Dr. Pletser’s experience includes 30 years of working with the European Space Agency as a Senior Physicist/Engineer and coordinating their parabolic flight campaigns, and he is the Guinness World Record holder for the most number of aircraft flown (12) in parabolas, personally logging more than 7,300 parabolas.
\\n\\n
Seeing the 5,000th book published makes us at the same time proud, happy, humble, and grateful. This is a great opportunity to stop and celebrate what we have done so far, but is also an opportunity to engage even more, grow, and succeed. It wouldn't be possible to get here without the synergy of team members’ hard work and authors and editors who devote time and their expertise into Open Access book publishing with us.
\\n\\n
Over these years, we have gone from pioneering the scientific Open Access book publishing field to being the world’s largest Open Access book publisher. Nonetheless, our vision has remained the same: to meet the challenges of making relevant knowledge available to the worldwide community under the Open Access model.
\\n\\n
We are excited about the present, and we look forward to sharing many more successes in the future.
\\n\\n
Thank you all for being part of the journey. 5,000 times thank you!
\\n\\n
Now with 5,000 titles available Open Access, which one will you read next?
Preparation of Space Experiments edited by international leading expert Dr. Vladimir Pletser, Director of Space Training Operations at Blue Abyss is the 5,000th Open Access book published by IntechOpen and our milestone publication!
\n\n
"This book presents some of the current trends in space microgravity research. The eleven chapters introduce various facets of space research in physical sciences, human physiology and technology developed using the microgravity environment not only to improve our fundamental understanding in these domains but also to adapt this new knowledge for application on earth." says the editor. Listen what else Dr. Pletser has to say...
\n\n\n\n
Dr. Pletser’s experience includes 30 years of working with the European Space Agency as a Senior Physicist/Engineer and coordinating their parabolic flight campaigns, and he is the Guinness World Record holder for the most number of aircraft flown (12) in parabolas, personally logging more than 7,300 parabolas.
\n\n
Seeing the 5,000th book published makes us at the same time proud, happy, humble, and grateful. This is a great opportunity to stop and celebrate what we have done so far, but is also an opportunity to engage even more, grow, and succeed. It wouldn't be possible to get here without the synergy of team members’ hard work and authors and editors who devote time and their expertise into Open Access book publishing with us.
\n\n
Over these years, we have gone from pioneering the scientific Open Access book publishing field to being the world’s largest Open Access book publisher. Nonetheless, our vision has remained the same: to meet the challenges of making relevant knowledge available to the worldwide community under the Open Access model.
\n\n
We are excited about the present, and we look forward to sharing many more successes in the future.
\n\n
Thank you all for being part of the journey. 5,000 times thank you!
\n\n
Now with 5,000 titles available Open Access, which one will you read next?
\n'}],latestNews:[{slug:"stanford-university-identifies-top-2-scientists-over-1-000-are-intechopen-authors-and-editors-20210122",title:"Stanford University Identifies Top 2% Scientists, Over 1,000 are IntechOpen Authors and Editors"},{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"}]},book:{item:{type:"book",id:"3492",leadTitle:null,fullTitle:"Climate Change and Regional/Local Responses",title:"Climate Change and Regional/Local Responses",subtitle:null,reviewType:"peer-reviewed",abstract:"Understanding climate change requires analysis of its effects in specific contexts, and the case studies in this volume offer examples of such issues. 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1. Introduction
Termites belong to the order Isoptera [1] and include more than 3500 species described in the world [2]. Some of them play beneficial roles to man [3, 4], but some cause to him significant economic losses [5]. In both cases, there are different termites considering their habitats and caste type. In recent years, there has been a large increase in the scientific literature concerning termites [6]. The control of species of termites with detrimental effects relies mainly on soil chemical termiticide applications, especially in African countries. But despite this reliance on chemical termiticides, termite control strategies need to conform to higher environmental standards [7]. In this regard, several research projects focus their activities on biological control methods which are environmentally safe. Among these methods is the use of entomopathogenic nematodes (EPNs). These nematodes have a worldwide distribution [8]. Apart from being environmentally safe, the use of EPN in pest control in general, and in termite control in particular, is rapid, sustainable, and cost effective. For the use of EPNs to control termites, different research methodologies are considered. But the results of these researches are sometimes controversial. This is related to the origin and biology of the species of the nematodes, to the type of termites, but also to the environment where the nematodes have been applied. Usually, newly described EPN species are first tested under laboratory conditions before best isolated are selected and tested under field conditions. Even under those conditions, methodologies used to evaluate the performance of the nematodes vary with researchers [9], leading to different results. The current review paper gives information on termites with focus on those with detrimental effects to man. It also discusses several methodologies commonly used to study the characteristics and also the performance of EPNs in the control of termites.
2. Termites
2.1. Classification and distribution of termites
Like ants, wasps, and bees, termites are social insects. They constitute 10% of all animal biomass in the tropics. Baker and Marchosky [10] divided termites into three general categories based on their habitat: dampwood, drywood, and subterranean termites. A typical termite colony contains larvae, nymphs, workers, soldiers, and reproductives, each type having its specific role inside the nest. Termites are grouped into seven families and 15 subfamilies [11], 281 genera [12], and over 3500 species identified worldwide [13]. Africa has the richest intercontinental diversity of termites with over 70% of all the identified species [14]. The family Termitidae alone comprises more than 664 African species grouped in four subfamilies: Apicotermitinae with 70 species [15], Termitinae with 272 species [16], Macrotermitinae with 165 African fungus-growing termites [17], and Nasutitermitinae with 56 species [18]. The total number of species of termites in the four subfamilies may surpass 90% of the world’s known termite species [14]. These authors reported species richness and diversity (see below the formulas for their calculation) as a result of the friendly climatic conditions in Africa, and that, dry climate is a factor contributing for low numbers of termite species in some regions of the world. For example, termite species diversity is lower in Northern Africa compared to Eastern, Western, and Southern regions of the continent [14]. Kemabonta et al. [19] also reported that termites are prominent in both tropical and subtropical ecosystems, but highest diversity is observed in tropical forests where they build very complex communities [16]. In recent years, there has been a large increase in the scientific literature concerning termites [6]. The different researches done on termites indicated their beneficial activities as well as detrimental effects to man.
Formulas are used to calculate termite species richness and diversity according to Ref. [19].
Termite species richness is calculated using the Shannon-Wiener diversity Index (H′) as follows:
H′ = −Σ (Pi ln Pi), where Pi is the proportion of individuals found in the ith species, while ln is the natural logarithm.
Termite diversity D is calculated using the Simpson index as D=∑i=1S−1/NN−1, where ni is the number of individuals in the ith species, while N is the total number of entities in the dataset.
2.2. Beneficial activities of termites
Termites play a major role in peoples’ lives, in physical as well as spiritual aspects [20]. Reis de Figueirêdo et al. [21] cataloged 43 species of termites, belonging to four families used in human diet and/or in livestock feeding and nine species used as a therapeutic resource. These authors registered termite use in 29 countries over three countries: Africa (19), America (5), and Asia (5). Authors of Refs. [4, 5] reported that termites are of highly nutritive value. Their soil is often eaten by pregnant women in Africa [20]. Termites also play a role as oracle, in superstitious beliefs, art, and literature [20]. Their mounds are often associated with the spiritual world, especially containing the spirits of ancestors. In agriculture, termites produce organic matter from dead wood and woody tissues of plants, thereby restore organic matter to the soil and to air, serve as ecological indicators [22]. They play significant role in subsistence agriculture as their mounds, with nutrient enriched soils, are incorporated into traditional cropping systems. Termite mound materials are also made hard and used to make roads, tennis court, and bricks used in buildings and are also source of pottery clay [23]. In this book chapter, we will focus on termites as pests and their control.
2.3. Detrimental activities of termites
More than 300 species of termites are known to be of economic importance [5] causing billions of dollars in damage worldwide. Since their food supply is mainly wood and woody tissues of plants, they feed on anything containing cellulose component including crop residues, mulches, and humus. They cause damage to agricultural crops such as cash crops and food crops [2], timbers in buildings, fences, clothes, books [24], removal of plant covers exposing soil surface to erosive forces [25]. They cause economic losses by directly injuring and destroying both living and dead vegetation and can damage right from sowing the crops till harvest [26].
Baker and Marchosky [10] reported drywood and subterranean termites as the most significant and costly termite pests. They feed on a wide range of living, dead, or decaying plant material [16, 27], including the consumption and turnover of large volumes of soil rich in organic matter and fungi. These feeding habits make termites important ecosystem engineers, which over long periods of time can modify the physical properties of soil such as texture, water infiltration rates, and nutrient content [28]. They are among the most important insect pests in forests, and many destructive species live in the soil. For example, the forest termite Coptotermes acinaciformis causes more than 92% of total loss to Virgin Eucalyptus pilularis. In 2011, wood-eating termites consumed more than $220,000 worth of Indian rupee notes [29].
