of virulent nematode species or pathotypes (Hildalgo-Diaz and Kerry 2008; Ansari and Khan 2012a, b). Obligate parasites of phytonematodes have better efficacy on tolerant cultivars than on resistant ones. Contrary to resistant plants, the population density of nematode which supports the establishment and multiplication of obligate parasites is higher on tolerant plants. For example, densities in soil and parasitising abilities of Nematophthora gynophila on cereal and sugar beet cyst nematode increased when the tolerant host of each nematode was cultivated successively (Kerry 1987). Soil suppressiveness to cereal cyst nematodes in monocultures in Western Europe may occur because of concomitant presence of fungal BCAs and partial resistance (Cook and Starr 2006). Suitable integration of tolerant cultivars of sugar beet with facultative parasites of nematode, short crop rotation and nematicide increased the efficacy of the BCAs as well. Concomitant use of mentioned measures could successfully control the first generation of sugar beet nematode (Heterodera schachtii) with Pochonia chlamydosporia and the second generation with Cylindrocarpon destructans (Crump 1989, 1991).
10.2.2 Host Plant Resistance
Resistance can be generated either by selecting plants with natural resistance gene(s) or by inserting new resistance gene into proper crops (Davies and Elling 2015). Several approaches are usually used for engineering resistance including expression of the inserted natural resistance genes in transgenic plants; aiming at and disruption of the initial nematode–plant interaction; aiming directly at the nematode (Bt & Cry proteins, plantibodies, lectins, protease inhibitors and RNA interference); and interfere with feeding site formation (Cottage and Urwin 2013). A number of major resistant (R) genes with the ability of conferring resistance to sedentary endoparasitic nematodes have been either cloned or mapped from agronomic or wild plants (Davies and Elling 2015). Resistance to phytonematodes may be provided by dominant, recessive, co-dominant R genes or by quantitative trait loci (Molinari 2011). Most of the R genes that have been already identified are translated to resistant proteins with a similar structure. These proteins consist of a central nucleotide-binding site (NBS) and a C-terminal leucine-rich repeat (LRR) region (Kaloshian et al. 2011). Resistant high-yielding crops offer an idle basis upon which further controlling tactics can be built (Sikora et al. 2005). Since resistance is considered as a major method for nematode management, a few researches have examined the combined effect of host resistance and BCAs. Despite scarce references, it seems that application of BCAs on resistant plants resulted in better nematode management. However, it must be taken into consideration that continuous planting of resistant cultivars often resulted in development and establishment of nematode races which could feed and colonise those resistant plants. Application of Hirsutella rhossiliensis on a resistant cultivar of potato to Pratylenchus penetrans produced synergistic effect and better nematode control was achieved compared with when each treatment was used alone (Timper and Brodie 1994).
10.2.3 Induction of Host Plant Resistance
Host plants could defend against pathogen infection through a number of different constitutive, induced and systemic defence mechanisms (Walters 2011). Induction of plant immunity system is a fascinating method for controlling phytonematodes (Leadbeater and Staub 2014; Alesadi et al. 2017). The symbiotic fungi-mediated resistance, systemic acquired resistance, induced systemic resistance, and β-aminobutyric acid-induced resistance are the suggested methods for controlling the pathogenic nematodes (Bakker et al. 2006). Plant hormones or their derivatives are considered as defence inducer molecules which could trigger the inducible defence mechanisms. Salicylic acid, jasmonic acid and ethylene are the most famous defence inducers (Conrath 2011; Takur and Sohal 2013), However, it has been illustrated that other hormones like auxins, abscisic acid, cytokinins, gibberellins and brassinosteroids have regulatory role on plant defence (Denancé et al. 2013; Moosavi 2017). Plant defences are induced by nematode attack but can also be started by exogenous application of defence inducers. Application of these molecules may decrease phytonematode invasion, development and reproduction. BCAs may control the pathogens by direct or indirect mechanisms. It has been frequently reported that BCAs can indirectly antagonise the pathogens by improving plant photosynthetic and respiratory activities (Shoresh et al. 2010) or by inducing the host plant resistance (Walters and Bennett 2014). It has been reported that endophytic fungi (non-pathogenic Fusarium oxysporum) could stimulate defence mechanisms in tolerant cultivars of bananas against Radopholus similis (Paparu et al. 2007). Similarly, P. chlamydosporia induced zucchini defence responses to Meloidogyne javanica (Lalezar et al. 2016). It has been also reported that induced resistance to nematode by BCAs is inheritable. For example, Trichoderma atroviride could stimulate tomato resistance against M. javanica which could be inherited to tomato progeny (de Medeiros et al. 2017). The combined application of BCA and defence inducer molecules will satisfactorily control the nematode while defence inducer molecule prevents initial nematode damage and the BCA provides long-term protection (Moosavi and Ghani 2019). Soil application of P. chlamydosporia in combination with foliar sprays of benzothiadiazole (BTH) or cis-jasmone reduces Meloidogyne chitwoodi reproduction on potato. The number of eggs per egg mass was lesser and the proportion of parasitised eggs was greater in plants treated with both the defence activators and the fungus than in the plants treated only with one of the treatments (Vieira Dos Santos et al. 2014). Conversely, integrated use of P. chlamydosporia with spraying tomato plants with methyl jasmonate, acibenzolar-S-methyl or ethephon reduced the ability of the fungus to lessen the gall number of M. javanica or activate local induced resistance (de Medeiros et al. 2015). Applying salicylic acid as a defence inducer and Arthrobotrys oligospora as a BCA against M. javanica considerably decreased diameter of nematode galls, number of galls per plant, number of egg masses per plant and number of eggs per egg mass, but their simultaneous application reduced these indices to a greater extent (Mostafanezhad et al. 2014).
10.3 Agronomic Practices
Agronomic practices have been among the most important concepts in managing phytonematodes for a long time. The involved mechanisms for nematode suppression are starvation, entrapping, antagonism, induction of soil antagonistic activity and/or biofumigation (Sikora et al. 2005). Biological control and agronomic measures can synergistically contribute in management of phytonematodes. Here a concised outline of some cultural-based tactics for controlling phytonematode is presented with emphasis on those that can be implemented integratedly with biological control. Their advantages and disadvantages along with selected examples of each tactic are included.
10.3.1 Rotation
The oldest and one of the most operational measures to manage phytonematodes is crop rotation. Succession of the crops can be temporal or spatial. Rotation of susceptible plants with non-host or poor-host provides adequate time after each susceptible host to decrease nematode population under the level which allows the next crop to grow and yield acceptably (Trivedi and Barker 1986). A crop rotation system can be successful only when resistant or tolerant plants are available for cultivation in the target agricultural systems. The host range of parasitic nematodes must also be considered for devising a practical rotational programme. Choosing a proper host plant is so difficult when the host range of the target nematode is an extensive one. Differences in host resistance to various populations of a species are another problem. However, the presence of multiple or polyphagous species of phytonematodes in a given soil restricts the ability of selecting appropriate plants for rotation (Viaene et al. 2013). When multiple species exist in soil, a non-host plant for one species might possibly be a proper host for the non-target species. Despite its deceptive simplicity, devising a specific crop rotation system for controlling phytonematodes needs much knowledge. The nematode population density is to same degree under the influence of both individual crops and their sequence in time and space (Trivedi and Barker 1986). As well, the BCA population is also affected by different plant species. Therefore, more reduction in nematode population will occur if poor or non-host plant for nematode can support the growth of BCAs (Timper 2014). Various plants secrete different root diffusates which are effective on soil and rhizosphere microbial construction. However, our knowledge about the effect of root diffusates on the performance of BCAs is so limited (Viaene et al. 2013). The needed time span between susceptible hosts or the needed number of rotational plants may be varied in relation to many factors. To recommend a rotational scheme we first need information about species, race and the host range of the local nematodes in a particular region. The host status of different crop cultivars and weeds must be determined. An understanding of nematode (species and/or races) population dynamics on different crops, relationship of nematode populations to crop loss and the environmental effect on the population of nematodes and BCAs is also vital in developing efficient rotation schemes. The attenuation of nematode population densities during rotation differs significantly with the time, place, pathogens, weed hosts, and the nature and length of the rotation (Kratochvil et al. 2004; Viaene et al. 2013). A two- to four-year rotation programme of cultivating non-host plants usually resulted in acceptable management of economically important phytonematodes (Trivedi and Barker 1986). However, rotation is not useful where a large spectrum of nematode species exists and no rotation scheme can adequately control a wide range of nematode species on different plants (Barker 1991). On the other hand, nematode population decline in consequence of cultivating non-host plants for a long time may be detrimental to BCAs especially for obligate ones (Timper 2011; Stirling 2014). Combining rotation with biological control could reciprocally improve efficacy of both tactics when non- or poor-host rotating plants reduce nematode population densities to levels that prevent or lessen initial infection of successive susceptible host. Then application of BCAs in an augmentation or inundation strategy manages the phytonematode during the cultivation of susceptible host. Otherwise the rotation plants must be carefully selected to support the survival of the existent BCAs and therefore to maintain phytonematode suppression. There are contradictory results about the survival and maintenance of BCAs during rotation programme that emphasise on our inadequate knowledge about interactional, ecological and environmental factors which impact on BCAs’ potency. It has been demonstrated that parasitism ability of H. rhossiliensis on motile phytonematodes depended on nematode population density (Jaffee et al. 1992). Planting susceptible cultivars of soybean to Heterodera glycines resulted in more parasitised juveniles (Chen and Reese 1999). But when maize- or soybean-resistant cultivars were cultivated in rotation with susceptible cultivar, the proportion of infected juveniles decreased (Chen and Liu 2007). Planting switchgrass (Panicum virgatum) in rotation with peanut for controlling Meloidogyne arenaria caused shifting in rhizosphere bacterial diversity. The shifts in bacterial community structure were connected to fluctuations in phytonematode populations (Kokalis-Burelle et al. 2002). In another experiment, P. chlamydosporia was applied to a field with high populations of M. incognita, and then bean and cabbage (poor-hosts for the nematode) were cultivated prior to tomato (susceptible host). The population densities of M. incognita declined considerably during rotation period. But when tomato was again planted in the field, the nematode population density increased only in control treatment and remained low in plots where P. chlamydosporia was used several months earlier. This showed that the fungus population maintained at sufficient levels during rotation that could adequately control the nematode on tomato (Atkins et al. 2003). Maize, bean and cabbage are good choice for rotation programme where M. incognita is the main pest. These crops are poor hosts for the nematode while P. chlamydosporia could grow well in their rhizosphere (Puertas and Hidalgo-Díaz 2007). Contrasting to P. chlamydosporia, the efficiency of Purpureocillium lilacinum is less affected by the host plant. So, P. lilacinum persistence in soil is not related to particular rotation schemes. Among 12 plant species, the decline of fungus population was seen only when Phaseolus vulgaris was planted (Rumbos and Kiewnick 2006). The nematode antagonistic bacteria or fungi with endophytic life style depend on their exclusive hosts on which they can endophytically establish and develop. Therefore, certain crop rotation system could support their survival (Hildalgo-Diaz and Kerry 2008). The host plants can evidently affect the abundance of BCAs through root exudates and other plant characteristics (Timper 2014). Higher populations of BCAs could support host plants against soilborne pathogens (Weller et al. 2012). Therefore, continuous cultivation of a plant species may sometimes resulted in a selective enhancement in population densities of particular BCAs and the formation of suppressive soils (Stirling 1988), but it is not surely evidenced that crop rotation always annihilates suppressiveness in a soil (Timper 2014).
