See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/277017477

A Review of Biopesticides and Their Mode of Action Against Pests

Book · February 2015 DOI: 10.1007/978-81-322-2056-5_3

CITATIONS READS 64 31,937

1 author:

Senthil-Nathan, Sengottayan Manonmaniam Sundaranar University

132 PUBLICATIONS 3,314 CITATIONS

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Induced defenses in rice (Oryza sativa) by exogenous chemical elicitor against specialized pest and disease of the rice View project

DBT sponsored project during 2011-14 at AC&RI, Madurai View project

All content following this page was uploaded by Senthil-Nathan, Sengottayan on 22 May 2015.

The user has requested enhancement of the downloaded file. A Review of Biopesticides and Their Mode of Action Against Insect Pests

Sengottayan Senthil-Nathan

Abstract Biopesticides, including entomopathogenic viruses, bacteria, fungi, nema- todes, and plant secondary metabolites, are gaining increasing importance as they are alternatives to chemical pesticides and are a major component of many pest control programs. The virulence of various biopesticides such as nuclear polyhedrosis virus (NPV), bacteria, and plant product were tested under laboratory conditions very successfully and the selected ones were also evaluated under fi eld conditions with major success. Biopesticide products (including benefi cial ) are now available commercially for the control of pest and diseases. The overall aim of biopesticide research is to make these biopesticide products available at farm level at an affordable price, and this would become a possible tool in the integrated pest management strategy. Moreover, biopesticide research is still going on and further research is needed in many aspects including bioformulation and areas such as commercialization. There has been a substantial renewal of commercial interest in biopesticides as demon- strated by the considerable number of agreements between pesticide com- panies and bioproduct companies which allow the development of effective biopesticides in the market. This paper has reviewed the important and basic defection of major biopesticides in the past. The future prospects for the development of new biopesticides are also discussed.

1 Introduction

1.1 Biopesticides S. Senthil-Nathan (*) Division of Biopesticides and Environmental Toxicology, Sri Paramakalyani Centre for Excellence Biopesticides are developed from naturally occur- in Environmental Sciences, Manonmaniam ring living organisms such as , plants, and Sundaranar University , 627 412 Alwarkurichi, microorganisms (e.g., bacteria, fungi, and viruses) Tirunelveli , Tamil Nadu , India e-mail: [email protected]; that can control serious plant-damaging insect [email protected] pests by their nontoxic eco-friendly mode of

P. Thangavel and G. Sridevi (eds.), Environmental Sustainability, 49 DOI 10.1007/978-81-322-2056-5_3, © Springer India 2015 50 S. Senthil-Nathan actions, therefore reaching importance all over the lems seen with chemical pesticides. Biopesticides world. Biopesticides and their by-products are are frequently target specifi c, are benign to mainly utilized for the management of pests inju- benefi cial insects, and do not cause air and water rious to plants (Mazid et al. 2011 ). quality problems in the environment, and also Biopesticides are classifi ed into three different agricultural crops can be reentered soon after categories: (1) plant-incorporated protectants, (2) treatment. Microorganisms from nature can also microbial pesticides, and (3) biochemical pesti- be used in organic production, and risks to human cides. They do not have any residue problem, health are low. In addition, the usage of biopesti- which is a matter of substantial concern for con- cides has other several advantages; e.g., many sumers, specifi cally for edible fruits and vegeta- target pests are not resistant to their effects bles. When they are used as a constituent of (Goettel et al. 2001 ; EPA 2006 ). insect pest management, the effi cacy of biopesti- Biopesticides derived from bacteria like cides can be equal to that of conventional pesti- Bacillus thuringiensis (Bt), a large array of fungi, cides, particularly for crops like fruits, vegetables, viruses, protozoa, and some benefi cial nematodes nuts, and fl owers. By combining synthetic pesti- have been formulated for greenhouse, turf, fi eld cide performance and environmental safety, crop, orchard, and garden use (Hom 1996 ; Butt biopesticides execute effi caciously with the trac- et al. 2001a , b; Grewal et al. 2005; EPA 2006 ). tability of minimum application limitations and Biocontrol microbials, their insecticidal meta- with superior resistance management potential bolic products, and other pesticides based on (Kumar 2012 ; Senthil-Nathan 2013 ). living organisms are sorted as biopesticides by Copping and Menn ( 2000 ) reported that the EPA. There are hundreds of registered products biopesticides have been gaining attention and enlisted in EPA (2013 ). interest among those concerned with developing environmentally friendly and safe integrated crop management (ICM)-compatible approaches and 2 Microbial Pesticides tactics for pest management. In particular, farm- ers’ adoption of biopesticides may follow the 2.1 Bacteria recent trend of “organically produced food” and the more effective introduction of “biologically 2.1.1 Bacillus thuringiensis based products” with a wide spectrum of biologi- Beginning in the 1980s and continuing to the cal activities against key target organisms, as well present, a different molecular approach has been as the developing recognition that these agents employed to develop market acceptance of can be utilized to replace synthetic chemical pes- biopesticides. Earlier, several efforts were ticides (Menn and Hall 1999 ; Copping and Menn aimed at establishing microbial insecticides, 2000 ; Chandrasekaran et al. 2012 ; Senthil- like Bt, which has been used commercially over Nathan 2013 ). 40 years (Gelernter and Schwab 1993 ). Later, Insecticides from microorganisms extend a some Bacillus species such as Bacillus thuringi- unique chance to developing countries to ensis israelensis Bti and Bacillus sphaericus research, and they have possessed to develop 2362 (Bs ) were found particularly effective natural biopesticide resources in protecting crops. against mosquito (Revathi et al. 2013 ) and other The utilization of biopesticide programs would dipteran larvae. Bti was fi rst discovered to have be required to prevent the development of resis- increased toxicity against mosquito larvae in tance in target insect pests to synthetic chemical 1975 (Goldberg and Margalit 1977 ). pesticides and toxins from biopesticides (Copping Various bacterial species and subspecies, and Menn 2000 ; Senthil-Nathan 2006 ; Senthil- especially Bacillus , Pseudomonas , etc., have Nathan et al. 2006 , 2009 ). been established as biopesticides and are primar- Compared with chemical pesticides, biopesti- ily used to control insect and plant diseases. Most cides do not present the same regulatory prob- salient among these are insecticides based on A Review of Biopesticides and Their Mode of Action Against Insect Pests 51