In West Africa, several species of termites, including Macrotermes bellicosus, Macrotermes natalensis, Coptotermes sjostedti, and Pseudocanthotermes militaris, have been reported as general pests of living trees. The establishment of eucalyptus is limited by two termite species, i.e., Ancistrotermes cavithorax and Amitermes evincifer in drier areas of Ghana. In this country, termite attack of living trees is a potentially important problem facing the use of exotic forest species. In Nigeria, termite pest species of the genus Macrotermes are the most destructive to plants causing 5–18% yield losses [3]. Ten species of termites were found associated with citrus orchards in Benin: Amitermes guineensis, Ancistrotermes crucifer, Angulitermes truncates, Coptotermes intermedius, Cubitermes sp., M. bellicosus, Microcerotermes progrediens, Pericapritermes sp., Trinervitermes occidentalis, and Trinervitermes trinervius [30]. Among these, M. bellicosus, a fungus-growing termite, is the most important species that undermines citrus production and T. occidentalis, a grass-feeder termite, the most important to maize, cassava, groundnut, and bean grown under citrus canopies [31]. Abe et al. [2] also reported that the most troublesome termites in agriculture are the fungus-growing termites. In the absence of crop residues, mulches, and humus, these termites eat live plant material as groundnuts, millets, and maize. Odontotermes erraticus, Macrotermes sibhyalinus, Amitermes evuncifer, Psammotermes hybostoma, and Microtermes lepidus with a wide predominance of the O. erraticus were found ravaging cassava in Tivaouane, Senegal [32]. In South Africa, Coptotermes spp., Cryptotermes spp., and Neotermes spp. were observed undermining crop productivity [33]. But since termites make openings to the outside, farmers are aware of their presence only at an advanced stage of their invasion [34]. In regard of all this, the menace of termite activities is enormous. It is then important to bring these activities to a manageable level. For experimental purposes, termites are collected and used immediately or maintained for days before use.
2.4. Termite collection and maintenance
Termites are cryptic social insects. If some of them live in galleries made on the surface of wood products (examples of plant stems and trunks), some others live deep in the soil or inside wood products. Methods for collecting them will therefore depend on their habitat structures. Wang et al. [35] collected subterranean termites, Reticulitermes flavipes and Coptotermes formosanus, using cardboard bait buried in the field infested with termites. For the same type of termites, El-Bassiouny et al. [36] used El-Sebay’s [37] modified trap. Baimey et al. [31] broke at the top nests made by T. occidentalis and M. bellicosus in citrus orchards to collect directly workers and soldiers of the termites. Alternatively, these authors covered broken nests with dried straws. The straws were left well colonized by termites for 3–4 h and then termites were easily collected. For experiments designed to evaluate the nest reconstruction by termites following the break, it is advised to measure the height and surface denuded by the termites prior to breaking the nests.
Termites are usually collected in plastic containers, transferred to the laboratory where they are kept for given period of time before they are used for experiments. Authors of Refs. [31, 38] advised to put in the containers some moistened piece of paper as source of cellulose for the termites and also wet sand collected from termite nests. They also advised to keep the containers slightly open for aeration and in the dark at 25°C and 75–80% RH for 24 h before very active individuals are selected for experiments. El-Bassiouny et al. [36] rather kept termites at 25–28°C for 7 days in 9-cm diameter Petri dishes containing moistened corrugated cardboard before selecting active and vigorous individuals for use. Razia et al. [39] kept in the laboratory at 21–25°C workers of R. flavipes and Odontotermis hornei in plastic containers with 1–2 cm deep vermiculite sand and corrugated wood blocks added. Faye et al. [32] used sterilized soil (wetted soil heated to 80°C over a wood fire) on the surface of which vegetable debris was placed as culture media for Odontotermes spp.
2.5. Methods of control of termites
In response to the destructive activities of termites, man developed several preventative and remedial methods which are currently used against the pests [23]. Billions of dollars are spent annually throughout the world in this regard [26].
Chemical methods are practices frequently used against termites [40]. The methods rely on the use of synthetic chemicals such as dichloro diphenyl trichloroethane (DDT), benzene hexachloride (BHC), aldrin, dieldrin, soil barrier termiticides, dust and fumigant, treated zone termiticides [41]. These pesticides give quick control effects when they can reach termites but are costly, hazardous, and environmentally not safe. Therefore, despite this heavy reliance upon the application of chemical termiticides, future termite control technologies need to conform to higher environmental standards [7].
The most common nonchemical termite control method is the destruction of termite nests [42] because termites build epigeous mounds that affect cultivation and farm preparation [41]. This implies breaking and digging out the mound to reach and kill the reproductive queen and king of the nest [42]. But this method showed limitations as comeback is experienced after a period of time for some groups of termites that are capable of grooming new queen and king (Cubitermes and Macrotermes). Other nonchemical termite control methods include botanical termiticides [43], intercropping, crop rotation, planting of resistant crops [44], physical methods, i.e., debris removal, mechanical barriers, heat, high voltage electricity or electrocution, wood replacement, and biological control, i.e., use of predators [45], biological control agents such as fungi [46], bacteria, and nematodes [31, 35]. In a partial review, Myles [47] reported 2 viruses, 5 bacteria, 17 fungi, 5 nematodes, and 4 mites that have the potential to kill termites; the full list of these organisms being no doubt larger. But Weeks and Baker [48] reported that the behavior of termites affects the success of biological control. Lenz et al. [46] also reported that to be effective, biological control agents should be virulent, tolerate temperatures above 30°C, pose no health threats to man and higher animals, be easy mass produced and easy formulated, applied, and stored. Lacey et al. [49] observed that fast host killing ability, increased environmental persistence, long shelf life, good fitness into integrated systems, acceptance by growers, and general public are also parameters to consider. This book chapter will focus on the use of entomopathogenic nematodes as biological control agents against termites of economic importance in agriculture.
3. Entomopathogenic nematodes
3.1. Classification and distribution of entomopathogenic nematodes
Entomopathogenic nematodes (EPNs) are soil-inhabiting microorganisms. They have been isolated from all continents (except the Antarctic) and from a wide range of soil habitats: fields, forests, grasslands, desert, and ocean beaches [50]. They have been described from more than 40 nematode families. But only the Steinernematidae and Heterorhabditidae families have received the most attention because they possess several attributes of effective biological control agents [51, 52]. The family Steinernematidae contains two genera, i.e., Steinernema with more than 100 species and Neosteinernema with only one species, Neosteinernema longicurvicauda as parasite of termites [53]. The family Heterorhabditidae contains one genus, Heterorhabditis, with more than 20 species. The list of EPN species described in the world being too long, we give here only those reported from Africa. In Africa, to our knowledge, EPNs have been observed in Algeria, Benin, Cameroon, Egypt, Ethiopia, Kenya, Morocco, Nigeria, Rwanda, South Africa, and Tanzania (Table 1).
S. citrae; S. khoisanae; S. yirgalemense, H. zealandica and H. bacteriophora S. khoisanae and H. bacteriophora H. safricana S. beitlechemi S. fabii S. innovationi S. jeffreyense S. sacchari S. tophus H. noenieputensis S. nguyeni
Species of entomopathogenic nematodes isolated in Africa.
S. = Steinernema; H. = Heterorhabditis.
3.2. Advantages of the use of entomopathogenic nematode
Entomopathogenic nematodes have several distinct advantages over other forms of pest control in that they have a broad host range are easy to mass produce in vivo and in vitro [83] and to store. The use of EPNs for insect pest control is a rapid, sustainable, environmentally safe, and cost-effective method [84]. The nematodes can be applied with standard spray equipment in open environment [83, 85]. They are effective against a number of insect pests that occur in cryptic habitats including termites, having a high degree of safety among vertebrates and other non-target organisms [86]. Also, they have the potential to recycle in the environment, are amenable to genetic selection for desirable traits, and are exempt from registration in many countries [86, 87]. They are compatible with many chemical pesticides: herbicides, fungicides, acaricides, insecticides, nematicides [88–91], azadirachtin [92], Bacillus thuringiensis products, and pesticidal soap [93]. They are also compatible with many biological pesticides [86, 87] and with some parasitoids [49, 94]. Synergistic interaction between EPNs and other control agents has been observed for various insecticides [95, 96] and pathogens [97, 98].
3.3. Characteristics of entomopathogenic nematodes
Species of EPNs of the genera Steinernema and Heterorhabditis are successfully used to control insect pests. The IJs of the nematodes (the stage used as biopesticide) live symbiotically with bacteria of the genera Xenorhabdus and Photorhabdus, respectively [99]. They are nonfeeding and the only stage observed in the soil. They rely solely on energy reserves for survival and infectivity [100]. Their efficacy in the control of insect hosts is dependent on their attack strategy, survival, and persistence [101]. They use “sit and wait” (ambush foragers = most Steinernema nematodes), cruise (most Heterorhabditis nematodes), or intermediate foraging (some Steinernema nematodes) strategies to attack their insect hosts. Once inside the host haemocoel, the IJs of the nematodes release their symbiotic bacteria which proliferate and kill the host by septicemia within 48 h postinfection. Proliferated bacteria serve as source of food for the nematodes [102]. Also, these bacteria protect the host cadaver from colonization by other microorganisms including late arriving nematodes. Zhou et al. [103] reported that bacterial products from both Xenorhabdus and Photorhabdus make the infected insect repellent to ants. Fenton et al. [104] observed the protection of Heterorhabditis bacteriophora-infected cadavers from the avian predator, the European robin Erithacus rubecula. The authors reported that this protection was attributed to the red color reinforced by unpalatable taste of the cadavers and that the fact that the birds did not need to bite cadavers to reject them implies that some deterrent factor is emitted through the cadavers’ cuticles. Thus, it is a nematode/bacterium complex that works together as a biological control unit to kill an insect host [85]. Insect susceptibility to EPN varies with insect species and is influenced by nematode species and strain [48]. Good knowledge of the IJs of EPNs and also of the relationships between IJs-insect-bacteria will allow increasing efficacy of treatment used to limit populations of pests [101]. Several researches are done in this regard using different protocols. The overall objective of these researches is to minimize pest populations to reduce losses they caused to crops. In countries where EPNs are observed and identified for the first time, researches usually start with the study of their biology under environmental extreme conditions in laboratory. This allows predicting which nematode isolate or species to use in target areas where environmental stress is expected.