It is too hard to correlate the general suppression of phytonematodes in soil to any specific BCA. However, choosing the appropriate plants for rotation has undeniable effect on preserving nematode suppression by BCAs. Suppressiveness to Heterodera schachtii was endangered when wheat was cultivated in a soil but not when an H. schachtii-resistant sugar beet was planted. It was assumed that the BCAs could colonise and reproduce in the rhizospheric soil of resistant sugar beet rather than wheat (Westphal and Becker 2001).
The performance of P. chlamydosporia in a double-cropping system of lettuce and tomato was examined in soil infested with M. javanica for two successive growing seasons. The fungus was detected from M. javanica eggs up to 9 months after application to soil and survived at low densities in the rhizospheric soil for the entire growing season (Verdejo-Lucas et al. 2003). The efficacy of P. chlamydosporia in reducing M. javanica population densities or enhancing yield was different when it was applied in two different cropping systems. Cropping system I included eggplant–okra–tomato–okra–eggplant–tomato–okra while cropping system II composed of eggplant–broad bean–tomato–broad bean–cabbage–tomato–cabbage. Both the nematode population density and yield in cropping system II decreased respectively by 12 and 65% than in cropping system I (Amer-Zareen et al. 2004). The proportion of involvement in nematode decline was different among various cropping systems. During a two-year crop rotation in the absence of potato plants, between 76 and 80% of the Globodera rostochiensis decline occurred in relation to spontaneous hatch while only 10% was due to bacterial BCAs (Devine et al. 1999). But when Purpureocillium sp. (=Paecilimyces sp.) was applied against G. rostochiensis in combination with two different legominous plant, the proportion of Purpureocillium involvement in G. rostochiensis decline was more than rotation. When the fungus was applied in combination with two different legominous plants, 89% of nematode population reduced but the decline percent for rotation alone was 31% (López-Lima et al. 2013). There was meaningful difference among various plants (oilseed rape, sugarbeet and wheat in the potato rotation) in supporting the survival or abundance of P. lilacinum, Monographella cucumerina and P. chlamydosporia var. chlamydosporia and P. chlamydosporia var. catenulata (Manzanilla-López et al. 2011).
10.3.2 Trap Crops
Usually, sedentary endoparasitic nematodes are the target of trap cropping. The concept of this tactic involves planting a susceptible host with fast and extensive root growth in a nematode-infested soil during a short period of time (Sikora et al. 2005). The motile juveniles of sedentary nematodes invade the roots and soon start their development to sedentary growth stage. Thereafter, the non-motile juveniles are annihilated via destruction of trap crop with herbicide, ploughed in, or physical removal before the juveniles could complete their life cycle and reproduce (Viaene et al. 2013). A crop trap is considered as an idle one if it stimulates the nematode eggs to hatch, be very attractive to juveniles, being heavily infected but not supporting nematode reproduction (Trivedi and Barker 1986). The trap crop should be cultivated quite densely in infested soil so that root system and/or its diffusates can contact as many juveniles as possible. The success of this tactic depends on appropriate cultivation methods, accurate timing and complete destruction of the crop when it is a susceptible one (Viaene et al. 2013). Though proper implementation of trap cropping can be an extremely helpful measure for phytonematode management, it has not been welcomed by the farmers due to the time and cost involved. I found only one literature in which trap cropping was used in combination with BCAs. Dandurand and Knudsen (2016) applied Solanum sisymbriifolium as a trap crop against Globodera pallida alone or together with Trichoderma harzianum or Plectosphaerella cucumerina. Soil of three different ‘cropping systems’ including potato (Solanum tuberosum), S. sisymbriifolium, or soil only (fallow) was amended with P. cucumerina, T. harzianum or left unamended. The trap crop S. sisymbriifolium significantly decreased nematode reproduction rate by 99% with or without BCAs assistance. Since the outcome of S. sisymbriifolium on reproduction rate of the nematode was large, addition of the BCAs made no further reduction.
10.3.3 Antagonistic Crops
These plants usually could produce detrimental compounds which have antagonistic effects on phytonematodes. The antagonistic substances may be secreted when the roots are growing or be released after biodegradation in the soil (Hildalgo-Diaz and Kerry 2008). Non-host status of antagonistic crops for some phytonematode species is another mechanism for control (Viaene et al. 2013). Phytonematodes do not usually invade the roots of antagonistic plant, but if penetration occurs, little progress is seen in their life cycle (Trivedi and Barker 1986). The most famous antagonistic plants are marigold, neem, sunn hemp, castorbean, partridge pea, asparagus, rape seed, velvet bean, some grass species (family Poaceae) and sesame (Grubišić et al. 2018). The application of this approach may practically be achieved by pre-plant cover crops, intercropping or green manures (Viaene et al. 2013). The antagonistic crops that could make money have greater potential to be accepted by the growers. Acceptability and application of Tagetes spp. have been greatly increased when food industry began to use them as a food colourant (Hooks et al. 2010). Cultivation of antagonistic plants may offer a substitute for chemical nematicides if integrated with other measures such as BCAs. However, few researches have studied the combined effect of antagonistic plants and biological control on phytonematodes. Forty-nine species of endophytic bacteria were recovered from Tagetis erecta and Tagetis patula, of those Microbacterium esteraromaticum (recovered from T. patula) and Kocuria varians (recovered from T. erecta) significantly reduced the population density of Pratylenchus penetrans in the potato rhizosphere without decreasing the tuber fresh weight (Sturz and Kimpinski 2004). There are also reports on the adverse effect of marigolds on useful microorganisms. It was suggested that antifungal molecules were present in fresh marigold tissue (Baker 1981) and Owino (1992) demonstrated that extracts of T. patula could prevent Fusarium solani and F. oxysporum to prarasitise M. javanica and M. incognita eggs on water agar. Therefore, it is feasible to use antagonistic plants in combination with augmented releases of BCAs to enhance phytonematode suppression but this needs more investigation.
10.3.4 Cover Crops
Cover crops refer to plants that are not cultivated for their commercial value but for management of phytonematodes, suppression of weed growth and soil conservation throughout the off season (winter or dry period). Noteworthy, little or no nematode control might be obtained if off season overlaps with nematode low activity or over-seasoning period. The cover crops may finally be incorporated to soil as a green manure or utilised for livestock fodder. Cover crops decrease nematode population densities simply by their non-host status or by their antagonistic, suppressive or damaging properties (Sikora et al. 2005; Viaene et al. 2013). Incorporating the cover crops into the soil usually leads to considerable enhancement in BCAs activity and increase in the host plant growth. Cover crops have the potency to regulate soil microbial structure and ecosystem services (DuPont et al. 2009).
Applying P. chlamydosporia simultaneously with planting cover crop had interesting results. The population densities of P. chlamydosporia increased in soil where black oat or oil radish was cultivated, but decreased in fallow soil or in soil where tomato was planted. Despite increase in population, the fungus fails to efficiently control M. javanica on tomato plant that is being cultivated after either black oats or oil radish. Contradictorily, galling and egg production of the nematode decreased when tomato plants were cultivated after fallow or tomato (Dallemole-Giaretta et al. 2011). In another approach used in warm climate, organic mulch is prepared from intact remainder of the cover plants which provide several advantages than when residues are incorporated into soil. Cover mulch can enhance BCAs activity by supplying a carbon resource, and by preventing excessive changes in soil temperature and moisture. The population densities of nematophagous bacteria were increased when sunn hemp is used as organic mulch (Wang et al. 2008). Leaving sugarcane residues on soil resulted in greater suppressiveness to M. javanica and Pratylenchus zeae than adding the residue into soil (Stirling et al. 2011).
10.3.5 Fallow and Flooding
Fallow is a simple tactic in which no crop is planted in a varying period of time, but no measure is employed against weed growth. ‘Clean fallow’ or ‘black fallow’ refers to a period of time when no plants (including weeds) are permitted to grow on farm by using herbicide or frequent tillage (Viaene et al. 2013). The phytonematode controlling strategy in fallow is to reduce populations by starvation, while desiccation and exposure to heat emanated from sun may assist (Trivedi and Barker 1986). Fallow has many problems which make it an unpractical method in many countries. The adverse effect on soil conservation via erosion; no contribution to farm income, being less-effective or ineffective in dry weathers, and no or low controlling impact on cyst or some lesion nematodes (like Pratylenchus brachyurus) progressively diminish the palatability of this measure. The growth of BCAs may be limited under fallow periods since they need the root diffusates or their phytonematode host to grow. During fallow period, the BCAs usually remain in resting phase without vegetation (Kerry 2000). The abundance of P. lilacinum, Monographella cucumerina and P. chlamydosporia var. chlamydosporia (Pc280, potato cyst nematode biotype) and P. chlamydosporia var. catenulata (Pc392, root-knot nematode biotype) was significantly lower in fallow than their abundance in the presence of different plants (oilseed rape, sugarbeet and wheat) in the potato rotation (Manzanilla-López et al. 2011). The population of G. rostochiensis declined by 84% when Purpureocillium sp. applied to soil left in fallow while the decline percent in soil left in fallow (without BCA) was as low as 7% (López-Lima et al. 2013). When it is possible, flooding for an extended time may kill phytonematodes because of high moisture level, soil anaerobic conditions and the production of toxic substances (Trivedi and Barker 1986). This measure can be used in non-sloping fields where water is not a limiting factor. In the paddy rice fields where the soil was flooded for 3 months or more, the root-knot nematodes were undetectable on the succeeding tomato crop (Sikora et al. 2005).
