Number of steinernematid and heterorhabditid species by continent and number and identity of the EPN species described from each continent since the year 2010 based on published data.
Abstract
Entomopathogenic and molluscoparasitic nematodes are important parasites of many insects and molluscs, respectively. Due to their infectivity, the possibility of mass production by industrial techniques and the relative safety to nontarget organisms and environment, these organisms represent an attractive agent for biological control of many pests. This chapter summarises the current knowledge of the diversity of these organisms. In this chapter, we review the recent advances in production, storage, application techniques genetic improvement and safety of these organisms.
Keywords
- nematodes
- entomopathogenic
- molluscoparasitic
- Steinernema
- Heterorhabditis
- Phasmarhabditis
- diversity
- occurrence
- rearing
- application
- safety
1. Introduction
Entomopathogenic nematodes (EPNs) in the families of
Over the past decade, a large number of new EPN species have been described from throughout the world. New lineages present a unique combination of characteristics and thus have a great potential for biological control of particular insect pests.
Mollusc-parasitic nematodes (MPNs) represent a taxonomically more diverse group, consisting of members of seven families (Agfidae, Alaninematidae, Alloionematidae, Angiostomatidae, Cosmocercidae, Diplogasteridae, Mermithidae and Rhabditidae). However, to date, only
This chapter provides thorough information about the diversity and biology of EPNs and MPNs. We also focus on the recent advances in production, storage and application techniques.
2. Overview of EPN and MPN biology and diversity
2.1. Diversity of entomopathogenic nematodes
EPNs are common in all types of soils and more frequently inhabit agricultural and secondary forest ecosystems, which represent suitable conditions for insect host populations. These organisms have a worldwide distribution [1]. Over the past few decades, numerous surveys were performed mainly in Europe [2] and North America [3]. However, recently a huge effort for the study of EPNs field occurrence was recorded from other continents of all zoogeographical regions. Results of these surveys increased rapidly a number of new described species, especially from South Africa, Ethiopian region [4], Southeast Asia, Indo-Malaysian region [5] and tropical areas in Neotropical region [6]. Over the past decade, regularly used DNA analysis facilitated discrimination of the morphologically almost identical sibling species.
This led to the tremendous increase in the known EPN diversity. From the year 2000, the number of the described steinernematids and heterorhabditids more than tripled from 25 to 92 and from 6 to 18, respectively (Figure 1). Understanding of EPNs diversity should be considered as a basic requirement for a successful field control of noxious insects.
It is generally accepted that steinernematids are more common in cooler, temperate zone whereas heterorhabditids prefer warmer, tropical and subtropical conditions (torrid zone) [7]. Geographically, the torrid zone lies between the Tropic of Capricorn and the Tropic of Cancer parched with heat. In this zone, many new species have been recently detected from Vietnam and southern China. Temperate zones contain the areas or regions between the tropic of Capricorn and the Antarctic circle or between the tropic of Cancer and the arctic circle, having a moderate climate. According to the number of described species, this zone seems to be the richest for the EPNs occurrence. Frigid zones represent the areas or regions between the Antarctic circle and the south pole or between the arctic circle and north pole, intensively cold, have probably a low EPNs occurrence represented only by several findings.
Continent | From 2010 | Species | |
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Africa | 16/6 | 11 |
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Asia | 52/5 | 14 |
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Australia | 3/4 | 0 | – |
Europe | 16/4 | 3 |
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North and Central America |
15/9 | 1 |
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South America | 15/4 | 5 |
The highest species diversity of the genus
2.1.1. Geographic distribution of EPN species
Several EPNs are known to have a cosmopolitan occurrence, such as
Species | Distribution |
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Worldwide, all continents |
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Worldwide, all continents |
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Worldwide, all continents |
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Worldwide, all continents |
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Worldwide, Australia, Africa, North America, Europe |
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Holarctic—USA, Argentina, Azores, China, Korea and Spain |
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Holarctic—Europe, Russia, Canada |
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Holarctic—Europe, Russia, Canada |
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Palearctic—Europe, Russia |
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Palearctic—USA, Europe |
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Palearctic—Europe, Russia |
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Palearctic—North America, Asia, Europe |
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Northern Africa, India |
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Central and Northern Europe, Turkey |
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Central and Southern Africa |
Central and Northern Europe, United Kingdom |
Bacterium | Nematode |
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Unknown |
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Unknown |
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Unknown |