3.4. Environmental stresses and their effect on the performance of entomopathogenic nematodes and their symbiotic bacteria
Authors of Refs. [48, 105] reported that the prevalence of infective juveniles (IJs) of EPNs in different habitats is affected by both intrinsic (behavioral, physiological, and genetic characteristics) and extrinsic (antibiotics, competition, natural enemies, temperature, soil moisture, pH, soil type, soil texture, relative humidity, UV radiation, and desiccation) factors. For experimental purposes, performance of EPNs is known by studying their ability to withstand conditions of drought, lack of oxygen, tolerance to heat [38, 106], capacity to search for targeted pests in the soil at specific concentration [107], to kill them, and to multiply inside them. The nematodes’ tolerance to biotic factors is also studied under laboratory conditions. Most of the experiments designed in this regard are conducted using the larvae of the greater wax moth Galleria mellonella Linnaeus (Lepidoptera: Pyralidae), a model insect for EPN biology and pathogenicity studies [108]. Nematode isolates that perform best under laboratory conditions are then taken to semi-controlled and fields conditions [31, 36, 45] and tested against insect pests in biological control programs [31, 36, 106, 109, 110]. Grewal et al. [111] observed greatest performance of indigenous EPN isolates as compared to exotic ones for the control of insect pests for being used in their natural environment.
To evaluate the tolerance of IJs of indigenous EPNs to environmental stresses, the nematodes are subjected to temperatures varying between −5 and 40°C [38, 112–116], to hypoxia [38, 117], to dehydration/desiccation for up to 75% RH [118, 119], and to ultraviolet radiation stress (for example, at 340 nm, [120]). The persistence or longevity of indigenous EPN species in the soil [121], their genetic improvement, their infectivity [118, 119, 122], trehalose content/accumulation [123], motility, development, virulence, and reproduction inside insect hosts [124] under environmental stresses are some traits that are often evaluated. Antagonists [125], soil type [126], cultural conditions [127], and nematode species of strain [128] also affect nematode survival in soil. Studies on the symbiotic bacteria of EPNs include evaluation of growth and virulence of the bacteria under heat and cold temperatures [124]. All these different experiments are not only conducted mainly under laboratory [38, 106, 109, 118, 119] but also under greenhouse and field conditions [129, 130] either in open environments or in the dark [124].
The results from the different experiments are controversial and show variations for the potential of the nematode IJs to tolerate environmental stresses. This could be explained by differences among species and a great variability within species of EPNs, insect hosts, and also environmental stresses used in different experiments. Authors of Refs. [51, 131] reported moisture, temperature, foraging strategy, and pathogenicity for the targeted insect as the four most critical factors. Under adequate range of temperatures and moisture and with a susceptible host, EPNs with cruiser and intermediate foraging strategies are suitable for use in subterranean and certain aboveground habitats (foliar, epigeal, and cryptic habitats), while ambushers will be most effective in cryptic and soil surface habitats [132]. Authors of Refs. [122, 133] reported that temperatures of ca. 15–30°C provide highest and most stable survival (more than 95%) to nematodes’ IJs than temperatures of ca. −5 to 10°C which reduce the nematodes’ movement. Shapiro-Ilan et al. [134] reported significant contribution of the ability of EPNs to tolerate freezing conditions (−2°C for 6 or 24 h) to their biological control efficacy. But these authors did not observe any relationship between freezing and desiccation tolerance. This observation did not corroborate that of Solomon et al. [135] and Grewal et al. [136] who reported that tolerance to cold and desiccation is related in EPNs and that both stress factors cause an increase in trehalose levels, which is implicated as a physiological protectant. At high temperatures of ca. 35–40°C, nematode physiological activity is high, increasing the consumption of its stored energy and resulting in limited shelf life [112] and low searching [137] and pathogenicity [138] potential of the nematodes. Hang et al. [124] observed nematode IJs’ development to adult at 13, 18, 24, 30, and 35°C and progeny production at 18, 24, and 30°C but not at 13 or 35°C. Zadji et al. [38] evaluated heat tolerance of 29 Benin isolates of H. sonorensis and one of Heterorhabditis indica under laboratory conditions using a method modified from Ref. [139]. Nematodes were subjected to 40°C for 2, 4, 6, and 8 h while being shaken at 70 rpm. The greatest survival of infective juveniles to heat (8 h), desiccation (8 h), and hypoxia (72 h) was observed with H. sonorensis isolates (72.8, 72.5, and 81.5%, respectively). Desiccation is important to conserve nematode IJ energy and improve their shelf life [140]. However, dehydration presents many challenges including difficulty in application because the carriers can block spray nozzles [141]. Genetic improvement of H. bacteriophora in beneficial traits as heat and desiccation tolerance by cross breeding and genetic selection is also reported. An overall increase in mean heat tolerance of 5.5°C by cross breeding five strains of the nematode species has been observed. But this enhanced heat tolerance and also tolerance to desiccation are often lost again during mass production. Fortunately, for Heterorhabditid nematodes, methods have now been developed to stabilize the traits by selection of tolerant inbred lines. This technique provides a pathway to genetic improvement of commercial strains which will maintain the improved characters also during in vitro mass production. For Steinernematid nematodes in contrast, the technique needs more investigation as these nematodes are amphimictic and production of inbred lines is much more laborious. Shapiro-Ilan et al. [139] reported that the effect of hypoxia on nematode IJs’ survival varied significantly with duration of exposure of the nematodes to stressed conditions and with nematode isolates from 33.2 to 81.5% and from 85.9 to 96.9% after 24 and 72 h of exposure, respectively. Entomopathogenic nematodes are sensitive to UV light. This is why they are usually applied to protected environments, particularly soil [86, 142]. But extended persistence of nematode IJs in the soil results in greater cumulative insect host mortality and reduced need for multiple nematode applications.
3.5. Mass production of entomopathogenic nematodes for laboratory and field application
Before EPN isolates with desirable characteristics such as tolerance to environmental stresses and virulence to insect hosts are used for experiments or for commercialization [143], they are cultured in vivo or in vitro at a small scale [144] or at a large scale [145].
3.5.1. In vivo production
For laboratory use and small-scale field experiments, in vivo production of EPNs appears to be appropriate method. Though various caterpillars and large beetle larvae are very susceptible insects to EPNs, for most laboratories and some field experiments, EPNs are mostly reared in last instar larvae of the greater wax moth, G. mellonella as described by Kaya et al. [144]. The larvae of G. mellonella can be produced using an artificial medium containing 22% ground wheat, 22% ground maize, 11% honey, 11% glycerol, 11% milk powder, 5.5% yeast extract, and 17.5% bee wax in a glass jar at 25°C in the laboratory [146]. The larvae of this insect are preferred because they are very susceptible to the nematodes and very easy to mass rear, they are commonly sold as fish bait. Nematode-infected larvae are incubated for around 72 h at 25-27°C before being transferred onto White trap. Hundreds of thousands of IJs of the nematodes emerge from infected G. mellonella larvae as progeny in few days [31, 109]. Emerged nematodes are collected [36, 39, 106] and used immediately [31] for experiments. They may be stored in tissue culture flask at 13°C [36, 115, 147] or at 19°C [39] and are used within 5 days [36, 39] or 2–6 weeks [109, 145] after collection. Though in vivo production of EPN is simple, reliable and results in high quality nematodes, the method is labor intensive and costly.
3.5.2. In vitro production
In vitro method of nematode production is used when large-scale production is needed at reasonable quality and cost. Two methods are used for in vitro production of EPN, i.e., solid media and liquid fermentation [148, 149]. The first method uses crumbed polyether polyurethane foam coated with a nutritive medium and inoculated first with symbiotic bacteria and then with nematodes. This method requires limited experience, its capital costs are low and logistics of production is flexible. The liquid fermentation method has the lowest mass production cost and is used by large companies with multiple products. The method relies on suitable medium composed of yeast extract as nitrogen source, a carbohydrate source as soy flour, glucose, or glycerol, lipids of plant or animal origin and salts and requires adequate oxygen [150, 151]. The following EPN species have been successfully produced using liquid fermentation method with yield capacity as high as 250,000 infective juveniles/ml: Steinernema carpocapsae, Steinernema riobrave, Steinernema kushidai, Steinernema feltiae, Steinernema glaseri, Steinernema scapterisci, H. bacteriophora, and Heterorhabditis megidis in 7500–80,000 liter bioreactors. Ehlers [152] reported that industrial-scale in vivo EPN production is applicable in developing countries and the large-scale in vitro production best suited for countries with low labor costs or for serving high value markets.
3.6. Storage and formulation of entomopathogenic nematodes
When nematodes are not to be used immediately, they are kept in appropriate conditions for a while to avoid their deterioration. Several methods are used to store EPNs for extended periods or to formulate them immediately following their mass production. But before they are stored or formulated for successful control of insect pests, the quality (i.e., viability based on their movement, energy reserves, and infectivity) of IJs of the nematodes is checked. Authors of Refs. [100, 153] reported the one-on-one (one nematode to one G. mellonella larvae) sand-well assay. The energy reserves (dry weight and total lipid content) are predictors of nematode longevity. Because each nematode species has its specific requirements for temperature, moisture and oxygen [112, 140, 154, 155], it becomes difficult to obtain a formulation or storage condition suitable for all EPN species. Nematodes are stored on moist sponge, in formulations that contain alginate, vermiculite, clays, activated charcoals, polyacrylamide, and water dispersible granules or are partially desiccated in water dispersible granules [88, 149]. To be successful, any formulation method should consider reducing nematode metabolism by immobilization or partial desiccation. Steinernema species can be stored in aqueous suspension for 6–12 months at 4–15°C, while Heterorhabditis species can be stored only for 3–6 months at the same temperature. Partially-desiccated infective juveniles in water dispersible granules have a shelf life of 5–6 months for S. carpocapsae at 25°C and 2 months for S. feltiae, and 1 month for S. riobrave [156] at the same temperature.
3.7. Quality control of entomopathogenic nematodes
Before EPNs are used in the laboratory or in the field after being stored or formulated, they are acclimated at room temperature of ca. 25°C for 2 h. Their quality is then checked again, and their concentrations to be used in experiments are adjusted by volumetric dilutions in distilled water using the formula as given in Ref. [157].