When both sterilised and non-sterilised soils were water-saturated, the populations of nematodes significantly reduced in non-sterile soil compared with those reduced in sterile one. This illustrated the potential role of microbial activity in decrease of nematode numbers in flooded soil (Hollis and Rodriguez-Kabana 1966). Though flooding may control phytonematodes, it is not a feasible tactic in many parts of the world due to water deficiency. Another disadvantage is to exclude the inundated farm from cultivation so produce no revenue (Viaene et al. 2013).
10.3.6 Organic Amendments
The growers have been practising this tactic for centuries without noticing its influences on phytonematodes (Renčo 2013). Studying the impact of organic matter amendment on biocontrol and soil microbial populations is a progressively growing research area (Ciancio et al. 2016; Ansari et al. 2019; Ansari and Mahmood 2019a, b). Organic amendments usually cause an enhancement in diversity and populations of soil inhabitant microorganisms and lead to more phytonematode suppression. However, neutral or negative impacts of organic amendment on BCAs have also been reported. It seems that the change in biocontrol activity of antagonists is depended on the kind and amount of organic matter as well as on the types of BCAs (Timper 2014). For example, trapping activity and populations were mutually related for Dactylellina haptotyla but not for Arthrobotrys oligospora when soil was amended with organic matter (Jaffee et al. 1998; Jaffee 2004). It has been frequently reported that addition of organic matter to soil alone could suppress phytonematode populations (Fatemy and Moosavi 2019) but increase saprophytic ones (Viaene et al. 2013). The added organic matters usually originate from animal dung, chitinous materials, industrial wastes, composts, processing residues and green manure (Sikora et al. 2005; Timper 2014). They may be applied as composted or fresh material or as the exudates from the roots of growing plants (Hildalgo-Diaz and Kerry 2008). Management typically ascribes to any one or more mechanisms as liberation of nematicidal molecules (like glucosinolates) from organic matters; release of allelochemicals (like antibiotics and hydrolytic enzymes) from microorganisms whose populations were enhanced by amendments; augmentation of the BCAs potency; and better plant growth and improved nematode-tolerance (by improving soil structure and water-holding capacity, and by increasing the activity of plant growth-promoting organisms) (Widmer et al. 2002; Thoden et al. 2011). It is rational to expect that organic amendment increases the abundance and performance of facultative parasites of nematode but not of obligate ones. However, the conducted experiments have not supported the hypothesis. Many indirect effects may involve in this rebuttal. For example, incorporations of organic matter into soil may increase the population level of bacteriophagous nematodes which are accessible prey for obligate parasites such as P. penetrans (Gomes et al. 2002) or Drechmeria coniospora (Van den Boogert et al. 1994). Application of organic matters can enhance the activity of soil resident antagonists. It seems that their application in combination with promising BCAs has potency to manage nematode on a large-field basis. Amending soil with castor oil cakes increased the parasitisation of Tylenchulus semipenetrans females by T. harzianum (Reddy et al. 1996). The infection rate of M. javanica eggs by Trichoderma longibrachiatum (Sajadi et al. 2016) and T. harzianum (Amir-Ahmadi et al. 2017) was improved by increase in the soil organic matter content. The efficiency of P. lilacinum and Cladosporium oxysporum increased when applied combinedly with oil cakes. The best eggplant growth and M. javanica management was seen in treatments which received P. lilacinum and groundnut cake simultaneously (Ashraf and Khan 2010). Populations of P. chlamydosporia and the parasitised percent of M. incognita eggs increased when neem (Azadirachta indica) leaves were incorporated into soil (Reddy et al. 1999). Similarly, adding dry neem leaves to field soil increased the antagonistic activity of P. chlamydosporia, P. lilacinum and T. harzianum against female and egg masses compared with the antagonistic activity when fungi were applied alone (Khan et al. 2012). The effect of T. patula residual on increasing activity of BCAs was reported. However, the enhancement was not adequate to control Rotylenchulus reniformis on pineapple (Ko and Schmitt 1996). To examine the rise or fall of biocontrol level of a BCA after specific amendment, we need to design an experiment with a factorial structure. Two winter cover crops (rye and crimson clover) were cultivated for 1 month, then killed and their above ground part was left on soil or removed. Afterward P. lilacinum was applied to soil. Suppression of M. incognita on cotton in the presence of the fungus and residues was 60% for rye and 49% for crimson clover compared with 35% for soil left in follow. Greater decrease in the nematode reproduction rate was seen when the above-ground residues were left on the soil surface than when it was eliminated. In the treatments where the above-ground residues were removed, nematode suppression was lower than in the fallow soil (Timper and Parajuli 2012). To separate the effect of nematicidal metabolites from the effect of enhancing BCAs activity, it is better to assess the biocontrol level of phytonematodes several months after adding organic matters into soil. Five months after incorporating sugarcane residue into soil, biological suppression of P. zeae was observed (Stirling et al. 2005). Likewise, after one and 2 years of combined adding of poultry manure and sawdust, biological suppression of M. javanica was demonstrated (Stirling et al. 2012).
Amending soil with specific substances such as chitin will enhance the populations of chitinase-producing microorganisms which in turn may increase the degradation of chitinous layer of nematode eggshell, especially those aggregated in gelatinous matrixes or cysts. Amending soil with chitin stimulated the activity of antagonistic fungi in soil and resulted in reduction in population of M. arenaria (Godoy et al. 1983). As well, incorporating 1% (w/w) chitin into soil could efficiently suppress M. incognita on cotton and enhance the population level of chitinolytic bacteria (Hallmann et al. 1999). The same result was obtained when chitin was applied in M. arenaria-infested soil in combination with P. lilacinum (Culbreath et al. 1986; Rodriguez-Kabana et al. 1987). Though the abundance of antagonistic BCAs is increased after chitin amendments, the main impact of chitin on nematodes attributed to the liberation of ammonia, at least near to application time (Viaene et al. 2013). As said before, enhancing response may not be always seen by BCAs to organic amendments. The impact of organic amendments on the performance of BCAs may be nematode species-, organic matter type- and organic matter amount-dependent. Compared to bare soil, the vermiform stages of R. reniformis were more parasitised by amending soil with sunn hemp (Crotalaria juncea) and pineapple (Ananas comosus) but not with rapeseed (Brassica napus) and marigold (Tagetes erecta). More eggs of R. reniformis were parasitised only when soil was amended with sunn hemp (Wang et al. 2001). Amending soil with composted leaves of T. minuta induced parasitic activity of P. lilacinum on M. javanica eggs but the percent of infected eggs was too low to establish a considerable nematode suppression (Oduor-Owino 2003). Soil amendments may sometimes adversely affect the population densities of feeble saprophytic BCAs which surrender the competition to other strong saprotroph microorganisms whose population is much increased. However, more secreted fungicidal molecules by enhanced populations of soil microbiota should not be neglected (Timper 2014). Controlling ability of H. rhossiliensis did not increase subsequent to applying huge amounts of chicken manure, wheat straw or composted cow manure (Jaffee et al. 1994). Organic soil amendments may increase the nutrient level of soil and make the BCAs less aggressive by decreasing their tendency to switch from saprophytic to parasitic phase. In the presence of glucose and quickly absorbable nitrogen sources, the production of serine proteases by P. chlamydosporia and P. lilacinum was suppressed (Viaene et al. 2013). Supplemented soil with either grape (Vitis vinifera) or alfalfa (Medicago sativa) leaves resulted in increasing populations of Arthrobotrys oligospora and Dactylellina candidum, but trap formation was only enhanced with D. candidum (Jaffee 2004). It seems that their trophic status involves in this difference. Network-producing nematophagous fungi (such as A. oligospora) usually are good saprophytes and by increase in soil nutrient level, their reliance on phytonematodes will decrease. But, reliance of weak saprophytes (such as D. candidum) on phytonematodes is more (Moosavi and Zare 2012). Predatory behaviour of nematode-trapper fungi is considered as a tactic of surviving competition when microbial activity increased consequent to organic amendments and is not correlated to nematode population levels (Stirling 1988). Population densities of nematode-trapping fungi were increased 1 month after T. erecta residues were incorporated into soil but the effect was not durable and disappeared soon (Wang et al. 2002). Incorporating plant parts which may produce allelopathic molecules into soil can cause adverse effect on BCAs. Amending soil by organic matter with low C/N ratio may also cause negative effect on BCAs due to enhancing ammonia (NH3) concentrations during decomposition (Rodriguez-Kabana et al. 1987; Oka 2010). Though soil amendment could reduce plant host infection by phytonematode, this task might be achieved only by incorporating a huge quantity of amending matters into soil. The impact of soil amendment on BCAs populations is complicated and cannot be interpreted easily. Critical investigations are needed to reveal the suppression mechanisms of organic amendments; to determine the amounts of organic matter which can practically and efficiently be applied to soil; and to better comprehend the interaction of organic matter with soil biota, host plant and phytonematodes.
10.3.7 Tillage Effect
Routine tillage practice may adversely affect the soil community by mechanical damage (ripping and inverting the soil), being buried deep or by brining to soil surface. Few studies have been found to investigate the effect of combined application of tillage and BCAs. But investigating the effect of tillage on BCAs has been resulted in inconsistent results. The parasitism of H. glycines eggs was more in the soil that was disc ploughed compared with those that were moldboard ploughed or no-tilled (Bernard et al. 1996). No significant differences were detected in parasitism of H. glycines juveniles by H. rhossiliensis and H. minnesotensis in soybean fields with conventional tillage and no-tillage (Chen and Liu 2007), but the parasitised percent of H. glycines juveniles by H. rhossiliensis was lower in simulated tillage (sieving the soil) than in minimal tillage (Bao et al. 2011). Rotary tilling soil caused 28% decrease in percentage of P. penetrans-infected juveniles of M. incognita than in no-tilled (Talavera et al. 2002b). However, no significant differences were observed in parasitising H. glycines on soybean by Pasteuria nishizawae when the plots were subjected to conventional and no tillage (Noel et al. 2010). When conservation tillage was adopted in wheat fields of Australia, the cyst populations of Heterodera avenae on roots and its damage to yield were decreased (Roget and Rovira 1987). The population densities of nematodes were a little more in no-tilled regime than in conservation tillage (Fortnum and Karlen 1985). More study is required to understand the effect of tillage on BCAs efficacy.