Fig. 1 Mode of action of Bt toxin against lepidopteran insects

several subspecies of Bacillus thuringiensis Toxicity of Bti and some other toxic strains is Berliner. These include B. thuringiensis ssp. commonly imputed to the parasporal inclusion kurstaki and aizawai, with the highest activity bodies (δ-endotoxins) which are produced during against lepidopteran larval species; B. thuringi- sporulation time. These endotoxins must be ensis israelensis, with activity against mosquito assimilated by the larvae to accomplish toxicity. larvae, black fl y (simuliid), and fungus gnats; B. Bt and their subspecies produce different insecti- thuringiensis tenebrionis , with activity against cidal crystal proteins (δ-endotoxins), and their coleopteran adults and larvae, most notably the toxicity was determined (Chilcott et al. 1983 ; Colorado potato beetle (Leptinotarsa decemlin- Aronson and Shai 2001 ). These toxins, when eata ); and B. thuringiensis japonensis strain ingested by the larvae, can damage the gut tis- Buibui, with activity against soil-inhabiting sues, leading to gut paralysis. After that, the beetles (Carlton 1993 ; Copping and Menn 2000 ). infected larvae stop feeding and fi nally they die Bt produces crystalline proteins and kills few from the combined effects of starvation and mid- target insect pest species like lepidopteran species. gut epithelium impairment (Fig. 1 ) (Betz et al. The binding of the Bt crystalline proteins to insect 2000 ; Zhu et al. 2000 ; Darboux et al. 2001 ). gut receptor determines the target insect pest Some other microbial pesticides act by out- (Kumar 2012 ). competing insect pest organisms. Microbial 52 S. Senthil-Nathan pesticides need to be continuously supervised to was termed M. anisopliae by Sorokin in 1883 ensure that they do not become capable of injur- (Tulloch 1976 ). ing nontarget organisms, including humans Several entomopathogenic fungi and their (Mazid et al. 2011). In previous studies, the derivatives are also used as microbial pesticides. M. microbial pesticide advance has resulted in a sig- anisopliae are hyphomycete entomopathogenic nifi cant decrease of synthetic chemical insecti- fungi most widely used for insect pest control and cide usage (James 2009 ). are ubiquitous worldwide. This species comprises Gray et al. (2006 ) reported Bt toxins produced a huge number of different strains and isolates of by plant growth-promoting rhizobacteria, which various geographical origins and from different also develop bacteriocin compounds of insecti- types of hosts (Roberts and St. Leger 2004 ). cidal attributes. Bt is marketed worldwide for the Under natural conditions, Metarhizium are control of different important plant pests, mainly found in the soil, where the moist conditions per- caterpillars, mosquito larvae, and black fl ies. mit fi lamentous growth and production of infec- Commercial Bt -based products include powders tious spores, called conidia, which infect containing a combination of dried spores and soil-dwelling insects upon contact (Fig. 2 ). M. crystal toxins. They are applied on leaves or other anisopliae has the potential to be used as a bio- environments where the insect larvae feed. Toxin control agent, particularly for malaria vector spe- genes from Bt have been genetically engineered cies, and is also a suitable candidate for further into several crops. research and development (Mnyone et al. 2010 ). Driver et al. (2000 ) reevaluated the of the Metarhizium using sequence data from 3 Fungi ITS and 28S rDNA D3 regions and also using RAPD patterns, revealing ten distinguishable 3.1 Metarhizium anisopliae clades. M. anisopliae var. anisopliae represents clade 9. These entomopathogenic fungi have been M. anisopliae Sorokin var. anisopliae is an viewed as safe and regarded as an environmentally essential entomopathogenic fungus. It propa- satisfactory alternative to synthetic chemical pesti- gates worldwide in the soil, demonstrating a cides (Domsch et al. 1980 ; Zimmermann 1993 ). wide range of insect host species. This subspe- Recently, these entomopathogenic fungi have been cies was fi rst described in 1879 by Metschnikoff, registered as microbial agents and are also under under the term Entomophthora anisopliae, as a commercial development for the biological control pathogen of the wheat cockchafer, and later it of several pests (Butt et al. 2001a , b ).

Fig. 2 Mode of action of entomopathogenic fungi against lepidopteran insects A Review of Biopesticides and Their Mode of Action Against Insect Pests 53

M. anisopliae strains are obtained from different (Moscardi 1999 ). Even so, the application of geographical localities (Fegan et al. 1993 ), as sug- baculoviruses is still limited in the fi eld of agricul- gested, among others, by extremely variable toxici- ture and horticulture where the thresholds for pest ties (Goettel and Jaronski 1997 ). M. anisopliae have damage tend to be minimized. In , i.e., been used on a large scale in countries like Brazil, the primary group where baculoviruses have been where 100,000 ha of sugarcanes are treated every isolated, they only cause mortality in the larval year (Faria and Magalhães 2001 ). They are released stage (Cory 2000 ). in the fi eld after thorough assessment of strains. Baculoviruses need to be ingested by the lar- Consorting to Goettel et al. ( 2001) have reported vae to initiate infection. After ingestion, they that the growth and application of fungi as micro- enter the insect’s body through the midgut and bial agents for biocontrol of insect pest involve tests from there they spread throughout the body, with mammalian models to evaluate possible although in some insects, infection can be limited human and health risks. to the insect midgut or the fat body (Fig. 3 ). Two groups of baculoviruses exist: the nucleopoly- hedroviruses (NPVs) and granuloviruses (GVs). 4 Virus In NPVs, occlusion bodies comprise numerous virus particles, but in GVs, occlusion bodies 4.1 Baculovirus ordinarily contain just one virus particle. A common feature of baculoviruses is that they are Baculoviruses are double-stranded DNA viruses occluded, i.e., the virus particles are embedded present in , mainly insects. Baculoviruses in a protein matrix. The presence of occlusion are usually highly pathogenic and have been used bodies plays an essential role in baculovirus effi caciously in their natural form as biocontrol biology as it allows the virus to survive outside agents against numerous serious insect pests the host (Cory 2000 ).

Fig. 3 Mode of action of baculoviruses against lepidopteran insects 54 S. Senthil-Nathan