4. Control of termites using entomopathogenic nematodes and their symbiotic bacteria
Authors of Refs. [158, 159] first reported the presence of parasitic head inhabiting nematodes in the termites Reticulitermes lucifugus and C. formosanus. But only 40 years later, Tamashiro [160] first proposed the use of nematodes against termites. Control of the pest based on the use of EPNs became a promising technology for future termite control option. Since then, a plethora of laboratory and in some extent field research efforts resulting in subsequent publications on biological control of termites have been observed [83, 161–164].
4.1. Control under laboratory conditions
Several experiments showed the effectiveness of EPNs to control termites under laboratory conditions. In the laboratory, bioassays with termites and EPNs are usually carried out in containers such as Petri dishes lined with wet filter paper or sterile sand [39, 109], PCV tubes, or Eppendorf tubes [109]. In all cases, piece of filter paper [165], straw [106], and also corrugated wood blocks [39] are usually used in the containers to serve as food for termites [48]. Nematodes strains used for inoculations are usually selected from a number of strains based on their greater virulence to G. mellonella larvae [39]. Selected strains are then mass reared [144] to have sufficient inoculums. Each container receives given population densities of nematodes, most of the time in the form of water suspension with appropriate water volumes. In the case of low population densities, nematodes are transferred into the containers using micropipettes [165].
According to the objectives of the experiment, termite castle (reproductive adults, soldiers, or workers) or developmental stage (larvae, nymphs, and adults) is selected and transferred into containers following nematode introduction [36]. Host-finding ability and nematode virulence (ability of the nematodes to kill their host and to produce offspring inside them) are recorded. Nematode mortality is recorded daily or at given intervals of time following inoculation to evaluate lethal dose (LD10, LD50, or LD90) and lethal time (LT10, LT50, or LT90). Insects that are killed are dissected 48 h postinoculation in Ringer solution under stereo-microscope to confirm parasitism and to record population density of infecting nematodes inside each termite and developmental stage of the nematodes. Also, part of termites killed by the nematodes is transferred to White traps (i.e., emerging from hosts and accumulating in water) for days to evaluate nematode progeny production [39, 109]. Because termites are very fragile, some usually die naturally during the course of the experiments. In this case, insect mortality data are corrected using the following formula of Ref. [166]: Mc = [(Mo − Mc′)/(100−Mc′)] × 100, where Mc = corrected mortality, Mo = Mortality caused by the nematodes, Mc′ = Mortality observed in control treatments.
Wang et al. [35] showed that S. carpocapsae and H. bacteriophora were effective against workers of the subterranean termite R. flavipes under laboratory conditions. The same authors also reported that H. indica was more efficient than both S. carpocapsae and H. bacteriophora against R. flavipes. Razia et al. [39] studied in sand assay method the virulence of S. siamkayai, S. pakistanense, and H. indica applied at 100, 250, 300, 500, 700, and 900 IJs/ml suspension on workers of subterranean termites, R. flavipes and O. hornei (25 termites/Petri dish). The authors observed positive relationship between concentration and exposure time and mortality and variation between nematode and termite species for LD10, LT50, and LT90. El-Sebay et al. [36] conducted similar experiment using Egyptian isolates of Heterorhabditis baujardi and H. indica to control Psammotermes hypostoma and Anacanthotermes ochraceus under laboratory conditions. The authors observed LC50 and LC90 values of, respectively, 15.03 and 361.53 for P. hypostoma and H. baujardi and 20.26 and 398.59 for H. baujardi and A. ochraceus at day 3 after inoculation. For the experiment, highest rate of insect mortality was observed at day 3 after inoculation. Zadji et al. [38] tested in 2-ml Eppendorf tubes (each with 50 nematodes and 1 insect) the pathogenicity of 29 Benin isolates of H. sonorensis and one H. indica against workers of M. bellicosus. The results of the experiment showed that 73% of the nematode isolates killed more than 80% of the insects. In another study, Zadji et al. [106] evaluated the differential susceptibility of workers and soldiers of two termite species, M. bellicosus and T. occidentalis, to four Benin isolates of EPNs: one H. indica, two H. sonorensis, and one Steinernema sp. (5, 10, 25, 50, or 100 nematodes/well of tissue culture plates with one insect). A significant difference in termite mortality was recorded between termite castes but not between EPN isolates and termite species. Soldiers of both M. bellicosus and T. occidentalis were similarly susceptible but more susceptible than workers. The LD50 varied with termite species and nematode isolates from 12 IJs (T. occidentalis with Steinernema sp.) to 23 IJs (M. bellicosus with Steinernema sp.).
The reproduction potential of EPNs inside termites varies not only with nematode species but also with termite species and caste. Zadji et al. [109] observed up to 20,213 H. sonorensis IJs per worker of M. bellicosus 10 days postinoculation with an average of six nematodes penetrating each insect. Wang et al. [35] similarly, but in much lower population densities, observed an average number of IJs of 289 ± 50 and 642 ± 93 per worker, respectively, produced from R. flavipes and C. formosanus (based on 11 and 8 workers, respectively). The nematodes were seen through the cuticle of dead termites 4–5 days postinoculation, and they began to emerge at day 5 after infestation. The authors concluded that EPNs have the potential to continue their infestation to termites after an initial treatment. But in the same experiments, they observed consumption of some nematode-killed termites by healthy termites or by a saprophagous mite, Australhypopus sp. This mite is very common on the body of R. flavipes, especially on the head. Once the termite dies, the mite reproduces quickly in large numbers and feeds on the dead termite. The consumption of dead termites by healthy ones and also by Australhypopus sp. is a cause for the failure of nematode recycling in termites.
Some others experiments are designed to evaluate the potential of the nematodes’ symbiotic bacteria to kill termites or to evaluate the efficacy of combined effect of nematodes with other insect control methods on termites. H. bacteriophora and their associated bacteria were found to be effective against workers and nymphs of six different species of termites: C. formosanus, Gnathamitermes perplexus, Heterotermes aureus, P. hybostoma, R. flavipes, and R. virginicus. Meanwhile, H. indica and Photorhabdus luminescens complex were found to be effective against three species of termites: C. formosanus, C. vastator, and R. flavipes. S. carpocapsae together with their symbiotic bacteria, X. nematophila, are capable of suppressing population of eight different termite species including C. formosanus, C. vastator, G. perplexus, H. aureus, P. hybostoma, R. flavipes, R. virginicus, and Zootermopsis angusticollis.
Two-container choice device is used to evaluate the repellency of nematodes to termites [35] as described by Mauldin and Beal [167]. Wang et al. [35] used this method to study the repellency of four EPNs: S. carpocapsae, Steinernema riobrave, H. bacteriophora, and H. indica to two subterranean termites: R. flavipes and C. formosanus. H. indica repelled termites at high concentrations (90 nematodes/cm3 and above) in sand and vermiculite medium. The length of repellency varied (from 3 to 17 days postinoculation) with the nematode concentration and the size of the device used for the experiment. Similar experiment was conducted by Zadji et al. [106] with Benin nematode isolates: one H. indica, two H. sonorensis, and one Steinernema sp. (962.5 nematode IJs/cm3 of 40 cm3 sterilized sand) and termite species, M. bellicosus and T. occidentalis. The experiment did not show evidence that M. bellicosus and T. occidentalis would be able to detect the presence of IJs of any EPN isolates. However, it was observed that nematode dispersal occurred by infected termites or phoresis.
The results of these experiments showed that, usually, under laboratory conditions, pathogenicity of nematodes to termites is certain as the host contact is certain, environmental conditions are optimal and no ecological or behavioral barriers to infection exist [168]. But under field conditions, successful termite control using nematodes is less certain.
4.2. Control under field conditions
In the world in general and in Africa in particular, field studies on the use of EPNs to control termites are limited [31, 169]. The few studies compared the effects of various formulations and methods of applications of the nematodes on the mortality of different casts and life stages of termites evaluated the performance of different nematode isolates on the progress of termite nests’ reconstruction, the persistence of the nematodes in the nests, the percentage of nests for which the underground termite populations died, and the progeny production of the nematodes inside their host [31]. The ability of termites to detect the nematodes and to avoid them [48], and the overall behavior of termites following colonization of the nests by nematodes were also studied. The advantage of the use of EPNs over other methods, especially over chemical methods, for the control of termites under field conditions, is the capacity of nematodes to reach cryptic habitat of termites, difficultly reachable by chemical pesticides; termites live in an environment conducive to nematodes. A wide range of EPNs were identified in this regard as effective against various termite species [26, 31] under field conditions. But the nematode formulation used affects the success of the pest control.
Nematode water suspension (i.e., nematodes in water) or nematode-infected G. mellonella larvae are two nematode formulations mostly used in the fields to control termites [31, 46, 83]. In the case of nematode suspension, the nematode inoculum is applied using common nozzle type sprayers (hand and ground sprayers) with openings as small as 100 μm in diameter and with pressure of up to 1068 kPa on nematodes [170] in the field or using simple water cans on small areas against termites [171] successfully controlled Neotermes sp. associated with coconut palms and citrus trees. Meanwhile, Lenz et al. [172] injected Heterorhabditis indicus into cavity of mahogany tree against Neotermes sp. Also, Gouge [83] and Lenz [46] injected nematodes in tree trunks to control Mastotermes darwiniensis using Heterorhabditis sp. But the authors reported that the success of termite control is affected by the plant structure. For example, it is difficult to apply nematodes to the entire termite colony of branched trees, where termites find refuge in untreated branches of the plant.