10.4 Decreasing Phytonematode Populations
Any measure which involves in reducing phytonematode populations may help BCAs to complete their task better. Some of these tactics may be used in combination with BCAs and some may be employed prior to applying BCAs. Soil disinfestations by steaming, soil solarisation, biofumigation or broad-spectrum biocides may reduce the populations and activity of soil microbial competitors and applying BCAs after these treatments resulted in easier establishment and survival of the introduced BCAs. On the other hand, biocontrol of lesser populations of nematode is too easier (Viaene et al. 2013). No BCA can suppress phytonematode populations as rapidly as nematicides (Cumagun and Moosavi 2015), so several post-planting nematicides can be used in combination with BCAs where the chemical nematicide impedes initial nematode damage and the BCAs provide long-term protection (Moosavi and Zare 2012; Sokhandani et al. 2016).
10.4.1 Soil Solarisation
Soil solarisation can successfully disinfest soil of weeds, soilborne pests and pathogens where the climate is hot, water is available and the soil depth is shallow. Exposing moistened soil below plastic mulches to solar radiation for at least 4–6 weeks will kill phytonematodes (Hildalgo-Diaz and Kerry 2008); however, the cost of polyethylene sheeting and the needed length of time may be deterrent. The greenhouse effect under polyethylene sheeting causes an increase in soil temperature up to 35–50 °C in 30 cm upper depth. The efficacy of this tactic to disinfest soil of nematodes depends on soil type, solar intensity, soil moisture content and preceding tillage (Viaene et al. 2013). Successive cultivation of susceptible plants (tomato-melon) to root-knot nematodes became possible by solarising soil for 30 days in summer (Sano 2002). Biological control may integratedly be implemented with soil solarisation if the BCAs possess heat resistance propagules. Spores of Pasteuria are moderately resistant to heat and drought (Sikora 1992) so would survive solarisation. The use of soil solarisation and P. penetrans had synergistic effect on controlling M. javanica on grapevine (Walker and Wachtel 1988) and cucumber (Tzortzakakis and Goewn 1994). However, application of P. lilacinum after a 15-day soil solarisation could not adequately reduce root-knot nematode populations (Anastasiadis et al. 2008).
10.4.2 Biofumigation
Producing volatile molecules during hydrolysing of glucosinolate-containing plant residues or organic matters by soil microbiota is called biofumigation. The majority of glucosinolate-containing plants are clustered within the Brassicaceae, Capparaceae and Caricaceae families. These biocidal/nematicidal molecules have high toxicity against soilborne pests and pathogens (Kruger et al. 2013). However, biofumigation usage is now restricted mainly because of the bulky amount of organic materials to be incorporated to soil (Hildalgo-Diaz and Kerry 2008). For better control of M. incognita, it has been recommended to replace cover crop (such as small grains) by crops with biofumigation potential (Westphal 2011).
Despite appearing as a fair promising tactic for the control of soilborne diseases, it is improbable that biofumigation could sufficiently suppress the phytonematode by itself. But its application in combination with soil solarisation or resistant hosts could improve its efficacy (Ploeg 2008). The activity of nematode antagonist may increase after biofumigation (Sikora et al. 2005), but little literature has been found to study the combined effect of biofumigation and BCAs.
10.4.3 Chemical Nematicides
The main method to reduce the damage of phytonematodes is now based on chemical nematicides. These compounds could reduce the numbers of nematodes, stop or decrease nematode reproduction, or paralyse them (nematostatic) for a while (Haydock et al. 2013). Present chemical nematicides in the market can be divided to fumigants and non-fumigants and their classification usually is based on their mode of action (Ebone et al. 2019). Chemical nematicides severely endanger human health and environment (Moosavi and Zare 2016). It has been reported that phytonematode populations at the end of the season in the nematicide-treated plots are usually more than in the untreated plots (Sipes and Schmitt 1998) due to more spread root system which could support more nematode when the effect of nematicicde diminishes. However, growth in phytonematode populations may be for lower activity of BCAs in nematicide treated soil (Timper 2014). Notwithstanding theses disadvantages, nematicides cannot be eliminated, at least for now, from nematode management programmes. However, it seems that the best approach is to integrate the nematicides with other management methods instead of applying the nematicides as the only control measure (Hillocks 2012). The integrated application of synthetic chemicals and BCAs has drawn much interest for its probable additive or synergistic effects (Spadaro and Gullino 2005). Theoretically, non-fumigant nematicides could increase BCAs’ potency if they are applied combinedly. It is highly recommended that nematicides should be applied when more than one phytonematode species exist in soil. The nematicide will suppress the species that might not be susceptible to applied BCA or even the populations that do not encounter with applied BCA. A few investigations have tested the effect of combined application of nematicides and BCAs on phytonematode management, but it has been reported that fungal BCAs from different groups (trapping fungi, P. lilacinum and P. chlamydosporia) were little affected when they were exposed to standard doses of several different pesticides applied to soil (Kerry 1987). Thus, it is feasible to apply these BCAs with nematicides to extend and enhance nematode management (Sokhandani et al. 2016). The biological suppression of nematodes decreased immediately after nematicide application, but in the next spring biological suppression increased wherever nematicide applied (Timper et al. 2012). Applying P. lilacinum and Trichoderma viride in combination with mustard cake and furadan (nematicide) resulted in least M. incognita reproduction rate as compared to untreated treatments (Goswami et al. 2006). Applying granule formulations containing fosthiazate and Monacrosporium ellipsosporum resulted in better M. incognita control and increased the establishment of fungus BCA in soil (Taba et al. 2006). Contradictorily, the populations of nematode-trapping fungi in the fields were greatly enhanced subsequent to sunn hemp incorporation wherever no fumigant nematicide (1, 3-D) had been applied (Wang et al. 2003). This may be due to broader spectrum of organisms (including BCAs) that can be affected by fumigant nematicides. The growth and activity of P. penetrans are not affected by many chemical pesticides, except for chloropicrin that is directly toxic to this bacterium (Chen and Dickson 1998). Gall formation was reduced by 50 and 63% when P. penetrans was applied in combination with carbofuran on tomato to control M. javanica (Brown and Nordmeyer 1985) and M. incognita (Somasekhar and Gill 1991), respectively. As well, integrated application of carbofuran and P. penetrans reduced J2 penetration of Heterodera cajani into pigeonpea roots. A total number of females, eggs per cysts and final population were reduced compared with control treatment (Gogoi and Gill 2001). Aldicarb and ethoprop could not change the percentage of infected M. arenaria juveniles by P. penetrans (Timper 1999; Timper et al. 2001), but the controlling effect of P. penetrans against M. javanica on tomato and cucumber crops was additively increased when it was applied in combination with oxamyl (Tzortzakakis and Goewn 1994). Meloidogyne graminicola population was decreased by 79% on rice when Pseudomonas fluorescens was combinedly used with carbofuran. The decreased amount of M. graminicola population on rice was 69% in simultaneous use of T. viridae and carbofuran (Narasimhamurthy et al. 2017). The in vitro response of three different fungal BCAs was examined to frequently used pesticides in potato fields. No prevention was seen in P. lilacinum and Plectosphaerella cucumerina growth in response to pencycuron or oxamyl, but their growth was slowed down in response to fenpiclonil and tolclofos-methyl. All mentioned chemicals partially inhibited P. chlamydosporia growth (Jacobs et al. 2003). Combined application of T. harzianum and carbofuran resulted in more prominent suppression of M. incognita on french bean (Gogoi and Mahanta 2013), brinjal (Devi et al. 2016), Mentha arvensis (Haseeb et al. 2007) and pea (Brahma and Borah 2016).
Integrated application of P. chlamydosporia with carbofuran (Gopinatha et al. 2002), with neem cake and carbofuran (Dhawan and Singh 2009) and with dazomat (Nagesh and Jankiram 2004) increased suppression of M. incognita. But its integration with fosthiazate did not provide any additional decrease in potato cyst nematodes reproduction rate (Tobin et al. 2008). Optimum levels of Trichoderma longibrachiatum concentration and cadusafos dose were determined in their combined application for the control of M. javania on zucchini plants. The data were analysed using a custom response surface regression model and the optimum levels of the cadusafos and Trichoderma concentration that caused the best plant growth and lowest nematode reproduction were determined as 1.7 mg a.i./kg soil and 108 conidia/ml suspension, respectively (Sokhandani et al. 2016).
10.5 Application of Multiple BCA
Little studies directly investigate or compare the effect of combined application of several BCAs against phytonematodes in contrast with application one BCA. It is globally accepted that inconsistency in performance of BCAs is a main barrier to the broad usage of BCAs (Moosavi and Zare 2015); however, integration of two or more robust BCAs may help in overcoming this disadvantage. Arguably, integrated use of BCAs may increase the achieved control especially if the combined BCAs are compatible or have different mode of actions (Moosavi and Zare 2016). Fluctuation in populations of BCAs is hardly happened when several BCAs exist in or introduce into soil. Combined application of BCAs provides several benefits such as more and better colonisation of the rhizosphere; parasitising more than one stage of the life cycle of a nematode as well as parasitising more than one target species; being active in more extensive time span during growing season; possessing various mode of action; and performing more consistent under more broaden range of environmental and soil condition (Crump 1998; Siddiqui and Mahmood 1996; Meyer and Roberts 2002; Ansari and Mahmood 2017b; Ansari et al. 2017a, b). Applying BCAs with diverse mode of action such as Fusarium oxysporum (endophyte), P. lilacinum (egg parasite) and Bacillus firmus (antagonistic bacteria) increased biomanagement of R. similis on banana (Mendoza and Sikora 2009). The population density of added BCAs is a matter of importance. For example in the conducted experiments, the combined effect of two BCAs with a specific application rate (x) has been usually compared with the effect of each BCA used at the same rate alone (x) and not with one BCA used at twice the rate (2x). On the other hand, analysing the data which have presented in conducted investigations usually demonstrated additive effect more than synergistic one (Hildalgo-Diaz and Kerry 2008). Further experiments are required to evidently elucidate the phenomena after combined application of two or more BCAs especially on the ecological basis. BCAs have to survive and act in biologically complex environments where they are subjected to numerous inter- and intera-specific interactions (Knudsen and Dandurand 2014). Consequent to those interactions, the combined application of BCAs may result in competence, independence, additive or synergistic effect. Though analysing the published paper on combined application of BCAs indicated that antagonistic interactions are more probable (Xu et al. 2011), it has been suggested that introducing BCAs to soil as consortium might imitate natural soil condition and could stimulate host plant defence responses and enhance its growth (Sarma et al. 2015). More understanding on host plants’ responses to phytonematodes in the presence of several BCAs and the probable interactions is required for sound judgement.