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In contrast to ubiquitous species, the known geographic distribution of a majority of EPN species is much narrower, and some species are known just from a single country and even from a specific locality. This applies, for instance to
It is likely, that at least in some ubiquitous EPNs, their geographical distribution was recently enhanced by a human activity. This seems to be the case of
Unfortunately, the data on EPN diversity is partly influenced by the wrong identification of certain species. For instance, some EPNs originally described from South and North America, such as
2.1.2. Habitat preference
EPNs inhabit most terrestrial habitats, but their occurrence has been evaluated mainly in relation to soil type and habitat [20]. Interestingly, heterorhabditids were equally abundant in turf and weedy habitats, but never found in closed-canopy forest [21]. In Germany, the rate of prevalence of steinernematids was highest in woodland (50.3%) where
In general, the essential condition for the EPN occurrence and survival associates with biotic factors. Different species of EPNs occur in numerous habitats/ecosystems depending preferably on their insect host. It was demonstrated that at least some steinernematids show a distinct habitat preference that may reflect the distribution of suitable hosts, which are adapted for the habitat [7]. Even though, these nematodes are ubiquitous, their recovery from the field is influenced by a number of biotic factors, including nematode antagonists and host range that is dependent on the suitability for penetration of different insect hosts by nematodes, possibility of finding a suitable host in the habitats (e.g., leaf-feeding insects cannot be readily attacked in the natural habitat), and by the natural population density [25]. Till present, the impact of insect hosts has been, unfortunately, mostly overlooked. Insect aggregations and outbreaks of insect pests are a great opportunity to study EPN diversity and habitat preferences. Mráček and Bečvář [26] emphasised an essential impact of host aggregations on the incidence of EPNs. In their experiments, the high percentage, about 70%, of sampling sites with insect aggregations were nematode positive. Similarly, final mortality of the fly larvae and pupae from the bibionid (
Competition between EPN species can also have an impact on their distribution. It was shown that even though
2.1.3. Methods used for the study of EPN diversity
The outcome of the studies of EPN occurrence can be influenced by the method of isolation. A total of 40 soil samples from various habitats in Germany and the Czech Republic were studied for the presence of entomopathogenic nematodes using the
2.1.4. Symbiotic bacteria
Entomopathogenic nematodes (EPNs) of the families
Single species of
2.2. Mollusc-parasitic nematodes (MPNs)
Nematode parasites of molluscs (mollusc-parasitic nematodes) can be found in several families (e.g., Alloionematidae, Cosmocercidae, Mermithidae and Rhabditidae). Of these, only one species,
Similarly to entomopathogenic nematodes, most of MPNs spend a part of their life cycle in the soil environment. Nematodes that infect host in the soil need some mechanism how to find an appropriate host. Soil dwelling invertebrates movement is usually slow, but still too fast for the nematodes and thus, during their evolution, parasitic nematodes developed useful adaptations. As known from EPNs, also
Unlike EPNs, some MPNs are able to complete their life cycles in different organic matter in the soil. Naturally, the quality of the growing substrate affects nematode development, however, unlike in EPNs, the quality of the growing substrate is mostly expressed in the yield of dauer juveniles and not in the quality of progeny [42]. On the other hand, in EPNs, the substrate quality influences both yield and quality of IJs [44, 45]. The reason for this difference could be that while EPNs are the true parasites, MPNs retain both parasitic and free-living life cycles, and the ability to produce full quality dauer juveniles in a wide range of conditions is an essential advantage that helps them to survive in various changing environments.
2.2.1. Alloionematidae
Family Alloionematidae consists of three genera:
2.2.2. Cosmocercidae
The nematodes in the family Cosmocercidae are usually parasites of reptiles and amphibians, but two genera are known as mollusc-parasites, namely
2.2.3. Mermithidae
Mermithids are frequent parasites of many invertebrates in aquatic and terrestrial habitats, for example,
2.2.4. Rhabditidae
Rhabditidae is a large family consisting of many bacteriophagous free-living, phoretic and parasitic nematodes that are often associated with insects or terrestrial molluscs (e.g.,
3. Mass production
3.1. Entomopathogenic nematodes
An excellent review of the current situation regarding mass production of EPNs was published by Shapiro-Ilan et al. [57]. Therefore, in this chapter, we give only a short overview of the used methods.
The most simple method for EPN production is
For large-scale production, solid or liquid fermentation
EPN production in solid culture is usually performed in a three-dimensional rearing system with the liquid medium mixed with an inert carrier (e.g., pieces of polyurethane foam). Media were initially based on animal products (e.g., pig kidney) but were later improved by including various other ingredients (e.g., eggs, soy flour, peptone and yeast extract). The culture starts with the inoculation of the sterilised medium with bacteria followed by the nematodes. Nematodes are then harvested within 2–5 weeks by placing the foam onto sieves immersed in water. Only a few companies currently use this approach. A Chinese company Guangzhou Greenfine Biotechnology uses a solid culture method to produce several EPN species both for Chinese and international markets [57]. Other companies using this approach are Bionema (www.bionema.com), Andermatt Biocontrol AG (www.biocontrol.ch) and BioLogic USA (www.biologicco.com).