Recently, it has been substantially demonstrated lepidopteran pests, like the cotton bollworm and that baculoviruses are not infectious to vertebrates budworm, caterpillars that are mainly dangerous and plants. Also within the insects, their host range insect pests of corn, soybean, and other vegeta- is restricted to the order from which they were iso- bles (Arthurs et al. 2005 ). Furthermore, Certis lated. Genetic engineering of baculoviruses has so has registered a celery looper (Syngrapha fal- far been restricted to isolates from Lepidoptera cifera) NPV and an alfalfa looper (Autographa (Kolodny-Hirsch et al. 1997 ). Baculoviruses vary californica ) NPV (EPA 2006 ). in the number of hosts that they can infect; some seem to be particular to one species and hence are very unlikely to be a hazard when genetically mod- 5 Nematodes ifi ed, whereas others infect a range of hosts (Barber et al. 1993 ; Richards et al. 1999 ; Cory et al. 2000 ). 5.1 Steinernema (Rhabditida) The majority of new baculovirus recombi- nants now employ insect-selective toxins. One of the new hot products in biopesticide is Genetic modifi cation has been mostly carried nematodes. Pest nematodes can be supervised out on the alfalfa looper, Autographa califor- with cover crops, crop rotation, and internaliza- nica NPV (AcNPV)-the virus for which most tion of organic material into the soil (McSorely molecular information is available, including 1999). In the early 1990s, various effective ento- the complete DNA sequence, which permits mopathogenic nematodes from two genera, precise insertion of foreign genes. Recently, the namely, Steinernema and Heterorhabditis development of genetically modifi ed baculovi- (Nematoda: Rhabditida), were discovered and ruses has expanded to other strains of commer- established as a biocontrol agent against insects cial or regional interest (Popham et al. 1997 ; (Copping and Menn 2000 ). Cory 2000 ). Insect-parasitic nematodes may encroach Baculovirus-infected insect larvae have pri- upon soil-dwelling stages of insects and kill them marily initiated a cascade of molecular and cel- within 48 h through the expulsion of pathogenic lular appendages fi nally the larva enters into the bacteria. After the host dies, the infectious stages death and the development of huge amounts of of the nematodes become adults and a modern polyhedral occlusion bodies comprising rod- generation of infective juveniles (IJs) develops shaped virions (Miller 1997 ). Lately, a naturally (Fig. 4 ). Entomopathogenic nematodes are com- occurring baculovirus (Agrotis ipsilon multiple monly available for plant protection from serious nucleopolyhedrovirus, family Baculoviridae, insect pests and diseases, and also there have AgipMNPV) was indicated to have hope as a been various efforts to biocontrol insect pest pop- microbial insecticide for controlling A. ipsilon in ulations in the fi eld by employing IJs via spray- turf (Prater et al. 2006 ). ing. Nevertheless, little is known about the ability Numerous viral formulations are available pri- of indigenous nematodes to infl uence insect pest marily for the control of caterpillar pests. For populations (Peters 1996 ). instance, Certis has recently registered Madex™, In nematodes, the parasitic cycle is initiated an increased-potency codling granulosis by the third-stage IJs. These nonfeeding juveniles virus (GV) that also affects oriental fruit moth infest suitable insect host and enter through the (OFM). Certis also deals Cyd-X™, which also insect’s natural body openings like the anus, contains the codling moth GV and which can be mouth, and spiracles (Grewal et al. 1997 ). Once an effi cient tool for codling moth management they have entered inside the host, nematodes ( Arthurs and Lacey 2004 ; Arthurs et al. 2005 ). infest the hemocoel and then release their symbi- Aside from Madex and Cyd-X, Certis markets otic bacteria into the intestine. After that, the bac- Gemstar™, which contains Heliothis zea NPV, teria cause septicemia, killing the host within and Spod-X™, which contains beet armyworm 24–48 h (Fig. 4 ). The uptake of IJs is rapidly NPV. Gemstar is also registered for the control of manipulating by the bacteria and decomposed the A Review of Biopesticides and Their Mode of Action Against Insect Pests 55

Host finding Release of bacteria

Infection

Infective juvenile Host Killed

Development

Infective Juvenile Emergence Heterorhabditidae Adult stage

[Inside Egg] Steinernematidae Adult stage Reproduction

Fig. 4 Mode of action of entomopathogenic nematodes against lepidopteran insects

host tissues. Almost two to three generations of 6 Protozoa the nematodes are fi nished within the host cadaver (Pomar and Leutenegger 1968 ; Bird and 6.1 Nosema Akhurst 1983 ). In previous research studies, it has been In previous studies, protozoan diseases of clearly indicated that entomopathogenic nema- insects are ubiquitous in nature and constitute todes can be effective biocontrol agents against an essential regulatory role in insect populations some of the major insect pest families found in (Maddox 1987 ; Brooks 1988 ). Microsporidia, stored goods like Pyralidae (Shannag and such as Nosema spp., are generally host specifi c Capinera 2000) and Curculionidae (Duncan and and slow acting, most frequently producing McCoy 1996 ; Shapiro and McCoy 2000 ). Earlier, chronic infections. The biological activities of Morris (1985 ) had demonstrated the susceptibil- most entomopathogenic protozoa are complex. ity of insect pests found in stored products, They grow only in living hosts and some spe- including Ephestia kuehniella Zeller and cies necessitate an intermediate host. Tenebrio molitor L., to an increased concentra- Microsporidia species are among the most tion of nematodes. Georgis (1990 ) had also advo- commonly observed, and their main benefi ts cated a fi eld concentration of >2.5 billion are persistence and recycling in host popula- nematodes/ha against some of the major insect tions and their debilitating effect on reproduc- pests of row crops, but concentrations few times tion and overall fi tness of target insects. As higher (7–15 billion/ha) are demanded to accom- inundatively utilized microbial control agents, plish the control of pest population (Loya and some species have been moderately successful Hower 2002 ). (Solter and Becnel 2000 ). 56 S. Senthil-Nathan

Some protozoan species are pathogenic like 7.1 Neem Nosema locustae for grasshoppers, which is the only species that has been registered and estab- In Asia, neem has an extensive history of use lished commercially (Henry and Oma 1981 ). N. mainly against household and storage pests and, bombycis, the fi rst reported microsporidium, is a to some extent, against insect pests of crops. pathogen of silkworm pébrine, which persisted in Nevertheless, a breakthrough in the insecticidal Europe, North America, and Asia during the application of neem was attained by Pradhan mid-nineteenth century (Becnel and Andreadis et al. (1962 ) who successfully protected the crops 1999 ). Pébrine is still an epidemic and causes from insects by applying them with low concen- heavy economic losses in silk-producing coun- tration of 0.1 % neem seed kernel suspension tries such as China (Cai et al. 2012 ). during a locust invasion. The Indian neem tree Almost 1,000 protozoan species, mainly micro- ( Azadirachta indica ) is one of the most important sporidia, attack invertebrates, including numerous limonoid-producing plants from the Meliaceae insect species like grasshoppers and heliothine family. Several components of its leaves and . Virtually renowned insect- pathogenic pro- seeds show marked insect control potential, and tozoan species are Nosema spp. and Vairimorpha due to their relative selectivity, neem products necatrix . Protozoans produce spores, which are can be recommended for many programs on crop the infectious phase in several susceptible insects. pest management (Schmutterer 1990 ). Neem Nosema spp. spores are assimilated by the host product activity has been assessed against 450– and develop in the midgut. Germinating spores are 500 insect pest species in different countries released from the sporoplasm and invade host tar- around the world, and from that, 413 insect pest get cells, inducing massive infection and demol- species are reportedly susceptible at various con- ishing organs and tissues. Sporulation process centrations (Schmutterer and Singh 1995 ). begins again from the infected tissues and, upon In India alone, neem activity has been assessed expulsion and ingestion by a susceptible host, against 103 species of insect pests, 12 nematodes, induces an epizootic infection. Naturally, parasit- and several pathogenic fungi (Singh and Kataria oids and insect predators commonly act as vectors 1991 ; Arora and Dhaliwal 1994 ). Some recent distributing the disease (Brooks 1988 ). reviews on the potential of neem in pest manage- ment include those of Singh (1996 , 2000 ), Singh and Raheja (1996 ), Naqvi (1996 ), Saxena (1998 ), 7 Botanical Insecticides and Dhaliwal and Arora (2001 ). Most works have focused on azadirachtin (Fig. 5 ) richly from neem Since ancient times, natural compounds from seed extracts which act as both strong antifeed- plants were used, more or less effi caciously to ants and insect growth regulators. Azadirachtin give security from insect pests. In the nineteenth affects the physiological activities of insects century, these compounds became scientifi cally ( Mordue (Luntz) and Blackwell 1993 ) and does established and widely utilized in the earlier not affect other biocontrol agents. Further, neem period of the twentieth century (Morgan 2004 ). products are biodegradable and nontoxic to non- Plants and some insects have coexisted on the target organisms (Senthil-Nathan 2013 ). earth for almost three and a half million years, In several Asian countries, numerous studies which has allowed lots of time for both to develop have measured neem activity alone or in combi- offensive and defensive strategies. Plants have nation with established insecticides and other developed many strategies to assist themselves biocontrol agents of damaging insect pests in from being assaulted by predators. An example agricultural crop system (Abdul Kareem et al. of such plant strategy is developing compounds 1987; Senthil-Nathan et al. 2005a , 2006 ). In that are highly toxic to insects (Warthen and Indian fi eld trials carried out, neem treatments Morgan 1985 ; Arnason et al. 1989 ; Morgan and were determined to be effective against some Wilson 1999 ; Nisha et al. 2012 ). insect species like green leafhopper, yellow stem A Review of Biopesticides and Their Mode of Action Against Insect Pests 57