For successful termite control, especially with nematode-infected G. mellonella larvae, the aboveground termite nests are first demolished before nematode suspension or infected G. mellonella larvae are applied. Baimey et al. [31] applied 52-week-old EPN-infected G. mellonella larvae per nest, each larva containing ca. 200,000 of IJs of Benin isolates of H. sonorensis and H. indica. At day 70 after inoculation, the underground populations of 71 and 60% treated nests were controlled by H. sonorensis and H. indica-infected G. mellonella larvae, respectively. When applied in infected G. mellonella larvae, nematodes will be protected for a while against environmental stresses before emerging from the larvae and will certainly provide superior termite control as compared to nematodes applied in water suspension which will be rapidly affected by environmental stresses soon after their application.
Termite workers are able to reconstruct their nest after this is broken. Baimey et al. [31] reported that nest reconstruction as measured by the nest reconstruction rate (see formula below) differed significantly among nematode isolates and time of exposure of inocula to termites with significant correlation between the two parameters. The nest reconstruction rate (NRR) is estimated as followed: NRR = (Vn/V0) × 100, where Vn is the aboveground reconstructed nest volume n days after application of EPN-infected G. mellonella larvae and V0 the volume of the aboveground nest before its demolition. The nest volume is calculated using the formula to calculate the volume of a cone, V = 1/3π × R2 × h, where R (m) is the nest radius and h (m) the nest height.
Even though termite nest can be reconstructed after being broken or after nematode application, nematode persistence in the nest area is necessary to avoid frequent breaks and also frequent applications of the nematodes for successful control of termites. Nematode persistence in the nest can be assessed by randomly taking soil samples from treated nest at intervals of days and by baiting the samples with last instars G. mellonella larvae. Baimey et al. [31] took nest samples 10, 20, and 70 days postinoculation. The samples were baited with G. mellonella larvae for a week at 25 ± 1°C and dead larvae recorded daily from the 5th day to the 7th day. Cadavers of G. mellonella larvae were dissected to confirm EPN infection. Susurluk et al. [173] stated that the number of infected larvae found by sampling is related to the number of nematodes that were present in the soil.
Authors of Refs. [48, 174] reported an ability of some termite species (example of Reticulitermes tibialis) to detect EPN and avoid them or to detect other termites that have died from nematode infection. Nematode-killed individuals are walled off to avoid or reduce contamination to other individuals in the nest [175, 176]. Authors of Refs. [169, 177] stated that though nematodes appear to have a limited impact on subterranean and dampwood termites due to termite behavioral defense mechanisms, they successfully control drywood termites where colonies are contained within a single piece of wood or a single tree. Similarly, Fujii [178] reported that this walling-off behavior of certain termite species does not prevent the dispersal of nematodes inside the occlusion as, at least, nematodes that were produced from partially or loosely buried termites are often observed outside the occlusion. Wang et al. [35] reported a repellence of EPNs to termites and concluded that the repellence might be the main reason for the ineffectiveness of nematodes to termites in certain field experiments. Therefore, it is important to consider the species of termites before selecting the EPN isolates.
5. Limitations in the use of entomopathogenic nematodes as biological control agents of termites
The various information given in this chapter indicated that EPNs provides some successful control of termite. But the method presents some limitations that should be taken into account. An example of limitation is the high nematode population densities needed for successful control of termites: approximately 23,000 infective juveniles of H. bacteriophora, S. carpocapsae, and S. feltiae nematodes are required to treat one square foot of termite infested area. Authors of Refs. [179, 180] stated that for successful control of drywood termites, all portions of the gallery system need to be located and treated. Nematodes were effective on the dampwood termite in the genus Neotermes infesting unbranched trunks of coconut palms, but their effectiveness was inferior in branched trees of citrus, cocoa, or mahogany [172]. The high numbers of termites in a nest, the wide foraging range of termites, the limited mobility of nematodes, the low reproduction rate of some nematode isolates in dead termites, and the repellence of some nematodes to termites are other examples of limitations for successful control of termites by nematodes, especially in field conditions. In this regard, Wang et al. [35] advised inundative release of EPNs rather than classical biological control for the control of subterranean termites. To increase termite susceptibility to EPNs, some researchers refer to sublethal doses of chemical termiticides, other biological control agents as fungi [181, 182] and bacteria [98] and imidacloprid [95, 183, 184] in an integrated pest management programs. However, this method encounters the problem of delivery of those insecticides to termite individuals at a distance from the application site [185]. Moreover, the method needs to provide cost effective protection against termite damage [35]. Temperatures of above 30°C in the center of the nests of Coptotermes species, where reproductives and brood are housed, are lethal for the nematodes. This means that different isolates or species of EPNs that are tolerant to higher temperatures are required for subterranean termite species. The diffuse nest system, the presence of multiple sets of reproductives, large territory size, and simultaneous use of many feeding sites also make the successful control of some termite species using EPNs difficult. Weeks and Baker [48] reported that the nematodes must be placed in environments congenial to their survival or they prove useless for control. More studies are then needed on these limitations for easier and better control of termites using EPNs.
Acknowledgments
The Flemish Inter-University Council-University Development Co-operation (VLIR-UOS), Belgium funded the first soil samplings for EPNs in Benin and also the first research activities on the control of citrus termites using Beninese isolates of nematodes through the “Ecological Sustainable Citrus Production in Benin” Project. VLIR-UOS is gratefully acknowledged by the authors of this paper.
\n',keywords:"termites, entomopathogenic nematodes, biological control, methodology, Africa",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/56369.pdf",chapterXML:"https://mts.intechopen.com/source/xml/56369.xml",downloadPdfUrl:"/chapter/pdf-download/56369",previewPdfUrl:"/chapter/pdf-preview/56369",totalDownloads:1726,totalViews:400,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,dateSubmitted:"November 16th 2016",dateReviewed:"May 23rd 2017",datePrePublished:null,datePublished:"August 16th 2017",dateFinished:null,readingETA:"0",abstract:"Termites are social insects reported from many countries of the world. Some species of them are known to be beneficial to man, whereas some others cause substantial losses (billions of US dollars annually) of properties and amenities. Various preventive and remedial methods are used to control undesirable termite species. The current review paper gives an overview of beneficial and detrimental activities of termites. Methods of control of undesirable species of termites are given and their advantages and disadvantages are discussed. We emphasized on the use of entomopathogenic nematodes (EPNs) as effective, environmentally safe and sustainable biological control method against termites. Species of EPNs recovered in Africa are documented. Some techniques used to collect termites and to maintain them for experiments and also to propagate, to formulate, to store, and to check for the quality of EPNs for application in the laboratory and in the field are also discussed. The environmental factors affecting the potential of EPNs to control termites are discussed. The information provided in this chapter will help researchers to enhance their skills of the use of EPNs against termites by selecting from the methodologies described here the best ones to adapt to particular experimental conditions, especially in African soil conditions.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/56369",risUrl:"/chapter/ris/56369",book:{slug:"nematology-concepts-diagnosis-and-control"},signatures:"Hugues Baïmey, Lionel Zadji, Léonard Afouda, André Fanou, Régina\nKotchofa and Wilfrieda Decraemer",authors:[{id:"201690",title:"Dr.",name:"Hugues",middleName:null,surname:"Kossi Baimey",fullName:"Hugues Kossi Baimey",slug:"hugues-kossi-baimey",email:"baimeyhugues@gmail.com",position:null,institution:{name:"Université de Parakou",institutionURL:null,country:{name:"Benin"}}}],sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Termites",level:"1"},{id:"sec_2_2",title:"2.1. Classification and distribution of termites",level:"2"},{id:"sec_3_2",title:"2.2. Beneficial activities of termites",level:"2"},{id:"sec_4_2",title:"2.3. Detrimental activities of termites",level:"2"},{id:"sec_5_2",title:"2.4. Termite collection and maintenance",level:"2"},{id:"sec_6_2",title:"2.5. Methods of control of termites",level:"2"},{id:"sec_8",title:"3. Entomopathogenic nematodes",level:"1"},{id:"sec_8_2",title:"3.1. Classification and distribution of entomopathogenic nematodes",level:"2"},{id:"sec_9_2",title:"3.2. Advantages of the use of entomopathogenic nematode",level:"2"},{id:"sec_10_2",title:"3.3. Characteristics of entomopathogenic nematodes",level:"2"},{id:"sec_11_2",title:"3.4. Environmental stresses and their effect on the performance of entomopathogenic nematodes and their symbiotic bacteria",level:"2"},{id:"sec_12_2",title:"3.5. Mass production of entomopathogenic nematodes for laboratory and field application",level:"2"},{id:"sec_12_3",title:"3.5.1. In vivo production",level:"3"},{id:"sec_13_3",title:"3.5.2. In vitro production",level:"3"},{id:"sec_15_2",title:"3.6. Storage and formulation of entomopathogenic nematodes",level:"2"},{id:"sec_16_2",title:"3.7. Quality control of entomopathogenic nematodes",level:"2"},{id:"sec_18",title:"4. Control of termites using entomopathogenic nematodes and their symbiotic bacteria",level:"1"},{id:"sec_18_2",title:"4.1. Control under laboratory conditions",level:"2"},{id:"sec_19_2",title:"4.2. Control under field conditions",level:"2"},{id:"sec_21",title:"5. Limitations in the use of entomopathogenic nematodes as biological control agents of termites",level:"1"},{id:"sec_22",title:"Acknowledgments",level:"1"}],chapterReferences:[{id:"B1",body:'Grimaldi D, Engel MS. Evolution of the Insects. Cambridge University Press; Cambridge, UK. 2005. p. 145. ISBN-13 978-0-521-82149-0 hardback, ISBN-10 0-521-82149-5 hardback'},{id:"B2",body:'Abe T, Bignell DE, Higashi M. 