The
3.2. Molluscoparasitic nematodes
In slug parasitic nematodes, there are two species that can be easily produced in a large scale,
In vitro methods for mass production of
4. Formulation and application
4.1. Formulation of entomopathogenic nematodes
Entomopathogenic nematodes are always applied as infective juveniles and are mainly used for controlling the larval or pupal stages of insect pests in the soil or cryptic habitats. Under specific conditions, EPNs can successfully suppress also foliar pests [64].
EPNs have been classically applied in the form of aqueous suspension using sprayers, mist blowers, or irrigation systems. This approach turned out to have several limitations, mainly due to the sensitivity of the nematodes to desiccation and UV radiation [65]. For this reason, several alternatives improving formulation and application have been proposed and established.
4.1.1. Cadaver application
Insect cadaver application [66] has been proposed as a method enhancing EPN persistence. In this method, EPNs are applied in the infected insect host cadaver directly to the target site, and pest control is achieved by the infective juveniles that emerge from the host cadavers.
Insect cadaver application proved to be superior in EPN infectivity, survival, dispersal and pest control efficacy in some instances [67, 68]. EPN delivery can be further improved by formulating the infected hosts in coatings [69]. The cadaver application method has so far only been used commercially on a small scale relative to conventional methods [70], and it is especially useful for small- and medium-sized growers due to easier application and reduced storage costs [71].
Recently, the use of live insect hosts pre-infected with entomopathogenic nematodes against insect pests living in cryptic habitats was tested [72]. In this study, the release of the pre-infected lawn caterpillar,
4.1.2. Capsules
Formulation of EPNs in polymer-based capsules can protect EPNs from desiccation and UV radiation and from biotic stressors such as their natural enemies. This approach was first used with
The higher efficiency can be further achieved by addition of another compatible pesticide [58]. Also, the recently proposed ‘lure and kill’ approach based on the application of the nematodes in capsules with insect attractant may reduce the number of nematodes necessary to control the insect pest as has been shown [75]. These authors developed alginate capsules containing EPNs and buried them in the rhizosphere of maize (
4.1.3. Shelf life
Besides aforementioned cadaver and gel formulations, EPNs are formulated in water-dispersible granules, nematode wool, gels, vermiculite, clay, peat, sponge, etc. The formulation, together with nematode species, strongly affects the shelf life of the EPN-based products. Actively moving nematodes are metabolically very active and use energy reserves soon [77]. Thus, they can remain alive and infective for 1–6 months under refrigeration ranges. EPNs with reduced mobility (formulations in gels) are still infective after up to 9 months of storage, whereas EPNs formulated in partial anhydrobiosis (formulations in water soluble powders) remain so for up to 1 year.
The root exudates were revealed to induce quiescence in EPNs that is reversible after placing the IJs in soil with high water content [78]. This approach could be used to prolong the shelf life of beneficial entomopathogenic nematodes (EPNs).
4.2. Formulation of molluscoparasitic nematodes
As was mentioned in the previous subchapter, the only commercial product based on MPNs (
General recommendation is to apply
There are various strategies for the application. Common strategy is to apply the nematodes over the whole soil surface, and the alternative strategies are based on local applications. Slugs,
4.3. Genetic improvement
Genetic improvement has been an important contributor to the enormous advances in productivity that have been achieved over the past 50 years in plant and animal species that are of agricultural importance [88]. For entomopathogenic nematodes, main target characteristics are virulence, host range, heat and desiccation tolerance and shelf life. Glazer [89] summarised the four potential genetic-manipulation strategies: artificial selection, hybridisation, mutation and recombinant DNA techniques. Because it is unlikely that a transgenic EPN strain would meet public acceptance as a control agent [90], hybridisation and selective breeding are the most promising approaches to enhance EPN characteristics.
In a pioneer selection study performed with EPNs, the host-finding ability of
Many studies also attempted to enhance EPN tolerance to environmental stresses. Ehlers et al. [93] enhanced the low-temperature activity of
Ehlers et al. [93] increased the mean tolerated temperature from 38.5 to 39.2°C. (The heritability for heat tolerance was 0.68 and for activity at low temperature 0.38). Salame et al. [92] bred a heterogeneous population of the EPN
Perry et al. [90] concluded that screening among natural populations for high tolerance to desiccation is a feasible approach and cross-breeding and genetic selection can further improve tolerance. However, there is a crucial question of the stability of selected traits. In
According to Glazer [89] for EPNs, we lack markers to follow transfer or enhancement/degradation of traits and to identify ‘beneficial genes’ that can be transferred between populations. Further fundamental research in the field of the genetic architecture of key traits, such as infectivity, stress tolerance and reproduction, is needed.
Thanks to recent advances in EPN and bacteria genomics [99] it will be possible to determine genes from the whole genome that are being expressed, in order to detect those that are involved in a particular process and target them through genetic engineering methods.