The suppression effect of A. oligospora in combination with each of 11 different strains of bacteria on J2 populations of Meloidogyne mayaguensis was assessed in tomato rhizosphere. Greater control achieved when A. oligospora was integratedly applied with three different unidentified bacteria (Duponnois et al. 1998). When Embellisia chlamydospora, P. chlamydosporia and a sterile fungus were applied alone and in different binary combinations, the lowest number of females and cysts of H. schachtii was observed when either Embellisia or Pochonia was applied in combination with the sterile fungus. No nematode suppression was observed by individual application of the mentioned fungi or by the Embellisia–Pochonia combination (Hojat Jalali et al. 1998). Applying T. harzianum simultaneously with Monacrosporium lysipagum (nematode trapper fungus) resulted in better control of M. javanica and H. avenae (Khan et al. 2006). Together application of Acremonium strictum and T. harzianum enhanced biocontrol activity against M. incognita on tomato significantly (Goswami et al. 2008). When 90 combinations of different Trichoderma (18 strains from five species) and nematode-trapping fungi (six strains from four species) were examined against Caenorhabditis elegans, integration of T. harzianum and Monacrosporium cionopagum had the best compatibility (Szabó et al. 2012). Five different fungi (Pochonia bulbillosa (Pb), Pochonia chlamydosporia var. catenulata (Pccat), Pochonia chlamydosporia var. chlamydosporia (Pcc), Lecanicillium aphanocladii (La) and T. harzianum (Th)) whose in vitro pathogenicity on the M. javanica eggs was similar used alone and in binary or trinary combination for the control of M. javanica on eggplant. Combined application of these BCAs had no significant increasing effect on plant growth compared with growth in the pots treated by one BCA. But integrated application of BCAs increased the egg infection rate significantly. None of the treatment could manage M. javanica as the same level as cadusafos nematicide (96%); however, the integrated application of Pccat, La with Pcc (85%) or Th (83%) controlled M. javanica acceptably (Moosavi et al. 2015). The bacterium P. penetrans was compatibly combined with P. chlamydosporia (de Leij et al. 1992), P. lilacinum (Gautam et al. 1995) and Glomus sp. (Talavera et al. 2002a), and their integrated usage could control M. incognita on tomato plants better. Sometimes BCAs may be assisted by soil microbiota to fulfil their tasks. The endospores adherence of P. penetrans to M. graminicola increased with the help of rhizospheral resident bacteria (Duponnois et al. 1997). The population density of M. javanica on a cropping system consisted of eggplant–okra–tomato–okra–eggplant–tomato–okra was further reduced by 24% when P. chlamydosporia was applied in combination with P. penetrans rather than their solo application (Amer-Zareen et al. 2004). There are several reports that combination usage of BCAs makes no advantages over their individual application. Combined application of H. rhossiliensis and P. chlamydosporia against Meloidogyne hapla on lettuce did not enhance controlling activity compared with their individual usage (Viaene and Abawi 2000). Combined application of P. penetrans, P. lilacinum, B subtilis and Talaromyces flavus caused the same control level of root-knot nematode as their individual application did (Zaki and Maqbool 1991). Mixed usage of M. lysipagum with T. harzianum made no significant additive control of R. similis on banana compared with applying M. lysipagum alone (Khan et al. 2006). Combining BCAs sometimes results in lower management potential. The combination of Bacillus thuringiensis, Paecilomyces marquandii and Streptomyces costaricanus was not as effective as individual treatments for decreasing R. similis and Helicotylenchus multicinctus populations on banana (Esnard et al. 1998). Similarly, integration of S. costaricanus and B. thuringiensis resulted in lower biocontrol level of M. hapla on lettuce compared with biocontrol level achieved with their individual usage (Chen et al. 2000). While solitary application of Trichoderma virens and Burkholderia cepacia could successfully control M. incognita on bell pepper, their combined application was not as successful (Meyer et al. 2001). Integrated application of Calothrix parietina with either P. lilacinum or Pichia guilliermondii reduced their potency against M. incognita maybe due to antagonistic activity of C. parietina (Hashem and Abo-Elyousr 2011).
10.6 Conclusions and Future Prospects
Though phytonematode control is now based on chemical nematicides, it seems that in the near future it should inevitably be changed to an integrated multi-based management system. It must be also taken into consideration that inundative release of BCAs could not manage the phytonematodes consistently and must be applied in combination with other approaches. But careful consideration is required in choosing the effective measures that should be integrated. The selected ones must have several characteristics such as being compatible, provide synergistic effect, being economically affordable and impose the least environmental hazard. Maybe multidisciplinary studies could be of help to develop effective combinable measures.
From growers’ viewpoint, chemical nematicides have several priorities to biocontrol in characteristics such as cost, transportation, delivery technology, performance and simplicity of storage and application. Therefore, consolidated use of BCAs with other tactics that provide synergistic or additive effect could be of help in accepting biocontrol as a potent substitute. If biological control wants to become an important part of phytonematode management, more improvement is also needed in their producing procedures, formulation, efficacy, consistency and application methods. The improvement must primarily occur in reducing production cost and enhancing potency. Moreover, production of BCA derivatives such as bionematicides is another measure of choice which has both advantages of effectiveness and being eco-friendly. The preparation of natural nematicides whose bioactive ingredients derive from BCAs should be oriented to products with low amount but strongly effective natural molecules which could effectively control the phytonematodes. Another probable approach is host plants transformation with effective genes against phytonematodes supplied by different sources include BCAs. As many people prefer not to consume genetically modified crops, the exploitation of this approach is hesitated. However, transforming BCAs to enhance their detrimental effect against phytonematodes is another option. The efficiency, consistency, virulence, ecological adaptability and easier mass production and formulation of BCAs can be improved by genetic engineering. In fact, numerous nematode-antagonists exist in arable lands and their persistence or activity mainly depends on our chosen cultural practices. However, the possible lack of suitable native BCAs can be compensated by introducing potent antagonists. Integration of biocontrol with compatible measures surely increases nematode suppression to an acceptable level. The farmers should be informed that the increase in populations of beneficial BCAs and adequate nematode suppression may need more than one growing season. It seems that the proper combination of plant-BCA (indigenous or introduced) provides a liable foundation that other locally available measures can be constructed upon it.
References
Agrios GN (ed) (2005) Plant pathology, 5th edn. Academic Press, New York
Alesadi GA, Moosavi MR, Basirnia T (2017) Effect of nano-K, potassium sulphate and salicylic acid on tomato growth and control of root-knot nematode (Meloidogyne javanica). J Plant Prot 40(3):71–82; in Persian with English abstract
Amer-Zareen ZMJ, Abid M, Gowen SR, Kerry BR (2004) Management of root knot nematode (Meloidogyne javanica) by biocontrol agents in two crop rotations. Int J Biol Biotechnol 1(1):67–73
Amir-Ahmadi N, Moosavi MR, Moaf-Poorian GR (2017) Investigating the effect of soil texture and its organic content on the efficacy of Trichoderma harzianum in controlling Meloidogyne javanica and stimulating the growth of kidney bean. Biocontrol Sci Tech 27(1):115–127
Anastasiadis IA, Giannakou IO, Prophetou-Athanasiadou DA, Gowen SR (2008) The combined effect of the application of a biocontrol agent Paecilomyces lilacinus, with various practices for the control of root-knot nematodes. Crop Prot 27:352–361
Ansari RA, Khan TA (2012a) Parasitic association of root-knot nematode, Meloidogyne incognita on guava. e-J Sci Technol 5:65–67
Ansari RA, Khan TA (2012b) Diversity and community structure of phytonematodes associated with guava in and around Aligarh, Uttar Pradesh, India. Trends Biosci 5(3):202–204
Ansari RA, Mahmood I (2017a) Optimization of organic and bio-organic fertilizers on soil properties and growth of pigeon pea. Sci Hortic 226:1–9
Ansari RA, Mahmood I (2017b) Determination of disease incidence caused by Meloidogyne spp. and or Fusarium udum on pigeonpea in Aligarh district: a survey. Trends Biosci 10(24):5239–5243
Ansari RA, Mahmood I (2019a) Plant health under biotic stress: volume 2: microbial interactions. Springer, Singapore. https://doi.org/10.1007/978-981-13-6040-4
Ansari RA, Mahmood I (2019b) Plant health under biotic stress: volume 1: organic strategies. Springer, Singapore. https://doi.org/10.1007/978-981-13-6043-5
Ansari RA, Rizvi R, Sumbul A, Mahmood I (2017a) PGPR: current vogue in sustainable crop production. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and plant health. Springer, Singapore, pp 455–472
Ansari RA, Mahmood I, Rizvi R, Sumbul A (2017b) Siderophores: augmentation of soil health and crop productivity. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics in agroecosystem. Springer, Singapore, pp 291–312
Ansari RA, Sumbul A, Rizvi R, Mahmood I (2019) Organic soil amendments: potential tool for soil and plant health management. In: Ansari RA, Mahmood I (eds) Plant health under biotic stress. Springer, Singapore, pp 1–35