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Anhydrobiotic potential and long-term storage of entomopathogenic nematodes (Rhabditida: Steinernematidae). International Journal of Parasitology. 2000;30:995-1000. PMID: 10980289'},{id:"B157",body:'Navon A, Ascher KRS. Bioassays of Entomopathogenic Microbes and Nematodes. Wallingford, UK: CAB International; 2000. pp. 229-234. DOI: 10.1079/9780851994222.0000'},{id:"B158",body:'Merrill JH. Life-history and habits of two new nematodes parasitic on insects. Journal of Economic Entomology. 1916;9(1):148-149. DOI: 10.1093/jee/9.1.148'},{id:"B159",body:'Pemberton CE. Nematodes associated with termites in Hawaii, Borneo and Celebes. Proceedings of the Hawaiian Entomological Society; 1928. pp. 7:148-7:150. DOI: http://hdl.handle.net/10125/15760'},{id:"B160",body:'Tamashiro M. Susceptibility of Termites to Microbes. A Research Proposal submitted to the Office of Naval Research. Honolulu: Department of Entomology, University of Hawaii; 1968. p. 7'},{id:"B161",body:'Yu H, Gouge DH, Baker PB. Parasitism of subterranean termites (Isoptera: Rhinotermitidae) by entomopathogenic nematodes (Rhabditidae: Heterorhabditidae). Journal of Economic Entomology. 2006;99(4):1112-1119. PMID: 16937662'},{id:"B162",body:'Yu H, Gouge DH, Stock SP, Baker PB. Development of entomopathogenic nematodes (Rhabditida: Steinernematidae: Heterorhabditidae) in the desert subterranean termite Heterotermes aureus (Isoptera: Rhinotermitidae). Journal of Nematology. 2008;40(4):311-317. SN: 0022-300X'},{id:"B163",body:'Ibrahim SAM, El-Latif NA. A laboratory study to control subterranean termites. Psammotermes hybostoma (Desn.) (Isoptera: Rhinotermitidae) using entomopathogenic nematodes. Egyptian Journal of Biological Pest Control. 2008;18(1):99-103. ISSN: 1110-1768'},{id:"B164",body:'Shahina F, Tabassum KA, Salma J, Mahreen G. Biopesticidal affect of Photorhabdus luminescens against Galleria mellonella larvae and subterranean termite (Termitidae: Macrotermis). 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Status of the Tree Damaging Neotermes sp. in Fiji’s American Mahogany Plantation and Preliminary Evaluation of the Use of Entomopathogens for Their Control. Project Report, ACIAR Small Project No. FST/96/205; 2000. p. 111'},{id:"B173",body:'Susurluk A., Ehlers R-U. Field persistence of the entomopathogenic nematode Heterorhabditis bacteriophora in different crops. BioControl. 2008;53(4):627-641. DOI: 10.1007/s10526-007-9104-2'},{id:"B174",body:'Epsky ND, Capinera JL. Efficacy of the entomogenous nematode Steinernema feltiae against a subterranean termite, Reticulitermes tibialis (Isoptera: Rhinotermitidae). Journal of Economic Entomology. 1988;81(5):1313-1317. DOI: 10.1093/jee/81.5.1313'},{id:"B175",body:'Gaugler R, Wang Y, Campbell JF. Aggressive and evasive behaviors in Popillia japonica (Coleoptera: Scarabaeidae) larvae: Defenses against entomopathogenic nematode attack. Journal of Invertebrate Pathology. 1994;64(3):193-199. DOI: 10.1016/S0022-2011(94)90150-3'},{id:"B176",body:'Koppenhöfer AM, Grewal PS, Kaya HK. Synergism of imidacloprid and entomopathogenic nematodes against white grubs: The mechanism. Entomologia Experimentalis et Applicata. 2000;94(3):283-293. DOI: 10.1046/j.1570-7458.2000.00630.x'},{id:"B177",body:'Mankowski M, Kaya HK, Grace JK, Sipes BS. Differential susceptibility of subterranean termite castes to entomopathogenic nematodes. Biocontrol Science and Technology. 2005;15(4):367-377. DOI: 10.1080/09583150400016951'},{id:"B178",body:'Fujii JK. Effects of an entomogenous nematode Neoaplectana carpocapsae Weiser, on the Formosan subterranean termite, Coptotermes formosanus [Ph.D thesis]. University of Hawaii, Honolulu; 1975'},{id:"B179",body:'Woodrow RJ, Grace JK, Oshiro RJ. Comparison of localized injections of spinosad and selected insecticides for the control of Cryptotermes brevis (Isoptera: Kalotermitidae) in naturally infested structural mesocosms. 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Bayer 1996;49:103-145'},{id:"B184",body:'Ramakrishnan R, Suiter DR, Nakatsu CH, Humber RA. Imidacloprid-enhanced Reticulitermes flavipes (Isoptera: Rhinotermitidae) susceptibility to the entomopathogen Metarhizium anisopliae. Journal of Economic Entomology. 1999;92(5):1125-1132. DOI: 10.1093/jee/92.5.1125'},{id:"B185",body:'Su N-Y. Response of the Formosan subterranean termites (Isoptera: Rhinotermitidae) to baits or nonrepellent termiticides in extended foraging arenas. Journal of Economic Entomology. 2005;98:2143-2152. DOI: 10.1603/0022-0493-98.6.2143'}],footnotes:[],contributors:[{corresp:"yes",contributorFullName:"Hugues Baïmey",address:"baimeyhugues@gmail.com",affiliation:'
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1. Introduction
During the childhood years and into adolescence, the brain grows tremendously, causing a significant change in cognitive capacities. In later years of childhood and adolescence, many of the neurological changes correspond with advancements in perspective taking and reasoning; however, evidence from the early childhood years suggests that these changes more closely align with advancements in inhibitory control and executive functions more broadly [1, 2]. However, there are distinct developmental changes which inform our understanding of inhibitory control and which merit further discussion. Regardless, these developmental changes have profound impacts on children’s development overall, including academic and social outcomes. It is important to recognize, however, that children’s capacities to inhibit a prepotent response have been shown to vary by culture, as well as exposure to early adverse life events, and therefore a consideration of environment should be included when attempting to conduct research in this area or when making important policy or curriculum decisions. Nevertheless, research which utilizes inhibitory control (IC) training specifically within the early childhood ages demonstrates positive results, with more intensive training yielding more promising results.
2. Nature of inhibitory control during the early childhood years
Research has consistently demonstrated that the preschool years are a developmental time during which children experience profound growth in their ability to inhibit an unwanted response [3]. Younger preschool-age children are more likely to perseverate in their errors across multiple trials [4] by repeating a maladaptive behavior—for instance, a child who continues to shout out in class instead of raising their hand—whereas this pattern declines markedly by age 4. Similarly, 3-year-old children demonstrate an ability to inhibit an automatic prepotent response on a Simon Says task (e.g., Go/NoGo task [5]: children are trained to respond to one stimulus and are trained not to respond to a similar stimulus; see Table 1) for roughly one in four trials, in comparison to 4-year-old children who were successful on roughly 9 out of 10 trials [6]. Moreover, the impacts of inhibitory control on children’s cognitive capacities also seem to change as a function of age. For instance, younger preschool-age children’s inhibitory control capacities strongly predict their problem-solving strategy use and performance; however, older preschool-age children’s problem solving is better explained by their working memory capacities (see Table 1) rather than their inhibitory control abilities [7]. Relatedly, the development patterns of IC growth may not be limited to simply greater accuracy on relatively straightforward tasks. Older preschool-age children perform with greater success on more complicated tasks of IC than their younger peers [1], which may indicate that using multiple, progressive tasks when assessing IC may reveal important developmental patterns not captured by using a single task or by using multiple similar tasks. Overall, the findings on early childhood IC show robust and dramatic growth, particularly during the childhood years.
Key terms
Definitions
Executive functions (EF)
The constellation of foundation cognitive capacities, such as inhibitory control, working memory, and attention, which allow for later emergence of reasoning and problem solving
Inhibitory control (IC)
The cognitive capacity to inhibit a prepotent, automatic behavioral response
Working memory
A cognitive system for temporarily storing and managing information that is necessary for undertaking complex cognitive tasks
Theory of mind (ToM)
The understanding that others have mental states such as beliefs, desires, etc., which can vary from person to person or within one person over time
Go/NoGo task
Children are trained to respond to one stimulus (e.g., “Go” stimuli) and are trained not to respond to a similar stimulus (“NoGo” stimuli). This task measures behavioral inhibition
Day/Night Stroop task
Children are trained and must complete trials in which they say the word “night” when presented with an image of a sun on a white background and say “day” when presented with an image of a moon on a dark background. This task involves both behavioral inhibition and cognitive interference
Cognitive interference/interference control
It refers to attempts to suppress interference from competing stimuli. The response time of an IC task is usually considered as a measure of cognitive interference
Behavioral inhibition
It requires suppressing a behavioral response for a more optimal response. Cognitive interference and behavioral inhibition are two aspects of IC
Electroencephalogram (EEG)
A neurological testing that allows researchers to precisely measure brain activity during the behavioral tasks, which provides for a more complete examination and consideration of IC as a cognitive capacity
Inhibitory control training
A designed intervention that includes a training process which aimed at improving IC
Table 1.
A summary of definitions of the major concepts and techniques.
Although researchers agree on the tremendous growth of IC during this developmental age, there persists disagreement as to the specific nature of IC, and executive functions, during this time. Executive functions (EF) refer to the constellation of foundational cognitive capacities, such as inhibitory control, working memory, and attention [1], which allow for later emergence of reasoning and problem solving. In middle childhood and beyond, these executive function capacities can be considered as increasingly discrete processing mechanisms; however, during early childhood, these patterns remain more nebulous, and studies using confirmatory factor analysis have shown developmental differences in factor emergence and persistent factor unification into the childhood years. For instance, during the preschool years (broadly, ages 3 years to 6 years), studies using multiple assessments of inhibitory control, attention, and working memory yield a single unitary construct of executive function or inhibition generally [8, 9, 10, 11, 12], whereas studies of middle childhood have discerned multiple discrete factors, including working memory and attention shifting [13], and this trend continues and expands into later childhood and adolescence (see [14]).