O M. azedarach, otherwise known as chinaberry or Persian lilac tree, is a deciduous tree that origi- O C-OCH 3 nates from northwestern India, and it has been OH o recognized for its insecticidal properties, which o OH o are still to be entirely analyzed. This tree grows in the tropical and subtropical parts of Asia, but nowadays it is also cultivated in other warm O 7 o O places of the world because of its considerable OH climatic tolerance. The leaves of M. azedarach CH3C - O C o H are used for their insecticidal activity, whereas CH O 3 O the fruit extracts of M. azedarach produce a vari- ety of effects in insects, such as growth retarda- Fig. 5 Structure of azadirachtin tion, reduced fecundity, molting disorders, and behavior changes (Ascher et al. 1995 ). borer, rice gall midge, rice leaffolder, and grass- The antifeedant and insect growth-regulating hopper (Dhaliwal et al. 1996 ; Nanda et al. 1996 ; effects of M. azedarach extracts are known for Senthil-Nathan et al. 2009 ). many insects (Connolly 1983 ; Saxena et al. 1984 ; Champagne et al. 1992; Schmidt et al. 1998 ; Juan et al. 2000 ; Carpinella et al. 2003 ; Senthil-Nathan 7.2 Melia azedarach 2006 ; Senthil-Nathan and Sehoon 2006 ), the latter effect being the most essential physiological effect The promotion of botanicals as eco-friendly pes- of M. azedarach on insects (Ascher et al. 1995 ). ticides, microbial sprays, and insect growth regu- As previously mentioned, the Meliaceae plant lators has been a major concern amid the presence family has been known as a potential source for of other control measures like benefi cial insects, insecticide properties. Also, several extracts from all of which demand an integration of supervised neem and other plant seeds and leaves have excel- insect pest control (Ascher et al. 1995 ). Plant- lent insecticidal properties against vectors and are based insecticides are developed naturally from at the same time very eco-friendly (Schmutterer plant chemicals extracted for use against serious 1990 ; Senthil-Nathan et al. 2005a , b , c). The effi - insect pests. As a result of concerns about the caciousness of these neem products on mosqui- ecological continuity of synthetic pesticides and toes was also demonstrated (Chavan 1984 ; Zebitz their potential toxicity to humans, nontarget ben- 1984 , 1986; Schmutterer 1990 ; Su and Mulla efi cial insects, and some domestic animals, there 1999 ; Senthil-Nathan et al. 2005d ). is a regenerated interest in natural products to Without a doubt, plant-derived toxicants are a control insect pests. From this conclusion, the valuable source of potential insecticides. Plants development of biopesticides seems to be a logi- and other natural insecticides may play a vital cal choice for further investigation. Meliaceae role in mosquito control programs as well as in and Rutaceae species have received much atten- other major insect control programs (Mordue tion due to the fact that they are a rich source of (Luntz) and Blackwell 1993 ). triterpenes known as limonoids (Connolly 1983 ). The Meliaceae plant family is known to hold an assortment of compounds with insecticidal, 8 Biochemical Pesticides antifeedant, growth-regulating, insect- deforming, and growth-modifying properties (Champagne 8.1 Pheromones et al. 1989 ; Schmutterer 1990 ; Mordue (Luntz) and Blackwell 1993 ; Senthil-Nathan and Insects produce chemicals called pheromones to Kalaivani 2005 , 2006 ; Senthil-Nathan 2006 ; stimulate a certain behavioral reaction from other Senthil-Nathan et al. 2004 , 2005a , b , c ). individuals. These pheromones have numerous 58 S. Senthil-Nathan effects and are named according to their evoked Nowadays, pheromones and other semio- response, for example, sex pheromones, aggrega- chemicals are applied to monitor and control tion pheromones, alarm pheromones, etc. A few pests in millions of hectares. There are several pheromones function as sex attractants, permit- advantages of utilizing pheromones for monitor- ting individuals to detect and locate mates, ing pests, including lower costs, specifi city, ease whereas others induce trail following, oviposi- of use, and high sensitivity (Wall 1990 ; Laurent tion, and aggregation in other congeners. and Frérot 2007 ; Witzgall et al. 2010 ). Insect pest Pheromones have become essential tools for monitoring by using pheromone lures can profi t monitoring and controlling agricultural pest pop- management conclusions such as insecticide ulations, and as such, a huge collection of over application timing (Leskey et al. 2012 ; Peng et al. 1,600 pheromones and sex attractants has been 2012 ). reported (Witzgall et al. 2004 ). Pheromones produced by insects are highly In the past decades, there has been a signifi cant species specifi c. Virgin female insects are devel- volume of literature on insect pheromones and oping sex pheromones when expecting for a mate new opportunities have arisen to explore the use and males along the concentration slope for the of semiochemicals in managing insect pest prob- female producer. Aggregation pheromones are lems. Insect control by pheromones alone has pre- released by insects such as wood-invading bee- cincts, but they can be applied in integrated tles to show to others the presence of a good food control in combination with other practices source (Copping and Menn 2000 ). (Howse et al. 1998 ; Reddy and Guerrero 2004 ). Some of the alarm pheromones are developed Plant volatiles are recognized as an integral part by insects that are beneath approach from a pred- of the pheromone system of various Coleopteran ator and this contributes to a movement of the species studied so far. How the combinations of insect pest aside from the production source and, pheromones and plant volatiles are incorporated therefore it becomes dangerous. Plants and its into the insects’ olfactory systems so that they can derived attractants are also known that interact discriminate pheromone molecules alone and with the insects to a valuable food source and, pheromone plus odor plume strands and react while combine with insect-derived attractants behaviorally to these signals is a question of will be developed a potent attraction to some increasing importance (Baker and Heath 2004 ). insect pests (Copping and Menn 2000 ). Recently, the pest management system has In previous studies, Mayer and McLaughlin undergone an intentional shift from calendar- ( 1991 ) proposed that all insects produce approxi- based, broad-spectrum insecticide applications to mate form of pheromone and companies subsist more holistic, integrated, and high-effi cacy that synthesize a pheromone for any customer. approaches. Furthermore, environmental conser- Recently, 30 mating-disruption pheromone- vation, food safety, and resistance management based products are registered by the US EPA as are a few of the key components guiding current biocontrol agents of lepidopteran pest species pest management policies in commercial agricul- that can cause agricultural damage (Copping and ture (Witzgall et al. 2010 ). Menn 2000 ). Kogan and Jepson (2007 ) had reported that meeting the necessities of the quickly expanding global population while incorporating sustain- 9 Conclusion ability and ecological stewardship is a major challenge facing modern agriculture. In agricul- The utilization of natural products with com- tural fi elds, the application of pheromones and/or mercial value is directly manifested by the allelochemicals as behavioral manipulation tools numerous compounds present in the market and can replace or complement existing pest manage- that have remained there in many cases after ment programs (Witzgall et al. 2008 ), resulting in many years. These values of natural products a decreased rate of broad-spectrum use. are considered as a source of new mechanisms A Review of Biopesticides and Their Mode of Action Against Insect Pests 59 and their consequent incorporation into high-output Barber KN, Kaupp WJ, Holmes SB (1993) Specifi city screens is hard to evaluate. Recently, several testing of the nuclear polyhedrosis virus of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: works have been exercised and extend to be Lymantriidae). Can Entomol 125:1055–1066 undertaken to enhance the shelf life, immediate Becnel JJ, Andreadis TG (1999) Microsporidia in insects. death, the biological scheme, effi cient in the In: Wittner M, Weiss LM (eds) The Microsporidia and fi eld and dependability, and the effect of cost of Microsporidiosis. ASM Press, Washington, DC, pp 447–501 living systems and there have been some notable Betz FS, Hammond BG, Fuchs RL (2000) Safety and successes in situations where some disruption to advantages of Bacillus thuringiensis -protected plants the crop is acceptable. to control insect pests. Regul Toxicol Pharmacol 32:156–173 Bird AF, Akhurst RJ (1983) The nature of the intestinal Acknowledgments This book chapter was supported by vesicle in nematodes of the family Steinernematidae. the grants from the Department of Biotechnology, Int J Parasitol 13:599–606 Government of India (BT/PR12049/AGR/05/468/2009). I Brooks FM (1988) Entomogenous protozoa. In: Ignoffo would like to thank my lab members, Dr. Kannan Revathi, CM, Mandava MB (eds) Handbook of natural pesti- Dr. Rajamanickam Chandrasekaran, and Venkatraman cides, vol V, Microbial Insecticides, Part A, Pradeepa, for their help during the preparation of this Entomogenous Protozoa and Fungi. CRC Press Inc, book chapter. Also, I extend my thanks to K. Karthikeyan Boca Raton, pp 1–149 for his help. Butt TM, Jackson CW, Magan N (2001a) Fungi as bio- control agents: progress, problems and potential. CAB International, Wallingford References Butt TM, Jackson C, Magan N (2001b) Introduction- fungal biological control agents: problems and poten- tial. In: Butt TM, Jackson C, Magan N (eds) Fungi as Abdul Kareem A, Saxena RC, Justo HD Jr (1987) Cost biocontrol agents: progress, problems and potential. comparison of neem oil and an insecticide against rice CAB International, Wallingford, pp 1–9 tungro virus (RTV). Int Rice Res Newsl 12:28–29 Cai S-F, Lu X-M, Qiu H-H, Li M-Q, Feng Z-Z (2012) Arnason JT, Philogène BJR, Morand P (1989) Insecticides Phagocytic uptake of Nosema bombycis of plant origin. ACS symposium series 387, American (Microsporidia) spores by insect cell lines. J Integr Chemical Society, Washington, DC Agric 11:1321–1326 Aronson AI, Shai Y (2001) Why Bacillus thuringiensis Carlton BC (1993) Genetics of Bt insecticidal crystal pro- insecticidal toxins are so effective: unique features of teins and strategies for the construction of improved their mode of action. FEMS Microbiol Lett 195:1–8 strains. In: Duke SO, Menn JJ, Plimmer JR (eds), Pest Arora R, Dhaliwal GS (1994) Botanical pesticides in control with enhanced environmental safety. ACS insect pest management. In: Dhaliwal GS, Kansal BD symposium series 524, American Chemical Society, (eds) Management of agricultural pollution in India. Washington, DC. pp 326–337 Commonwealth Publications, New Delhi, pp 213–245 Carpinella MC, Defago MT, Valladares G, Palacios SM Arthurs SP, Lacey LA (2004) Field evaluation of commer- (2003) Antifeedant and insecticide properties of a cial formulations of the codling moth granulovirus: limonoid from Melia azedarach (Meliaceae) with persistence of activity and success of seasonal applica- potential use for pest management. J Agric Food Chem tions against natural infestations of codling moth in 15:369–374 Pacifi c Northwest apple orchards. Biol Control Champagne DE, Isman MB, Towers GHN (1989) 31:388–397 Insecticidal activity of phytochemicals and extracts of Arthurs SP, Lacey LA, Fritts R Jr (2005) Optimizing use the Meliaceae. In: Arnason JT, Philogene BJR, of codling moth granulovirus: effects of application Morand P (eds) Insecticides of plant origin. American rate and spraying frequency on control of codling Chemical Society symposium series 387, pp 95–109 moth larvae in Pacifi c Northwest apple orchards. J Champagne DE, Koul O, Isman MB, Scudder GGE, Econ Entomol 98:1459–1468 Towers GHN (1992) Biological activity of limonoids Ascher KRS, Schmutterer H, Zebitz CPW, Naqvi SNH from the Rutales . Phytochemistry 31:377–394 (1995) The Persian lilac or chinaberry tree: Melia aze- Chandrasekaran R, Revathi K, Nisha S, Kirubakaran SA, darach L. In: Schmutterer H (ed) The neem tree: Sathish-Narayanan S, Senthil-Nathan S (2012) source of unique natural products for integrated pest Physiological effect of chitinase purifi ed from Bacillus management, medicine, industry and other purposes. subtilis against the tobacco cutworm Spodoptera litura VCH, Weinheim, pp 605–642 Fab. Pestic Biochem Physiol 104:65–71 Baker TC, Heath JJ (2004) Pheromones-function and use Chavan SR (1984) Chemistry of alkanes separated from in insect control. In: Gilbert LI, Iatro K, Gill SS (eds) leaves of Azadirachta indica and their larvicidal/insec- Molecular insect science. Elsevier, Amsterdam, ticidal activity against mosquitoes. In: Schmutterer H, pp 407–460 Ascher KRS (eds) Natural pesticides from the neem 60 S. Senthil-Nathan