Ashraf MS, Khan TA (2010) Integrated approach for the management of Meloidogyne javanica on eggplant using oil cakes and biocontrol agents. Arch Phytopathol Plant Protect 43(6):609–614
Atkins SD, Hidalgo-Diaz L, Kalisz H, Mauchline TH, Hirsch PR, Kerry BR (2003) Development of a new management strategy for the control of root-knot nematodes (Meloidogyne spp.) in organic vegetable production. Pest Manag Sci 59:183–189
Baker KF (1981) Biological control. In: Mace E, Bell AA, Beckman CH (eds) Fungal wilt diseases of plants. Academic Press, London, pp 523–561
Bakker E, Dees R, Bakker J, Goverse A (2006) Mechanisms involved in plant resistance to nematodes. In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer Science + Business Media, New York, pp 314–334
Bao Y, Neher DA, Chen SY (2011) Effect of soil disturbance and biocides on nematode communities and extracellular enzyme activity in soybean cyst nematode suppressive soil. Nematology 13:687–699
Barker KR (1991) Rotation and cropping systems for nematode control: the North Carolina experience-introduction. J Nematol 23(3):342–343
Bernard EC, Self LH, Tyler DD (1996) Fungal parasitism of soybean cyst nematode, Heterodera glycines (Nemata: Heteroderidae), in differing cropping-tillage regimes. Appl Soil Ecol 5:57–70
Brahma U, Borah A (2016) Management of Meloidogyne incognita on pea with bioagents and organic amendment. Indian J Nematol 46:58–61
Brown SM, Nordmeyer D (1985) Synergistic reduction in root galling by Meloidogyne javanica with Pasteuria penetrans and nematicide. Rev Nematol 8:285–286
Bruinsma J (ed) (2003) World agriculture: towards 2015/2030: an FAO perspective. Earthscan Publications, London
Castagnone-Sereno P (2002) Genetic variability in parthenogenesis root-knot nematodes, Meloidogynes pp., and their ability to overcome plant resistance genes. Nematology 4:605–608
Chen ZX, Dickson DM (1998) Review of Pasteuria penetrans: biology, ecology, and biological control potential. J Nematol 30:313–340
Chen S, Liu S (2007) Effects of tillage and crop sequence on parasitism of Heterodera glycines juveniles by Hirsutella spp. and on juvenile population density. Nematropica 37:93–106
Chen SY, Reese CD (1999) Parasitism of the nematode Heterodera glycines by the fungus Hirsutella rhossiliensis as influenced by crop sequence. J Nematol 31:437–444
Chen J, Abawi GS, Zuckerman BM (2000) Efficacy of Bacillus thuringiensis, Paecilomyces marquandii, and Streptomyces costaricanus with and without organic amendments against Meloidogyne hapla infecting lettuce. J Nematol 32:70–77
Ciancio A, Pieterse CMJ, Mercado-Blanco J (2016) Editorial: harnessing useful rhizosphere microorganisms for pathogen and pest biocontrol. Front Microbiol 7:1620
Conrath U (2011) Molecular aspects of defense priming. Trends Plant Sci 16:524–531
Cook R, Starr JL (2006) Resistant cultivars. In: Perry RN, Moens M (eds) Plant nematology. CABI Publishing, Wallingford, UK, pp 370–389
Cottage A, Urwin P (2013) Genetic engineering for resistance. In: Perry RN, Moens M (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, UK, pp 437–458
Crump DH (1989) Interaction of cyst nematodes with their natural antagonists. Asp Appl Biol 22:135–140
Crump DH (1991) Biological control of the beet cyst nematode. Br Sugar Beet Rev 59:54–55
Crump DH (1998) Biological control of potato and beet cyst nematodes. Asp Appl Biol 53:383–386
Culbreath AK, Rodriguez-Kabana R, Morgan-Jones G (1986) Chitin and Paecilomyces lilacinus for control of Meloidogyne arenaria. Nematropica 16:153–166
Cumagun CJR, Moosavi MR (2015) Significance of biocontrol agents of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CABI Publishing, Wallingford, UK, pp 50–78
Dallemole-Giaretta R, de Freitas LG, Lopes EA, Ferraz S, de Podesta GS, Agnes EL (2011) Cover crops and Pochonia chlamydosporia for the control of Meloidogyne javanica. Nematology 13:919–926
Dalmasso A, Castagnone-Sereno P, Abad P (1992) Seminar: tolerance and resistance of plants to nematodes-knowledge, needs and prospects. Nematologica 38:466–472
Dandurand L-M, Knudsen GR (2016) Effect of the trap crop Solanum sisymbriifolium and two biocontrol fungi on reproduction of the potato cyst nematode, Globodera pallida. Ann Appl Biol 169(2):180–189
Davies LJ, Elling AA (2015) Resistance genes against plant-parasitic nematodes: a durable control strategy? Nematology 17:249–263
Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155
Devi TS, Mahanta B, Borah A (2016) Comparative efficacy of Glomus fasciculatum, Trichoderma harzianum, carbofuran and carbendazim in management of Meloidogyne incognita and Rhizoctonia solani disease complex on brinjal. Indian J Nematol 46:161–164
Devine KJ, Dunne C, O’Gara F, Jones PW (1999) The influence of in-egg mortality and spontaneous hatching on the decline of Globodera rostochiensis during crop rotation in the absence of the host potato crop in the field. Nematology 1:637–645
Dhawan SC, Singh S (2009) Compatibility of Pochonia chlamydosporia with nematicide and neem cake against root-knot nematode, Meloidogyne incognita infesting okra. Indian J Nematol 39:85–89
Duponnois R, Netscher C, Mateille T (1997) Effect of the rhizosphere microflora on Pasteuria penetrans parasitizing Meloidogyne graminicola. Nematol Mediterr 25:99–103
Duponnois R, Ba AM, Mateille T (1998) Effects of some rhizosphere bacteria for the biocontrol of nematodes of the genus Meloidogyne with Arthrobotrys oligospora. Fundam Appl Nematol 21:157–163
DuPont ST, Ferris H, Van Horn M (2009) Effects of cover crop quality and quantity on nematode-based soil food webs and nutrient cycling. Appl Soil Ecol 41:157–167
Ebone LA, Kovaleski M, Deuner CC (2019) Nematicides: history, mode, and mechanism action. Plant Sci Today 6(2):91–97
Esnard J, Marban-Mendoza N, Zuckerman BM (1998) Effects of three microbial broth cultures and an organic amendment on growth and populations of free-living and plant-parasitic nematodes on banana. Eur J Plant Pathol 104:457–463
FAO (Agriculture Organization of the United Nations), IFAD (International Fund for Agricultural Development) & WFP (World Food Programme) (2013) The state of food insecurity in the world 2013, the multiple dimensions of food security. FAO, Rome, Italy
Fatemy S, Moosavi MR (2019) Nematotoxic potential of daikon, chinaberry and purslane herbal green manures against Globodera rostochiensis in vitro and microplot. J Crop Prot 8(1):69–80
Fortnum BA, Karlen DL (1985) Effects of tillage systems and irrigation on population densities of plant nematodes in field corn. J Nematol 17:25–28
Gautam A, Siddiqui ZA, Mahmood I (1995) Integrated management of Meloidogyne incognita on tomato. Nematol Mediterr 23:245–247
Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818
Godoy G, Rodriguez-Kabana R, Shelby RA, Morgan-Jones G (1983) Chitin amendments for control of Meloidogyne arenaria infested soil. II. Effects on microbial population. Nematropica 13:63–74
Gogoi BB, Gill JS (2001) Compatibility of Pasteuria penetrans with carbofuran and organic amendments, its effect on Heterodera cajani. Ann Plant Prot Sci 9(2):254–257
Gogoi D, Mahanta B (2013) Comparative efficacy of Glomus fasciculatum, Trichoderma harzianum, carbofuran and carbendazim in management of Meloidogyne incognita and Rhizoctonia solani disease complex on French bean. Ann Plant Prot Sci 21:172–175
Gomes CB, De Freitas LG, Ferraz S, Oliveira RDDL, Da Silva RV (2002) Influence of cattle manure content in the substrate on the multiplication of Pasteuria penetrans in tomato. Nematol Brasil 26:59–65
Gomiero T, Pimentel D, Paoletti MG (2011) Is there a need for a more sustainable agriculture? Crit Rev Plant Sci 30:6–23
Gopinatha KV, Gowda DN, Nagesh M (2002) Management of root-knot nematode Meloidogyne incognita on tomato using bioagent Verticillium chlamydosporium, neem cake, marigold and carbofuran. Indian J Nematol 32:179–181
Goswami BK, Pandey RK, Rathour KS, Bhattacharya C, Singh L (2006) Integrated application of some compatible biocontrol agents along with mustard oil seed cake and furadan on Meloidogyne incognita infecting tomato plants. J Zhejiang Univ Sci B 7(11):873–875
Goswami J, Pandey RK, Tewari JP, Goswami BK (2008) Management of root knot nematode on tomato through application of fungal antagonists, Acremonium strictum and Trichoderma harzianum. J Environ Sci Health B 43(3):237–240
Grubišić D, Uroić G, Ivošević A, Grdiša M (2018) Nematode control by the use of antagonistic plants. Agric Conspec Sci 83(4):269–275
Hallmann J, Rodriguez-Kabana R, Kloepper JW (1999) Chitin-mediated changes in bacterial communities of the soil, rhizosphere and within roots of cotton in relation to nematode control. Soil Biol Biochem 31:551–560
Haseeb A, Kumar V, Abuzar S, Sharma A (2007) Integrated management of Meloidogyne incognita-Sclerotinia sclerotiorum disease complex of Mentha arvensis cv. Gomti by using Trichoderma species, neem seed powder, carbofuran and topsin-M. In: 7th national symposium on plant protection options implementation and feasibility. 20–22 Dec, p. 102
Hashem M, Abo-Elyousr KA (2011) Management of the root-knot nematode Meloidogyne incognita on tomato with combinations of different biocontrol organisms. Crop Prot 30:285–292
Haydock PPJ, Woods SR, Grove IG, Hare MC (2013) Chemical control of nematodes. In: Perry RN, Moens M (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, UK, pp 459–479
Hildalgo-Diaz L, Kerry BR (2008) Integration of biological control with other methods of nematode management. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetableand grain crops nematodes. Springer, Dordrecht, the Netherlands, pp 29–49
Hillocks RJ (2012) Farming with fewer pesticides: EU pesticide review and resulting challenges for UK agriculture. Crop Prot 31:85–93
Hojat Jalali AA, Segers R, Coosemans J (1998) Biocontrol of Heterodera schachtii using combinations of the sterile fungus, StFCH1-l, Embellisia chlamydospora and Verticillium chlamydosporium. Nematologica 44:345–355