The prevailing argument is that tasks of IC during the early childhood years necessitate activation of multiple other components of EF. take, for instance, the Day/Night Stroop task (see [15]; Table 1) in which a child is trained and must complete trials in which they say the word “night” when presented with an image of a sun on a white background and say “day” when presented with an image of a moon on a dark background. In this task, IC is typically measured by accuracy, with measurements of response time frequently included as well. This task clearly requires the child to inhibit the automatic response of verbalizing the association they have made between the sun and it being daytime, or between the moon being present during nighttime, and thus is inarguably a task of IC. However, some argue that this task measures additional facets of EF simply by the nature of the task. For instance, a child must have sustained attention throughout the assessment, and if the child loses focus for even a moment, the measurement of response time could be conflated, leading some scholars to argue that the attentional component of EF predicts IC [3, 16]. Similarly, the child must work to keep the rules of the moon/day and sun/night matching in the forefront of their mind during the assessment, and if they do not, then the accuracy measure could be conflated with working memory. Many researchers have argued, therefore, that the various EF components are highly integrated during the early childhood years and that these components emerge as more distinct with age and experience [1, 14].
As shown by the previous example, it is difficult for researchers to disentangle the various components of EF, from a measurement perspective, in early childhood. Researchers’ understanding and measurement of inhibitory control during the early childhood years should therefore be sensitive to the developmental nature of such phenomena and should perhaps consider using indices of a variety of executive function capacities. However, as described previously [14], a common conceptualization of EF in the early childhood literature seems to imply that EF and IC are analogous at this development time (e.g., [17]) or that IC developmentally precedes other domains of EF (e.g., [16]). Although IC contributes largely to early childhood EF, as demonstrated in the previous example, it may be problematic to consider these as synonymous. One argument in support of this claim is that children’s task performance on EF tasks most closely replicates issues of IC—that is, a child will persist in making prepotent errors, a classic demonstration of immature IC, while also activating other areas of EF, such as attention, working memory, etc. Although several arguments have been proposed to counter the position of equivocating EF with IC, most pertinent to the current chapter may be that IC itself may be multidimensional. Referring again to the aforementioned example, many researchers consider response time in the Day-Night Stroop task to be a measure of cognitive interference (sometimes referred to as interference control), which refers to attempts to suppress interference from competing stimuli, in contrast to behavioral inhibition which requires suppressing a behavioral response for a more optimal response [18, 19]. That is, the construct of inhibitory control as it pertains to developmental changes during the early childhood years requires both the cognitive power to limit attention to distractor stimuli and the behavioral power to engage an appropriate response.
Turning to developing an appreciation for the role of IC for holistic development, the capacity for IC has important implications in terms of development across a number of domains [20]. For instance, although IC has been shown to predict children’s academic achievement generally throughout the childhood years [21], strong IC consistently predicts more proficient mathematical knowledge [16, 22, 23, 24] and numerical strategy use [25]. Moreover, IC has been implicated in children’s emergent literacy proficiency [16, 24] and language development [26]. The development of IC during the early childhood years additionally has profound implications for children’s social and emotional development [27], such as the emergence and development of social perspective taking [28], problem solving and emotional control [27], and suppressing disruptive behaviors and aggression [11]. As such, IC should be considered by researchers and practitioners alike for the implications this capacity may hold across areas of maladaptive academic and social development.
Research methodologies employed for assessing IC during the early childhood years can vary considerably, and each assessment offers a wealth of strengths yet, as mentioned previously, may be incomplete on its own. Therefore, much of the research studies in this area use more than one type of assessment or multiple assessments with considerable methodological overlap. An important consideration in measurement of IC, indeed of any cognitive faculty, during the early childhood years is the developmental appropriateness of the task (see [8], for review). For instance, children in this age range are often concurrently experiencing emerging literacy skills and are often not yet proficient readers; therefore, it would be inappropriate to use a task which requires even low reading requirements, as such a task would likely require a cognitive load too great to allow for successful task completion. Moreover, such a task when used with an emerging reader would result in contaminated measurement in that task performance may indicate a lack of understanding the rules of the task, the lack of proficiency in reading, or inhibitory control. Similarly, tasks to be used on a study of early childhood should be rather straightforward, without overly complicated instructions or numerous steps. Therefore, much of the research studies in the area of inhibitory control that focus on early child development utilize tasks or games which require no reading, with simple instructions provided to the child verbally and repeated if necessary, and these tasks typically include a generous training time to ensure that the child understands and can perform the task.
Many of the commonly employed tasks resemble that of the Day/Night Stroop task [15, 29] and the Go/NoGo task [1, 5, 19, 30], both of which were described in the previous paragraphs. Importantly, these two tasks differ in terms of cognitive interference with regard to the expectations for children’s behavioral responses. Specifically, the Day/Night Stroop task involves embedded rule use, thus requires children to produce a verbal response to multiple stimuli, and therefore requires that the children process and act on multiple rules (i.e., if moon, then “day,” but if sun, then “night”), whereas the Go/NoGo task only requires a behavioral response to a single stimulus (e.g., if “Simon Says,” then response; if not, then no response). This distinction has led some to argue that the Day/Night Stroop task may be more complex particularly for younger children than other tasks, and therefore performance on this and similar tasks may be indicative of greater IC capacities compared with Go/NoGo tasks (see, e.g., [31, 32]).
Consistent with the recommendation noted previously regarding the need to use multiple indices of IC when attempting to correctly assess children’s capacities, many researchers employ the use of neurological testing, such as an electroencephalogram (EEG), in concert with a behavioral task, such as the Go/NoGo task (e.g., [30]). Using neurological measurement, such as EEG, allows researchers to precisely measure brain activity during the behavioral tasks, which provides for a more complete examination and consideration of IC as a cognitive capacity particularly from a developmental perspective. That is, as the brain is experiencing tremendous growth during the early childhood years, it is important to capture how such physical growth corresponds with cognitive growth, and this is perhaps best done by measuring neural activity during a cognitive task.
Overall, EF generally, and inhibitory control specifically, undergoes dramatic growth during the preschool years, which has important implications for their development overall [1, 2]. Although EF is discernable as more discrete constructs in later ages of development, this has not been consistently demonstrated during the early childhood years [8, 9, 10, 11, 12], and thus researchers should consider possibly utilizing multiple tasks, including neurological assessments if possible [30], to provide a more comprehensive understanding of IC during the early childhood years.
2.1 Impacts of culture and environment on young children’s inhibitory control development
Consistent with other cross-cultural research which shows variation in the timing and emergence of children’s cognitive capacities (e.g., [33]), evidence of IC development from non-Western societies is not entirely consistent with that of Western societies, suggesting that children’s inhibitory control may be impacted by cultural and environmental factors [34]. For instance, a variety of studies comparing Chinese samples to Western samples may suggest that preschool-age children reared in Chinese cultures outperform their US counterparts on tasks of IC [34, 35], which has also been found in other non-Western cultures (e.g., Japan [36]). Importantly, comparing samples of non-Western cultures from African and Latin American communities [37] as well as cultures which share both Western and Eastern ideals (i.e., Turkey [38]) to Western has not yielded differences by culture. Overall, the cross-cultural research on IC development in early childhood may indicate that although there is a large universality in terms of IC development, cultural and societal mores may cause differences in children’s IC and development more broadly.
Moreover, in terms of implications of the cross-cultural research for child development more broadly, in Western cultures IC has been consistently shown to predict theory of mind (i.e., the understanding that others have mental states such as beliefs, desires, etc., which can vary from person to person or within one person over time [39]) particularly during the early childhood years [31], which holds implications for children’s social competence during early childhood and beyond; however, this predictive relation between IC and theory of mind has not consistently been demonstrated in cross-cultural samples to the same degree as in Western samples [40]. For example, a recent meta-analysis discussed that although IC and EF generally did predict theory of mind and mental state understanding across cultures, the strength of this prediction was weaker among studies assessing East Asian samples than several Western samples, including the USA, Canada, and Europe [31].
Other environmental factors, such as exposure to poverty or low socioeconomic opportunity, have also been shown to impact children’s cognitive development, including the development of EF during the early childhood years, with children from low-income families generally underperforming their more affluent peers [41, 42]; however, the recent work has turned to focus on the adaptive strengths of children raised in environments with higher rates of adversity [43]. For example, although children from low-income families have demonstrated less accuracy on a Go/NoGo task, they did not perform more slowly on the task [44]. Moreover, children from low-income families performed less accurately on a simple working memory task than with peers, but these group differences were eliminated when the task was made to be more complex [44]. A similar finding has been shown for children who have experienced familial trauma, and this may be true even when considering the impacts of poverty exposure. Children who have been reported as experiencing family trauma, as assessed by indices of post-traumatic stress disorder (PTSD), showed poorer global EF than non-traumatized children [45]; however, the effect size was weaker for IC task performance than other types of EF, such as working memory and processing speed. This may suggest that children who experience familial trauma may develop adaptive responses to their environments which allow them to inhibit prepotent responses as indicated by the IC task performance.