tree and other tropical plant, proceedings of the 2nd genetic diversity in the entomopathogenic fungus international neem conference, Rauischholzhausen, Metarhizium anisopliae var. anisopliae . Microbiology Federal Republic of Germany, 25–28 May 1983, 139:2075–2081 pp 59–66 Gelernter W, Schwab GE (1993) Transgenic bacteria, Chilcott CN, Kalmakoff J, Pillai JS (1983) Characterization viruses, algae and other microorganisms as Bacillus of proteolytic activity associated with Bacillus thuringiensis toxin delivery systems. In: Entwistle PF, thuringiensis var. israelensis crystals. FEMS Microbiol Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringi- Lett 18:37–41 ensis , an environmental biopesticide: theory and prac- Connolly JD (1983) Chemistry of the Meliaceae and tice. Wiley, Chichester, pp 89–124 Cneoraceae . In: Waterman PG, Grunden MF (eds) Georgis R (1990) Formulation and application technol- Chemistry and chemical taxonomy of the rutales. ogy. In: Gaugler R, Kaya HK (eds) Entomopathogenic Academic, London, pp 175–213 nematodes in biological control. CRC Press, Boca Copping LG, Menn JJ (2000) Biopesticides: a review of Raton, pp 173–191 their action, applications and effi cacy. Pest Manag Sci Goettel MS, Jaronski ST (1997) Safety and registration of 56:651–676 microbial agents for control of grasshoppers and Cory JS (2000) Assessing the risks of releasing geneti- locusts. In: Goettel MS, Johnson DL (eds) Microbial cally modifi ed virus insecticides: progress to date. control of grasshoppers and locusts, vol 171, Memoirs Crop Prot 19:779–785 of the Entomological Society of Canada., pp 83–99 Cory JS, Hirst ML, Sterling PH, Speight MR (2000) Goettel MS, Hajek AE, Siegel JP, Evans HC (2001) Safety Native host range nucleopolyhedric virus for control of fungal biocontrol agents. In: Butt TM, Jackson C, of the browntail moth (Lepidoptera: Lymantriidae). Magan N (eds) Fungi as biocontrol agents: progress, Environ Entomol 29:661–667 problems and potential. CAB International, Darboux I, Nielsen-LeRoux C, Charles J-F, Pauron D Wallingford, pp 347–375 (2001) The receptor of Bacillus sphaericus binary Goldberg LH, Margalit J (1977) A bacterial spore demon- toxin in Culex pipiens (Diptera: Culicidae) midgut: strating rapid larvicidal activity against Anopheles ser- molecular cloning and expression. Insect Biochem gentii , Uranotaenia unguiculata , Culex univittatus , Mol Biol 31:981–990 Aedes aegypti and Culex pipiens. Mosq News Dhaliwal GS, Arora R (2001) Role of phytochemicals in 37:355–358 integrated pest management. In: Koul O, Dhaliwal GS Gray EJ, Lee KD, Souleimanov AM, Di Falco MR, Zhou (eds) Phytochemical biopesticides. Harwood X, Ly A, Charles TC, Driscoll BT, Smith DL (2006) A Academic Publishers, Amsterdam, pp 97–117 novel bacteriocin, thuricin 17, produced by plant Dhaliwal GS, Singh J, Dilawari VK (1996) Potential of growth promoting rhizobacteria strain Bacillus neem in insect pest management in rice. In: Singh RP, thuringiensis NEB17: isolation and classifi cation. J Chari MS, Raheja AK, Kraus W (eds) Neem and envi- Appl Microbiol 100:545–554 ronment, vol 1. Oxford and IBH Publishing Co. Pvt. Grewal PS, Lewis EE, Gaugler R (1997) Response of Ltd, New Delhi, pp 425–431 infective stage parasites (Nematoda: Steinernematidae) Domsch KH, Gams W, Anderson TH (1980) Compendium to volatile cues from infected hosts. J Chem Ecol of soil fungi. Academic, London, pp 413–415 23:503–515 Driver F, Milner RJ, Trueman JWH (2000) A taxonomic Grewal PS, Ehlers R-U, Shapiro-Ilan DI (2005) revision of Metarhizium based on a phylogenetic anal- Nematodes as biocontrol agents. CABI Publishing, ysis of rDNA sequence data. Mycol Res 104:134–150 Wallingford, pp 505 Duncan LW, McCoy CW (1996) Vertical distribution in Henry JE, Oma EA (1981) Pest control by Nosema locus- soil, persistence, and effi cacy against citrus root wee- tae, a pathogen of grasshoppers and crickets. In: vil (Coleoptera: Curculionidae) of two species of ento- Burges HD (ed) Microbial control of pests and plant mogenous nematodes (Rhabditida: Steinernematidae; diseases. Academic, London, pp 573–586 Heterorhabditidae). Environ Entomol 25:174–178 Hom A (1996) Microbials, IPM and the consumer. IPM EPA (Environmental Protection Agency) (2006) New Pract 18:1–11 biopesticide active ingredients. www.epa.gov/pesti- Howse P, Stevens I, Jones O (1998) Insect pheromones cides/biopesticides/product lists/ . Accessed 23 July and their use in pest management. Chapman and Hill, 2013 London, pp 639 EPA (Environmental Protection Agency) (2013) James C (2009) Global status of commercialized biotech/ Regulating biopesticides. www.epa.gov/opp00001/ GM crops. ISAAA Brief No. 41, I. ISAAA, Ithaca biopesticides . Accessed 23 July 2013 Juan A, Sans A, Riba M (2000) Antifeedant activity of Faria MR, Magalhães BP (2001) O uso de fungos ento- fruit and seed extracts of Melia azedarach and mopatogênicos no Brasil. Biotecnol Cienc Azadirachta indica on larvae of Sesamia nonagrioi- Desenvolvimento 22:18–21 des . Phytoparsitica 28:311–319 Fegan M, Manners JM, Maclean DJ, Irwin JAG, Samuels Kogan M, Jepson P (2007) Ecology, sustainable develop- KDZ, Holdom DG, Li DP (1993) Random amplifi ed ment and IPM: the human factor. In: Kogan M, Jepson polymorphic DNA markers reveal a high degree of P (eds) Perspectives in ecological theory and inte- A Review of Biopesticides and Their Mode of Action Against Insect Pests 61