Hollis JP, Rodriguez-Kabana RA (1966) Rapid kill of nematodes in flooded soil. Phytopathology 56:1015–1019
Hooks CRR, Wang K-H, Ploeg A, McSorley R (2010) Using marigold (Tagetes spp.) as a cover crop to protect crops from plant-parasitic nematodes. Appl Soil Ecol 46:307–320
Jacobs H, Gray SN, Crump DH (2003) Interactions between nematophagous fungi and consequences for their potential as biological agents for the control of potato cyst nematodes. Mycol Res 107(1):47–56
Jaffee BA (2004) Do organic amendments enhance the nematode-trapping fungi Dactylellina haptotyla and Arthrobotrys oligospora? J Nematol 36:267–275
Jaffee B, Phillips R, Muldoon A, Mangel M (1992) Density dependent host-pathogen dynamics in soil microcosms. Ecology 73:495–506
Jaffee BA, Ferris H, Stapleton JJ, Norton MVK, Muldoon AE (1994) Parasitism of nematodes by the fungus Hirsutella rhossiliensis as affected by certain organic amendments. J Nematol 26:152–161
Jaffee BA, Ferris H, Scow KM (1998) Nematode-trapping fungi in organic and conventional cropping systems. Phytopathology 88:344–350
Kaloshian I, Desmond OJ, Atamian HS (2011) Disease resistance-genes and defense responses during incompatible interactions. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, the Netherlands, pp 309–325
Kerry BR (1987) Biological control. In: Brown RH, Kerry BR (eds) Principles and practice of nematode control in crops. Academic Press, Sydney, Australia, pp 233–263
Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441
Khan A, Williams KL, Nevalainen HKM (2006) Control of plant-parasitic nematodes by Paecilomyces lilacinus and Monacrosporium lysipagum in pot trials. BioControl 51:643–658
Khan MR, Mohiddin FA, Ejaz MN, Khan MM (2012) Management of root-knot disease in eggplant through the application of biocontrol fungi and dry neem leaves. Turk J Biol 36:161–169
Knudsen GR, Dandurand LMC (2014) Ecological complexity and the success of fungal biological control agents. Adv Agric 2014:542703, 11 pages
Ko MP, Schmitt DP (1996) Changes in plant-parasitic nematode populations in pineapple fields following inter-cycle cover crops. J Nematol 28:546–556
Koenning SR, Barker KR, Bowman DT (2001) Resistance as tactic for management of Meloidogyne incognita on cotton in North Carolina. J Nematol 33:126–131
Kokalis-Burelle N, Mahaffee WF, Rodriguez-Kabana J, Kloepper W, Bowen KL (2002) Effects of switchgrass (Panicum virgatum) rotations with peanut (Arachis hypogaea L.) on nematode populations and soil microflora. J Nematol 34:98–105
Kratochvil RJ, Sardanelli S, Everts K, Gallagher E (2004) Evaluation of crop rotation and other cultural practices for management of root-knot and lesion nematodes. Agron J 96:1419–1428
Kruger DHM, Fourie JC, Malan AP (2013) Cover crops with biofumigation properties for the suppression of plant-parasitic nematodes: a review. South Afr J Enol Viticulture 34(2):287–295
Lalezar M, Moosavi MR, Hesami A (2016) Changes in zucchini defense responses against Meloidogyne javanica (Rhabditida: Meloidogynidae) induced by Pochonia chlamydosporia. Munis Entomol Zool 11(1):151–159
Leadbeater A, Staub T (2014) Exploitation of induced resistance: a commercial perspective. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defense: a sustainable approach to crop protection. Blackwell, Oxford, pp 300–315
de Leij FAAM, Davies KG, Kerry BR (1992) The use of Verticillium chlamydosporium Goddard and Pasteuria penetrans (Thorne) Sayre & Starr alone and in combination to control Meloidogyne incognita on tomato plants. Fundam Appl Nematol 15:235–242
Liang L-M, Zou C-G, Xu J, Zhang KQ (2019) Signal pathways involved in microbe–nematode interactions provide new insights into the biocontrol of plant-parasitic nematodes. Philos Trans Roy Soc B 374:20180317
López-Lima D, Sánchez-Nava P, Carrión G, Núñez-Sánchez A (2013) 89% reduction of a potato cyst nematode population using biological control and rotation. Agron Sustain Dev 33(2):425–431
Manzanilla-López RH, Esteves I, Powers SJ, Kerry BR (2011) Effects of crop plants on abundance of Pochonia chlamydosporia and other fungal parasites of root-knot and potato cyst nematodes. Ann Appl Biol 159:118–129
de Medeiros HA, Resende RS, Ferreira FC, Freitas LG, Rodrigues FÁ (2015) Induction of resistance in tomato against Meloidogyne javanica by Pochonia chlamydosporia. Nematoda 2:e10015. https://doi.org/10.4322/nematoda.10015
de Medeiros HA, de Araújo Filho JV, de Freitas LG, Castillo P, Rubio MB, Hermosa R, Monte E (2017) Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci Rep 7:40,216. https://doi.org/10.1038/srep40216
Mendoza AR, Sikora RA (2009) Biological control of Radopholus similis in banana by combined application of the mutualistic endophyte Fusarium oxysporum strain 162, the egg pathogen Paecilomyces lilacinus strain 251 and the antagonistic bacteria Bacillus firmus. BioControl 54:263–272
Meyer SLF, Roberts DP (2002) Combinations of biocontrol agents for management of plant-parasitic nematodes and soilborne plant-pathogenic fungi. J Nematol 34(1):1–8
Meyer SLF, Roberts DP, Chitwood DJ, Carta LK, Lumsden RD, Mao W (2001) Application of Burkholderia cepacia and Trichoderma virens, alone and in combinations, against Meloidogyne incognita on bell pepper. Nematropica 31:75–86
Molinari S (2011) Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Rep 30:311–323
Moosavi MR (2017) The effect of gibberellin and abscisic acid on plant defense responses and on disease amount caused by Meloidogyne javanica on tomato plants. J Gen Plant Pathol 83(3):173–184
Moosavi MR, Askary TH (2015) Nematophagous fungi- commercialization. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CABI Publishing, Wallingford, UK, pp 187–202
Moosavi MR, Ghani M (2019) The optimal concentrations of Purpureocillium lilacinum and jasmonic acid in controlling Meloidogyne javanica on tomato. Arch Phytopathology Plant Protect 52(6–7):582–600
Moosavi MR, Zare R (2012) Fungi as biological control agents of plant-parasitic nematodes. In: Merillon JM, Ramawat KG (eds) Plant defence: biological control, progress in biological control 12. Dordrecht, Netherlands, Springer Science + Business Media, pp 67–107
Moosavi MR, Zare R (2015) Factors affecting commercial success of biocontrol agents of phytonematodes. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CABI Publishing, Wallingford, UK, pp 423–445
Moosavi MR, Zare R (2016) Present status and the future prospects of microbial biopesticides in Iran. In: Singh HB, Sarma BK, Keswani C (eds) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia. Springer, Singapore, pp 293–305
Moosavi MR, Shakeri S, Mohammadi S (2015) The ability of separate and combined application of five nematopathogenic fungi against Meloidogyne javanica. Iran J Plant Prot Sci 46(1):179–190; in Persian with English abstract
Mostafanezhad H, Sahebani N, Nourinejhad Zarghani S (2014) Control of root-knot nematode (Meloidogyne javanica) with combination of Arthrobotrys oligospora and salicylic acid and study of some plant defense responses. Biocontrol Sci Tech 24(2):203–215
Nagesh M, Jankiram T (2004) Root-knot nematode problem in polyhouse roses and its management using dazomat, neem cake and Pochonia chlamydosporia (Verticillium chlamydosporium). J Ornamental Hortic New Series 7(2):147–152
Narasimhamurthy HB, Ravindra H, Sehgal M (2017) Management of rice root-knot nematode, Meloidogyne graminicola. Int J Pure Appl Biosci 5:268–276
Nicol JM, Turner SJ, Coyne DL, den Nijs L, Hockland S, Tahna Maafi Z (2011) Current nematode threats to world agriculture. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer Science + Business Media, Dordrecht, the Netherlands, pp 21–43
Noel GR, Atibalentja N, Bauer SJ (2010) Suppression of Heterodera glycines in a soybean field artificially infested with Pasteuria nishizawae. Nematropica 40:41–52
Oduor-Owino P (2003) Integrated management of root-knot nematodes using agrochemicals, organic matter and the antagonistic fungus, Paecilomyces lilacinus in natural field soil. Nematol Mediterr 31:121–123
Oka Y (2010) Mechanisms of nematode suppression by organic soil amendments—a review. Appl Soil Ecol 44:101–115
Owino OP (1992) Effect of marigold leaf extract and captafol on fungal parasitism of root knot nematode eggs—Kenyan isolates. Nematol Mediterr 20:211–213
Paparu P, Dubois T, Coyne D, Viljoen A (2007) Defense-related gene expression in susceptible and tolerant bananas (Musa spp.) following inoculation with non-pathogenic Fusarium oxysporum endophytes and challenge with Radopholus similis. Physiol Mol Plant Pathol 71:149–157
Ploeg A (2008) Biofumigation to manage plant-parasitic nematodes. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, the Netherlands, pp 239–248
Puertas A, Hidalgo-Díaz L (2007) Influence of the host plant and its interaction with Meloidogyne incognita on the effectiveness of Pochonia chlamydosporia var. catenulata. Revista de Protección Vegetal 22(2):104–109; in Spanish with English abstract
Reddy PP, Rao MS, Nagesh M (1996) Management of the citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematol Mediterr 24:265–267
Reddy PP, Rao MS, Nagesh M (1999) Eco-friendly management of Meloidogyne incognita on tomato by integration of Verticillium chlamydosporium with neem and calotropis leaves. J Plant Dis Prot 106(5):530–533
Renčo M (2013) Organic amendments of soil as useful tools of plant parasitic nematodes control. Helminthologia 50(1):3–14
Roberts PA (2002) Concepts and consequences of resistance. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nematodes. CABI Publishing, Wallingford, pp 23–41
Rodriguez-Kabana R, Morgan-Jones G, Chet I (1987) Biological control of nematodes: soil amendments and microbial antagonists. Plant Soil 100(1–3):237–247
Roget DK, Rovira AD (1987) A review on the effect of tillage on cereal cyst nematode. Wheat Research Council of Australia, Workshop Report Series, No. 1, pp 31–35
Rumbos CI, Kiewnick S (2006) Effect of plant species on persistence of Paecilomyces lilacinus strain 251 in soil and on root colonization by the fungus. Plant Soil 283:25–31