4.4. Safety
Entomopathogenic nematode-bacteria complexes are pathogens capable of invading and killing a large number of insects and even other arthropods, for example, spiders, ticks and millipedes [100]. It is thus necessary to establish the risk that these organisms applied for pest control pose to the environment and nontarget organisms.
Numerous studies have assessed the effect of these complexes on nontarget invertebrates, animals and humans and environment, and several conclusions can be drawn. The available data show that entomopathogenic nematode-bacteria complexes are generally safe to humans and animals, and their impact on nontarget insects and other invertebrates seems to be limited. An excellent review on this topic was given by Akhurst and Smith [101]. In this chapter, we shortly review the current knowledge and stress some recent findings.
4.4.1. Safety to the environment
Negative effect to the environment is likely to be much stronger if the introduced nematode establish in the target locality. Therefore, the establishment potential of the introduced beneficial nematodes represents a very important part of the risk assessment. The available information, however, is quite scarce and inconsistent. It has been shown that
4.4.2. Safety to nontarget invertebrates
According to Bathon [106], the mortality of nontarget animals in the field may occur, but will be temporal, spatially restricted, affecting a part of the population, and its impact can be considered negligible. Piedra-Buena et al. [107] stated that the impact of EPNs in general on organisms considered ‘non-target’ is limited, with infections only occurring when these organisms are exposed to very high concentrations and under laboratory conditions.
Laboratory experiments have shown that EPNs can negatively affect a large number of invertebrates, including predatory insects [108], parasitoids [109, 110], Symphyla, Collembola, Arachnida, Crustacea, Diplopoda [111], terrestrial isopods, millipedes and Gastropods [112]. However, the field data generally show none or only a small reduction in field populations of nontarget species after applications of entomopathogenic nematodes [113, 114].
In a recent study, Dutka et al. [115] reported that
4.4.3. Safety to humans and animals
Entomopathogenic nematode-bacteria complexes are generally considered safe to humans and animals. Many studies assessed the effect of EPNs on vertebrates. EPNs were applied orally, subcutaneously, peritoneally and intracerebrally to various vertebrates. In poikilotherms, the nematode application had usually no negative effect, with the exception of tadpoles, where nematode application caused mortality [117, 118]. However, the mortality was associated not with
The safety of bacterial symbionts has been tested by oral, intradermal, subcutaneous and intraperitoneal applications of the bacterial cells to various model vertebrates generally producing no adverse effect [120, 121]. There is, however, one exception, being
However, later studies identified also symbiotic strains of
European environmental risk assessment (ERA) excludes
Other commercially produced heterorhabditids,
Very recently, Gengler et al. [130] have revealed the capacity of EPNs to act as an efficient reservoir ensuring exponential multiplication, maintenance and dissemination of the human pathogenic bacterium
4.4.4. Phasmarhabditis hermaphrodita
The effect of commercial strain of
4.5. Synergy with other biocontrol agents
Entomopathogenic and mollusc-parasitic nematodes are widely used in integrated and biological pest control systems. Entomopathogenic nematodes are relatively resistant to many pesticides in recommended dosage, except for some, for example, carbamates [82], and some authors reported synergy between EPNs and chemicals [139, 140]. But they are also influenced by many, especially soil dwelling, micro- and macro-organisms that can hardly suppress [141–143] or synergistically support them [144].
Synergy between entomopathogenic nematodes and other bio-agents are in great demand because this strategy can significantly reduce application rates and increase efficacy [145] that leads to higher economic profit. The great example of synergy between EPN
Synergistic effects were also found between EPNs and entomopathogenic bacteria
Interestingly, the use of combination of several EPN species has been shown to increase the efficacy against insect pests. There was a very strong synergy of
Reports of synergy of EPNs and arthropod bio-agents are slightly less frequent, maybe because of the ability of EPNs to infect many of these organisms, but despite this there are some successful combined applications that clearly show synergistic effect [154]. These authors reported positive effect of combined application of predatory mite
Expectably there was also synergism of EPNs in combination with GM plants [155]. Entomopathogenic nematodes are not negatively influenced by the GM plant and can infect all soil-dwelling stages of insect pest that survive or avoid the effect of GM plant (e.g., Bt-corn) that results in higher efficacy of biocontrol.
Even though there are some reports of antagonism among nematodes and other bio-agents, we can say that, in general, higher diversity of predators and similarly also pathogens leads to better control of many pests [156], thanks to the synergy of their effects on pest populations. Conservation of natural enemies may carry additional benefits for biological control.
Acknowledgments
This chapter was completed with the support of the Czech Ministry of Education, Youth and Sport in the programme Czech-Israeli Cooperative Scientific Research, project 8G15006.
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