grated pest management. Cambridge University Press, feltiae and Heterorhabditis bacteriophora . Can Cambridge, UK, pp 1–44 Entomol 122:309–320 Kolodny-Hirsch DM, Sitchawat T, Jansiri T, Moscardi F (1999) Assessment of the application of bacu- Chenrchaivachirakul A, Ketunuti U (1997) Field eval- loviruses for control of Lepidoptera. Annu Rev uation of a commercial formulation of the Spodoptera Entomol 44:257–289 exigua (Lepidoptera: Noctuidae) nuclear polyhedrosis Nanda UK, Parija B, Pradhan WC, Nanda B, Dash DD virus for control of beet armyworm on vegetable crops (1996) Bioeffi cacy of neem derivatives against insect in Thailand. Biocontrol Sci Tech 7:475–488 pest complex of rice. In: Singh RP, Chari MS, Raheja Kumar S (2012) Biopesticides: a need for food and envi- AK, Kraus W (eds) Neem and environment. Oxford ronmental safety. J Biofertil Biopestic 3:4 and IBH Publishing Co. Pvt. Ltd, New Delhi, Laurent P, Frérot B (2007) Monitoring of European corn pp 517–527 borer with pheromone-baited traps: review of trapping Naqvi SNH (1996) Prospects and development of a neem system basics and remaining problems. J Econ based pesticide in Pakistan. In: Proceedings of the Entomol 100:1797–1807 16th Congress of Zoology, Islamabad, pp 325–338 Leskey TC, Wright SE, Short BD, Khrimian A (2012) Nisha S, Revathi K, Chandrasekaran R, Kirubakaran SA, Development of behaviorally-based monitoring tools Sathish-Narayanan S, Stout MJ, Senthil-Nathan S for the brown marmorated stink bug (Heteroptera: (2012) Effect of plant compounds on induced activi- Pentatomidae) in commercial tree fruit orchards. J ties of defense-related enzymes and pathogenesis Entomol Sci 47:76–85 related protein in bacterial blight disease susceptible Loya LJ, Hower AA Jr (2002) Population dynamics, per- rice plant. Physiol Mol Plant Pathol 80:1–9 sistence, and effi cacy of the entomopathogenic nema- Peng C-L, Gu P, Li J, Chen Q-Y, Feng C-H, Luo H-H, Du tode Heterorhabditis bacteriophora (Oswego strain) Y-J (2012) Identifi cation and fi eld bioassay of the sex in association with the clover root curculio (Coleoptera: pheromone of Trichophysetis cretacea (Lepidoptera: Curculionidae) in Pennsylvania. Environ Entomol ). J Econ Entomol 105:1566–1572 31:1240–1250 Peters A (1996) The natural host range of Steinernema Maddox JV (1987) Protozoan diseases. In: Fuxa JR, and Heterorhabditis spp. and their impact on insect Tanada Y (eds) Epizootiology of insect diseases. populations. Biocontrol Sci Technol 6:389–402 Wiley, New York, pp 417–452 Pomar GO Jr, Leutenegger R (1968) Anatomy of the Mayer MS, McLaughlin JR (1991) Handbook of insect effective and normal third stage juveniles of pheromones and sex attractants. CRC Press, Boca Steinernema carpocapsae Weiser (Steinernematidae: Raton Nematoda). J Parasitol 54:340–350 Mazid S, Kalida JC, Rajkhowa RC (2011) A review on the Popham HJR, Li Y, Miller LK (1997) Genetic improve- use of biopesticides in insect pest management. Int J ment of Helicoverpa zea nuclear polyhedrosis virus as Sci Adv Technol 1:169–178 a biopesticide. Biol Control 10:83–91 McSorely R (1999) Non-chemical management of plant- Pradhan S, Jotwani MG, Rai BK (1962) The neem seed parasitic nematodes. IPM Pract 21:1–7 deterrent to locust. Indian Farm 12:7–11 Menn JJ, Hall FR (1999) Biopesticides: present status and Prater CA, Redmond C, Barney W, Bonning BC, Potter future prospects. In: Hall FR, Menn JJ (eds) DA (2006) Microbial control of black cutworm Biopesticides use and delivery. Humana Press, Totowa, (Lepidoptera: Noctuidae) in turfgrass using Agrotis pp 1–10 ipsilon multiple nucleopolyhedrovirus. J Econ Miller LK (1997) The Baculovirus. Plenum Press, Entomol 99:1129–1137 New York, pp 7–32 Reddy GVP, Guerrero A (2004) Interactions of insect Mnyone LL, Koenraadt CJM, Lyimo IN, Mpingwa MW, pheromones and plant semiochemicals. Trends Plant Takken W, Russell TL (2010) Anopheline and culicine Sci 9:253–261 mosquitoes are not repelled by surfaces treated with Revathi K, Chandrasekaran R, Thanigaivel A, Kirubakaran the entomopathogenic fungi Metarhizium anisopliae SA, Sathish-Narayanan S, Senthil-Nathan S (2013) and Beauveria bassiana . Parasite Vectors 3:80 Effects of Bacillus subtilis metabolites on larval Aedes Mordue (Luntz) AJ, Blackwell A (1993) Azadirachtin: an aegypti L. Pestic Biochem Physiol 107:369–376 update. J Insect Physiol 39:903–924 Richards A, Speight MR, Cory J (1999) Characterization Morgan ED (2004) The place of neem among modern of a nucleopolyhedrovirus from the vapourer moth, natural pesticides. In: Koul O, Wahab S (eds) Neem: Orgyia antiqua (Lepidoptera Lymantriidae). today and in the New Millennium. Kluwer Academic J Invertebr Pathol 74:137–142 Publishers, Dordrecht, Holland, pp 21–32 Roberts DW, St Leger RJ (2004) Metarhizium spp., cos- Morgan ED, Wilson ID (1999) Insect hormones and insect mopolitan insect-pathogenic fungi: mycological chemical ecology. In: Mori K (ed) Comprehensive aspects. Adv Appl Microbiol 54:1–70 natural products chemistry. Elsevier, Amsterdam, The Saxena RC (1998) “Green revolutions” without blues: Netherlands, pp 263–375 botanicals for pest management. In: Dhaliwal GS, Morris ON (1985) Susceptibility of 31 species of agricul- Randhawa NS, Arora R, Dhawan AK (eds) Ecological tural pests to entomogenous nematodes Steinernema agriculture and sustainable development, vol 2. Indian 62 S. Senthil-Nathan