Sajadi Z, Moosavi MR, Moaf-Poorian GR (2016) The effect of soil texture and organic matter on ability of Trichoderma longibrachiatum in controlling Meloidogyne javanica and growth promoting of kidney bean. Iran J Plant Prot Sci 46(2):227–240
Sano Z (2002) Nematode management strategies in east Asian countries. Nematology 4:129–130
Sarma BK, Yadav SK, Singh S, Singh HB (2015) Microbial consortium-mediated plant defense against phytopathogens: readdressing for enhancing efficacy. Soil Biol Biochem 87:25–33
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43
Siddiqui ZA, Mahmood I (1996) Biological control of plant-parasitic nematodes by fungi: a review. Bioresour Technol 58:229–239
Sikora RA (1992) Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Annu Rev Phytopathol 30:245–270
Sikora RA, Bridge J, Starr JL (2005) Management practices: an overview of integrated nematode management technologies. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. Wallingford, CABI Publishing, pp 793–825
Sipes BS, Schmitt DP (1998) Nematode-pesticide interactions. In: Barker KR, Pederson GA, Windham GL (eds) Plant and nematode interactions. American Society of Agronomy, Madison, WI, pp 173–185
Sokhandani Z, Moosavi MR, Basirnia T (2016) Optimum levels of Trichoderma longibrachiatum concentration and cadusafos dose in controlling Meloidogyne javanica on zucchini plants. J Nematol 48(1):54–63
Somasekhar N, Gill JS (1991) Efficacy of Pasteuria penetrans alone and in combination with carbofuran controlling Meloidogyne incognita. Indian J Nematol 21:61–65
Spadaro D, Gullino ML (2005) Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Prot 24:601–613
Starr JL, McDonald AH, Claudius-Cole AO (2013) Nematode resistance in crops. In: Perry RN, Moens M (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, pp 411–436
Stirling GR (1988) Biological control of plant-parasitic nematodes. In: Poinar GO Jr, Jansson H-B (eds) Diseases of nematodes, volume II. CRC Press, Boca Raton, Fl, pp 93–139
Stirling GR (1999) Increasing the adoption of sustainable, integrated management strategies for soilborne diseases of high-value annual crops. Australas Plant Pathol 28:72–79
Stirling GR (2014) The soil environment and the soil–root interface. In: Stirling GR (ed) Biological control of plant-parasitic nematodes, soil ecosystem management in sustainable agriculture, 2nd edn. CABI Publishing, Wallingford, UK, pp 15–47
Stirling GR, Wilson EJ, Stirling AM, Pankurst CE, Moody PW, Bell MJ, Halpin N (2005) Amendments of sugarcane trash induce suppressiveness to plant-parasitic nematodes in a sugarcane soil. Australas Plant Pathol 34:203–211
Stirling GR, Halpin NV, Bell MJ (2011) A surface mulch of crop residues enhances suppressiveness to plant-parasitic nematodes in sugarcane soils. Nematropica 41:109–121
Stirling GR, Smith MK, Smith JP, Stirling AM, Hamill SD (2012) Organic inputs, tillage and rotation practices influence soil health and suppressiveness to soilborne pests and pathogens of ginger. Australas Plant Pathol 41:99–112
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43:83–116
Sturz AV, Kimpinski J (2004) Endoroot bacteria derived from marigold (Tagetes spp.) can decrease soil population densities of root-lesion nematodes in the potato root zone. Plant Soil 262(1–2):241–249
Szabó M, Csepregi K, Gálber M, Virányi F, Fekete C (2012) Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: the role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biol Control 63:121–128
Taba S, Moromizato K, Takaesu Z, Ooshiru A, Nasu K (2006) Control of the southern root-knot nematode, Meloidogyne incognita using granule formulations containing nematode-trapping fungus, Monacrosporium ellipsosporum and a nematicide. Jap J Appl Entomol Zool 50:115–122
Takur M, Sohal BS (2013) Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN Biochem 2013:762412. https://doi.org/10.1155/2013/762412
Talavera M, Itou K, Mizukubo T (2002a) Combined application of Glomus sp. and Pasteuria penetrans for reducing Meloidogyne incognita (Tylenchida: Meloidogynidae) populations and improving tomato growth. Appl Entomol Zool 37:61–67
Talavera M, Mizukubo T, Itou K, Aiba S (2002b) Effect of spore inoculum and agricultural practices on the vertical distribution of the biocontrol plant-growth-promoting bacterium Pasteuria penetrans and growth of Meloidogyne incognita-infected tomato. Biol Fertil Soils 35:435–440
Thoden TC, Korthals G, Termorshuizen A (2011) Organic amendments and their influences on plant-parasitic and free-living nematodes: a promising method for nematode management? Nematology 13:133–153
Timper P (1999) Effect of crop rotation and nematicide use on abundance of Pasteuria penetrans. J Nematol 31:575; abstract
Timper P (2011) Utilization of biological control for managing plant-parasitic nematodes. In: Davies K, Spiegel Y (eds) Biological control of plant-parasitic nematodes: building coherence between microbial ecology and molecular mechanisms. Springer, London, pp 259–289
Timper P (2014) Conserving and enhancing biological control of nematodes. J Nematol 46(2):75–89
Timper P, Brodie BB (1994) Effect of host-plant resistance and a nematode pathogenic fungus on Pratylenchus penetrans. Phytopathology 84:1090; abstract
Timper P, Parajuli G (2012) Suppression of Meloidogyne incognita by Paecilomyces lilacinus is enhanced by planting cover crops. J Nematol 44:494–495; abstract
Timper P, Minton NA, Johnson AW, Brenneman TB, Culbreath AK, Burton GW, Baker SH, Gascho GJ (2001) Influence of cropping systems on stem rot (Sclerotium rolfsii), Meloidogyne arenaria and the nematode antagonist Pasteuria penetrans in peanut. Plant Dis 85:767–772
Timper P, Davis R, Jagdale G, Herbert J (2012) Resiliency of a nematode community and suppressive service to tillage and nematicide application. Appl Soil Ecol 59:48–59
Tobin JD, Haydock PPJ, Hare MC, Woods SR, Crump DH (2008) Effect of the fungus Pochonia chlamydosporia and fosthiazate on the multiplication rate of potato cyst nematodes (Globodera pallid and G. rostochiensis) in potato crops grown under UK field conditions. Biol Control 46:194–201
Trivedi PC, Barker KR (1986) Management of nematodes by cultural practices. Nematropica 16:213–236
Tzortzakakis EA, Goewn SR (1994) Evaluation of Pasteuria penetrans alone and in combination with oxamyl, plant resistance and solarization for control of Meloidogyne spp. on vegetables grown in greenhouses in Crete. Crop Prot 13:455–462
Van den Boogert PHJF, Velvis H, Ettema CH, Bouwman LA (1994) The role of organic matter in the population dynamics of the endoparasitic nematophagous fungus Drechmeria coniospora in microcosms. Nematologica 40:249–257
Verdejo-Lucas S, Sorribas FJ, Ornat C, Galeano M (2003) Evaluating Pochonia chlamydosporia in a double-cropping system of lettuce and tomato in plastic houses infested with Meloidogyne javanica. Plant Pathol 52:521–528
Viaene NM, Abawi GS (2000) Hirsutella rhossiliensis and Verticillium chlamydosporium as biocontrol agents of the root-knot nematode Meloidogyne hapla on lettuce. J Nematol 32(1):85–100
Viaene N, Coyne DL, Davies KG (2013) Biological and cultural management. In: Perry RN, Moens M (eds) Plant nematology, 2nd edn. CABI Publishing, Wallingford, UK, pp 383–410
Vieira Dos Santos MC, Curtis RHC, Abrantes I (2014) The combined use of Pochonia chlamydosporia and plant defence activators—a potential sustainable control strategy for Meloidogyne chitwoodi. Phytopathol Mediterr 53(1):66–74
Walker GE, Wachtel MF (1988) The influence of soil solarization and non-fumigant nematicides on infection of Meloidogyne javanica by Pasteuria penetrans. Nematologica 34:477–483
Walters DR (2011) Sounding the alarm: signaling and communication in plant defense. In: Walters DR (ed) Plant defense: warding off attack by pathogens, herbivores, and parasitic plants. Blackwell Publishing, Oxford, pp 77–124
Walters DR, Bennett AE (2014) Microbial induction of resistance to pathogens. In: Walters DR, Newton AC, Lyon GD (eds) Induced resistance for plant defense: a sustainable approach to crop protection. Blackwell Publishing, Oxford, pp 149–170
Wang KH, Sipes BS, Schmitt DP (2001) Suppression of Rotylenchulus reniformis by Crotalaria juncea, Brassica napus, and Tagetes erecta. Nematropica 31:235–249
Wang K-H, Sipes BS, Schmitt DP (2002) Management of Rotylenchulus reniformis in pineapple, Ananas comosus, by intercycle cover crops. J Nematol 34:106–114
Wang KH, Sipes BS, Schmitt DP (2003) Enhancement of Rotylenchulus reniformis suppressiveness by Crotalaria juncea amendment in pineapple soils. Agric Ecosyst Environ 94:197–203
Wang K-H, Mcsorley R, Gallaher RN, Kokalis-Burelle N (2008) Cover crops and organic mulches for nematode, weed and plant health management. Nematology 10(2):231–242
Weller DM, Mavrodi DV, van Pelt JA, Pieterse CMJ, van Loon LC, Bakker PAHM (2012) Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403–412
Westphal A (2011) Sustainable approaches to the management of plant-parasitic nematodes and disease complexes. J Nematol 43(2):122–125
Westphal A, Becker JO (2001) Soil suppressiveness to Heterodera schachtii under different cropping sequences. Nematology 3:551–558
Widmer TL, Mitkowski NA, Abawi GS (2002) Soil organic matter and management of plant-parasitic nematodes. J Nematol 34:289–295
Xu X-M, Jeffries P, Pautasso M, Jeger MJ (2011) Combined use of biocontrol agents to manage plant diseases in theory and practice. Phytopathology 101:1024–1031
Zaki MJ, Maqbool MA (1991) Combined efficacy of Pasteuria penetrans and other biocontrol agents on the control of root-knot nematode on okra. Pak J Nematol 9:49–52
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Moosavi, M.R. (2020). Efficacy of Microbial Biocontrol Agents in Integration with Other Managing Methods against Phytoparasitic Nematodes. In: Ansari, R., Rizvi, R., Mahmood, I. (eds) Management of Phytonematodes: Recent Advances and Future Challenges. Springer, Singapore. https://doi.org/10.1007/978-981-15-4087-5_10
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