Similar to the pattern of IC mediating the impact of culture on early childhood competence, it may be that environmental exposure to poverty and adversity may additionally impact other areas of children’s development. Academic achievement and behavioral regulatory faculties are more strongly predicted by IC task performance for children from more affluent family backgrounds, for example, than their less affluent peers [46]. Additionally, among children attending a federally funded educational program for low-income families and their children, children with stronger IC performance were rated by their teachers as having better socio-emotional faculties and showed fewer internalizing behaviors (e.g., indications of anxiety and depression) than their low-income peers who performed less well on IC tasks [47, 48]. Children who experience other types of environmental adversity, such as children who experience violence or maltreatment at home, show similar patterns of poorer academic achievement and school adjustment, yet this relation is additionally explained by children’s IC [49]. In sum, although children who experience adverse early life events, or are raised in low-income families and neighborhoods, have shown to differ from more traditional samples in terms of academic achievement and socio-emotional competencies, these discrepancies may be explained by young children’s emerging IC faculties. Therefore, these children may show marked improvements in EF capacities, as well as other positive outcomes such as improved academic achievement, with IC training.
2.2 Inhibitory control training in early childhood and implications for development
Efforts in establishing inhibitory control as an effective tool for cognitive improvements have proven successful across the life span [50]. Moreover, as the early childhood years are an important time for the development of EF generally, and IC specifically, as previously discussed, this developmental age range is ideal for examining the possible power of IC training. Several studies have examined the impacts of IC training on child outcomes, and these studies consistently yield positive findings [19, 21, 50, 51, 52, 53, 54, 55, 56].
Importantly, the outcomes of IC training have been shown to vary considerably based on the types of training. Studies have shown, for example, the training of more global EF capacities rather than IC specifically (e.g., [53, 55]) may be successful in expanding cognitive performance across a wide range of tasks. This aligns with the aforementioned discussion of the entanglement of multiple components of EF during early childhood (i.e., that many factor analytic studies have shown that in the early childhood years the distinct components of EF, such as working memory and IC, may not be as separately discernable as evidenced during the later years of development [8, 9, 10, 11, 12]). To test this, some researchers have attempted to gauge the effectiveness of IC training compared with training in other areas of EF, such as working memory; for instance, children who received 5 weeks of computerized IC training, compared with a group who received a parallel program of working memory training, showed improvements in task performance for the task on which they received training; however these improvements did not transfer to other tasks of EF [55]. Limited transfer effects have been reported elsewhere as well, such as children showing increased performance on methodologically and structurally similar tasks as to the training task, but not other tasks [51], although this increase in performance was sustained over many months. However, other research has shown considerable transfer effects, such as children showing enhanced reasoning abilities after training on a Go/NoGo task [19] and children, adolescents, and adults showing enhanced perspective-taking capacities after receiving IC training [50].
Other types of training have also shown to be successful in improving EF performance. Having children engage in reflective metacognition regarding their performance on difficult cognitive tasks, such as their performance in the Day/Night Stroop task, has shown to be effective in enhancing their performance on that task even compared with more traditional training procedures, such as practice and corrective feedback [54]. Additionally, training on language skills can have a positive impact on children’s IC, as such trainings require engaging in multiple components of EF (e.g., sustained attention), as well as IC specifically [57] such as by requiring the child to use the correct term for a specific item within a larger category of items. This aligns with the espoused conceptualization of early childhood IC as profoundly entangled within EF and is consistent with other research on EF trainings more broadly. For instance, children who received 12 sessions over 4 weeks of training that included working memory, IC, and cognitive flexibility showed significant improvements across a range of EF capacities, and these effects transferred to other areas of children’s cognition as well [58].
Additionally, outcomes of IC training may yield important changes at the level of neuronal and brain activity [54], which may not necessarily correspond with immediate changes in behavior. For instance, studies have shown that children who received an 8-week program of training which targeted children’s IC, working memory, and planning ability found that, for children who received the training, neural activity levels changed in the corresponding brain regions as expected; however children’s task performance after the training did not differ significantly from their pre-training performance [30]. Other studies have found that a single training session of metacognitive reflection about controlling impulsive behaviors may lead to decreased activation of the brain region responsible for processing conflicting information, which may indicate a lessened likelihood to process the information as conflicting, and therefore possibly indicating better adaptation in integrating new rule schemes [54].
Moreover, the positive impacts of receiving EF training have been found effective for children from low-income families as well. For instance, one study showed that when classrooms serving low-income families implemented a full year of an EF training that included a broad range of EF skills deeply integrated into the classroom curriculum, compared with classrooms that had no such program, children who received the training outperformed children in the control group on both simple and advanced tasks [52]. Indeed, children in the control group showed a decline in task performance for the more advanced tasks, which was not found for children who received the training. What’s more, the program was so successful that the control condition was not allowed to repeat, by request of the school, as the teachers and parents noted such profound change in terms of academics and student behavior that the school refused to continue the project without full implementation of the program in all classrooms. In concert with findings from more traditional samples which included less intensive training, these outcomes would indicate that children from low-income families might be an especially important area for future research, given the overwhelming strength of the results.
Although studies using IC training with children of incarcerated parents, or children who have experienced abuse or neglect, were not revealed during the current literature search, the previously discussed research of IC training during early childhood could be extended to these populations [45]. For instance, research on treatment approaches for anxiety and depression (common outcomes of trauma) with adults has shown that training individuals to develop better self-regulatory executive processes, such as attention, have shown promising results (see [45] for discussion). Given that children’s EF faculties are more nebulous and entangled than adults, it stands to reason that such approaches would yield additionally promising results during the early childhood years.
Moreover, such intervention approaches might be promising for researchers working in clinical settings. For instance, mindfulness training approaches that capitalize on EF processes, such as attentional focus, for children with anxiety have proven effective in reducing anxiety symptomology [59]. Such training has proven effective for children from low-income families as well [60], with positive effects extending beyond advanced EF development to include positive socio-emotional and behavioral changes as well. However, much of the research in this area has been conducted with older children, and examinations of the promise of mindfulness training during the early childhood years may not yet exist. This may be an important area for future research, as the implications for positive outcomes may be more robust with earlier intervention.
Overall, findings with regard to improving child outcomes during the early childhood years as they relate to IC training suggest that IC training may be effective to varying degrees. Although a few studies showed limited transfer effects, the most promising findings come from studies which implemented a broader EF training program rather than those which utilized specific IC training. Additionally, research studies with longer training programs, such as the 1-year program discussed above, yield stronger effects in terms of global child outcomes than did shorter programs. Studies involving brain imaging have also shown positive outcomes in terms of changes in brain activity, indicating that such training may be important for effecting long-term change.
3. Conclusions
The cognitive capacity to inhibit a prepotent, automatic response grows tremendously during the early childhood years corresponding with and as a function of profound brain development taking place at this time [1, 2]. At later ages, this cognitive ability is rather distinct from other foundational cognitive capacities, such as attention and working memory; however, considerable research suggests that during early childhood these distinctions are less clear, leading many researchers to consider and research EF as a more global function at this age [8, 9, 10, 11, 12, 13, 14].
Research which focuses on IC during the early childhood years typically utilizes simple, game-like tasks which require brief or no verbal response, and researchers typically utilize a variety of tasks which may assess various areas of EF, including the Day/Night Stroop task [15, 29] and the Go/NoGo task [1, 5, 19, 30]. Importantly, and with regard for the important growth occurring at this age in specific brain regions, many researchers use these tasks in combination with brain imaging [30], providing important insights into developmental changes taking place in brain and neuronal activity.
Importantly, the current chapter includes much literature on EF broadly rather than focusing specifically on IC and IC training. Although this is consistent with the current conceptualization of IC during this developmental time within the literature, this may have resulted in certain findings and trainings being included in the current discussion with which some researchers may disagree. Additionally, the current chapter focuses narrowly on a specific developmental window and thus is not representative of the research on IC across childhood.
For transparency, the literature review for the current chapter used the following databases: Google Scholar, ScienceDirect, and Web of Science. The keywords were executive function, inhibitory control (training), working memory, sustained attention, cognitive development, self-regulation, preschoolers, early childhood, children, cross-cultural, and risk population. Specifically, inhibitory control is a broad term in the research procedure, which has been expanded and is not limited to the executive function and cognitive development [61]. For ease of understanding, an at-risk population was defined as any potential risk factors (i.e., poverty or low income, neighborhood violence, family violence, family maltreatment, low social status, low education background, rural area). However, and as is the case with many reviews, the current chapter does not include findings from unpublished works, and thus the positive support for IC training as discussed here may be an artifact of publication bias.
Nevertheless, in creating IC training programs, much of the research has shown positive outcomes across a variety of training programs; however, as is to be expected, more promising and profound results accompany programs with more intensive training with longer durations [50, 51, 52, 53, 54, 55, 56, 57, 58]. Such training programs have proven effective across cultures and changes in the environment [52], including children from low-income backgrounds and children who have experienced profound early adverse life events. Although little research to date has examined IC training during early childhood in clinical samples, extending from the work discussed in this chapter, it would follow that IC training broadly, and perhaps mindfulness training specifically, may yield positive outcomes across domains.
Conflict of interest
The authors declare there is no conflict of interest.
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Introduction",level:"1"},{id:"sec_2",title:"2. Nature of inhibitory control during the early childhood years",level:"1"},{id:"sec_2_2",title:"2.1 Impacts of culture and environment on young children’s inhibitory control development",level:"2"},{id:"sec_3_2",title:"2.2 Inhibitory control training in early childhood and implications for development",level:"2"},{id:"sec_5",title:"3. Conclusions",level:"1"},{id:"sec_9",title:"Conflict of interest",level:"1"}],chapterReferences:[{id:"B1",body:'Anderson PJ, Reidy N. Assessing executive function in preschoolers. Neuropsychology Review. 2012;22(4):345-360'},{id:"B2",body:'Munakata Y, Herd SA, Chatham CH, Depue BE, Banich MT, O’Reilly RC. A unified framework for inhibitory control. Trends in Cognitive Sciences. 2011;15(10):453-459'},{id:"B3",body:'Reck SG, Hund AM. Sustained attention and age predict inhibitory control during early childhood. Journal of Experimental Child Psychology. 2011;108(3):504-512'},{id:"B4",body:'Diamond A, Taylor C. 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