Ecological Society and Centre for Research in Rural bacterial toxins and botanical insecticides. and Industrial Development, Chandigarh, pp 111–127 Chemosphere 64:1650–1658 Saxena RC, Epino PB, Cheng WT, Puma BC (1984) Senthil-Nathan S (2006) Effects of Melia azedarach on Neem, chinaberry and custard apple: antifeedant and nutritional physiology and enzyme activities of the insecticidal effects of seed oils on leafhopper and rice leaffolder Cnaphalocrocis medinalis (Guenée) planthopper pests of rice. In: Schmutterer H, Ascher (Lepidoptera: Pyralidae). Pestic Biochem Physiol KRS (eds) Natural pesticides from the neem tree and 84:98–108 other tropical plants, proceedings of the 2nd Senthil-Nathan S (2013) Physiological and biochemical International Neem Conference, Rauischholzhausen, effect of neem and other Meliaceae plants secondary Federal Republic of Germany, 25–28 May 1983, metabolites against Lepidopteran insects. Front pp 403–412 Physiol 4:359 Schmidt GH, Rembold H, Ahmed AAI, Breuer AM Senthil-Nathan S, Choi M-Y, Paik C-H, Seo H-Y, (1998) Effect of Melia azedarach fruit extract on Kalaivani K (2009) Toxicity and physiological effects juvenile hormone titer and protein content in the of neem pesticides applied to rice on the Nilaparvata hemolymph of two species of noctuid lepidopteran lugens Stål, the brown planthopper. Ecotoxicol larvae (Insecta: Lepidoptera: Noctuidae). Environ Saf 72:1707–1713 Phytoparasitica 26:283–292 Shannag HK, Capinera JL (2000) Interference of Steinernema Schmutterer H (1990) Properties and potential of natural carpocapsae (Nematoda: Steinernematidae) with pesticides from the neem tree, Azadirachta indica . Cardiochiles diaphaniae (Hymenoptera: Braconidae), a Annu Rev Entomol 35:271–297 parasitoid of melonworm and pickleworm (Lepidoptera: Schmutterer H, Singh RP (1995) List of insect pests sus- Pyralidae). Environ Entomol 29:612–617 ceptible to neem products. In: Schmutterer H (ed) The Shapiro DI, McCoy CW (2000) Virulence of entomo- neem tree: source of unique natural products for inte- pathogenic nematodes to Diaprepes abbreviatus grated pest management, medicine, industry and other (Coleoptera: Curculionidae) in the laboratory. J Econ purposes. VCH, Weinheim, pp 325–326 Entomol 93:1090–1095 Senthil-Nathan S, Kalaivani K (2005) Effi cacy of nucleo- Singh RP (1996) Bioactivity against insect pests. In: polyhedrovirus and azadirachtin on Spodoptera litura Randhawa NS, Parmar BS (eds) Neem research and Fabricius (Lepidoptera: Noctuidae). Biol Control development. New Age International (P) Ltd., New 34:93–98 Delhi, pp 146–159 Senthil-Nathan S, Kalaivani K (2006) Combined effects Singh RP (2000) Botanicals in pest management: an eco- of azadirachtin and nucleopolyhedrovirus (SpltNPV) logical perspective. In: Dhaliwal GS, Singh B (eds) on Spodoptera litura Fabricius (Lepidoptera: Pesticides and environment. Commonwealth Noctuidae) larvae. Biol Control 39:96–104 Publishers, New Delhi, pp 279–343 Senthil-Nathan S, Sehoon K (2006) Effects of Melia aze- Singh RP, Kataria PK (1991) Insects, nematodes and darach L. extract on the teak defoliator Hyblaea puera fungi evaluated with neem ( Azadirachta indica Cramer (Lepidoptera: Hyblaeidae). Crop Prot A. Juss) in India. Neem Newsl 8:3–10 25:287–291 Singh RP, Raheja AK (1996) Strategies in management Senthil-Nathan S, Chung PG, Murugan K (2004) Effect of of insect pests with neem ( Azadirachta indica botanical insecticides and bacterial toxins on the gut A. Juss). In: Singh RP, Chari MS, Raheja AK, Kraus enzyme of the rice leaffolder Cnaphalocrocis medina- W (eds) Neem and environment, vol 1. Oxford & IBH lis . Phytoparasitica 32:433–443 Publishing Co. Pvt. Ltd., New Delhi, pp 103–120 Senthil-Nathan S, Chung PG, Murugan K (2005a) Effect Solter LF, Becnel JJ (2000) Entomopathogenic microspo- of biopesticides applied separately or together on rida. In: Lacey LA, Kaya HK (eds) Field manual of nutritional indices of the rice leaffolder Cnaphalocrocis techniques in invertebrate pathology: application and medinalis . Phytoparasitica 33:187–195 evaluation of pathogens for control of insects and Senthil-Nathan S, Kalaivani K, Murugan K, Chung PG other invertebrate pests. Kluwer Academic, Dordrecht, (2005b) Effi cacy of neem limonoids on Cnaphalocrocis pp 231–254 medinalis (Guenée) (Lepidoptera: Pyralidae) the rice Su T, Mulla MS (1999) Oviposition bioassay responses of leaffolder. Crop Prot 24(8):760–763 Culex tarsalis and Culex quinquefasciatus to neem Senthil-Nathan S, Kalaivani K, Murugan K, Chung PG products containing azadirachtin. Entomol Exp Appl (2005c) The toxicity and physiological effect of neem 91:337–345 limonoids on Cnaphalocrocis medinalis (Guenée) the Tulloch M (1976) The genus Metarhizium . Trans Br rice leaffolder. Pestic Biochem Physiol 81:113–122 Mycol Soc 66:407–411 Senthil-Nathan S, Kalaivani K, Murugan K (2005d) Wall C (1990) Principle of monitoring. In: Ridgeway RL, Effects of neem limonoids on the malaria vector Silverstein RM, Inscoe MN (eds) Behavior- modify- Anopheles stephensi Liston (Diptera: Culicidae). Acta ing chemicals for insect management: applications of Trop 96:47–55 pheromones and other attractants. Marcel Dekker Inc., Senthil-Nathan S, Kalaivani K, Murugan K (2006) New York, pp 9–23 Behavioural responses and changes in biology of rice Warthen JD, Morgan ED (1985) Insect feeding deterrents. leaffolder following treatment with a combination of In: Morgan ED, Mandava NB (eds) Handbook of natu- A Review of Biopesticides and Their Mode of Action Against Insect Pests 63

ral pesticides, vol 6, Insect Attractants and Repellents. kernel extracts on larvae of Aedes aegypti . Entomol CRC Press, Boca Raton, pp 23–149, 4 Exp Appl 35:11–16 Witzgall P, Lindblom T, Bengtsson M, Toth M (2004) The Zebitz CPW (1986) Effects of three neem seed kernel Pherolist. http://www.pherolist.slu.se/pherolist.php . extracts and azadirachtin on larvae of different mos- Accessed 23 July 2013 quito species. J Appl Entomol 102:455–463 Witzgall P, Stelinski L, Gut L, Thomson D (2008) Codling Zhu Y-C, Kramer KJ, Oppert B, Dowdy AK (2000) moth management and chemical ecology. Annu Rev cDNAs of aminopeptidase-like protein genes from Entomol 53:503–522 Plodia interpunctella strains with different suscepti- Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and bilities to Bacillus thuringiensis toxins. Insect their impact on pest management. J Chem Ecol Biochem Mol Biol 30:215–224 36:80–100 Zimmermann G (1993) The entomopathogenic fungus Zebitz CPW (1984) Effects of some crude and Metarhizium anisopliae and its potential as a biocon- azadirachtin-enriched neem ( Azadirachta indica ) seed trol agent. Pest Manag Sci 37:375–379

View publication stats