Chemical ecology and conservation biological control

Abstract Elucidating the chemical ecology of natural enemies, herbivores and host plants is important in the development of effective and successful integrated pest management (IPM) strategies where abundance and distribution of natural enemies could be manipulated by semiochemicals for improved conservation biological control (CBC). In response to attack by herbivores, plants produce semiochemicals called Herbivore-Induced Plant Volatiles (HIPVs) which act to repel pests and attract their natural enemies. Damaged, and in some cases, intact plants may also produce volatile signals that warn other plants of impending attack. Some of these intact plants are used as intercrops in ‘push–pull’ strategies; cropping systems based on stimulo-deterrent principle, where the target crop is intercropped with herbivore repellent plants (push) while attractant plants (pull) are planted around this intercrop. The intercrop, in addition to repelling the herbivores, attracts and conserves natural enemies thereby ensuring continued suppression of the pests. This natural delivery of semiochemicals for CBC is currently being exploited by smallholder farmers in eastern Africa in the management of cereal stemborers in maize and sorghum. Synthetic HIPVs also have the potential to effectively recruit natural enemies, thereby improving CBC as has been demonstrated in a series of field experiments in vineyards and hop yards in the Pacific Northwest of the United States. Potentially, plants could be ‘turned on’ by synthetic HIPV signals, and therefore become sources of natural enemy-recruiting volatiles. With the rapid development of plant molecular biology, modification of secondary plant metabolism is also possible which could allow appropriate semiochemicals to be generated by plants at certain growth stages. By identifying the promoter sequences associated with external plant signals that induce biochemical pathways, plant defense genes could be ‘switched on’ prior to insect attack. We review recent research on ‘push–pull’ strategies and synthetic HIPVs in recruitment of beneficial arthropods and warding off pest attack.

[1]  A. Arab,et al.  Differential Attractiveness of Potato Tuber Volatiles to Phthorimaea operculella (Gelechiidae) and the Predator Orius insidiosus (Anthocoridae) , 2007, Journal of Chemical Ecology.

[2]  M. Sabelis,et al.  LOCATION OF DISTANT SPIDER MITE COLONIES BY PHYTOSEIID PREDATORS: DEMONSTRATION OF SPECIFIC KAIROMONES EMITTED BY TETRANYCHUS URTICAE AND PANONYCHUS ULMI , 1983 .

[3]  Z. Dąbrowski,et al.  Biodiversity and Habitat Modification in Pest Management , 1994 .

[4]  Christine M. Woodcock,et al.  Exploiting chemical ecology and species diversity : stem borer and striga control for maize and sorghum in Africa , 2000 .

[5]  T. Meiners,et al.  Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison , 2002 .

[6]  G. Poppy,et al.  Identification of Semiochemicals Released During Aphid Feeding That Attract Parasitoid Aphidius ervi , 1998, Journal of Chemical Ecology.

[7]  J. Takabayashi,et al.  Volatile herbivore-induced terpenoids in plant-mite interactions: Variation caused by biotic and abiotic factors , 1994, Journal of Chemical Ecology.

[8]  J. van den Berg,et al.  Habitat management and its impact on maize stemborer colonization and crop damage levels in Kenya and South Africa , 2005 .

[9]  T. Grasswitz,et al.  Using synthetic herbivor-induced plant volatiles to enhance conservation biological control: field experiments in hops and grapes. , 2005 .

[10]  G. Yè,et al.  Differences in Induced Volatile Emissions among Rice Varieties Result in Differential Attraction and Parasitism of Nilaparvata lugens Eggs by the Parasitoid Anagrus nilaparvatae in the Field , 2006, Journal of Chemical Ecology.

[11]  Richard M. Caprioli,et al.  Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature , 2022 .

[12]  M. Sabelis,et al.  Long range dispersal and searching behaviour , 1985 .

[13]  A. Hall Induced Responses to Herbivory. , 1999 .

[14]  Christine Woodcock,et al.  Intercropping increases parasitism of pests , 1997, Nature.

[15]  H. Herren,et al.  Integrated pest management: the push–pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  J A Pickett,et al.  New roles for cis-jasmone as an insect semiochemical and in plant defense. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Polaszek,et al.  Utilisation of Wild Gramineous Plants for Management of Cereal Stemborers in Africa , 1997 .

[18]  D. G. James,et al.  Synthetic Herbivore-induced Plant Volatiles Increase Field Captures of Parasitic Wasps , 2005, BioControl.

[19]  I. Baldwin,et al.  Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  John H. Loughrin,et al.  How caterpillar-damaged plants protect themselves by attracting parasitic wasps. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  C. Borgemeister,et al.  Spatial dynamics of lepidopterous pests on Zea mays (L.) and Pennisetum purpureum (Moench) in the forest zone of Cameroon and their implications for sampling schemes , 2001 .

[22]  P. Edwards,et al.  Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.) , 2001 .

[23]  Maurice W. Sabelis,et al.  Spider mites: their biology, natural enemies and control: vol. 1A , 1985 .

[24]  W. Boland,et al.  Mevalonate-Independent Biosynthesis of Terpenoid Volatiles in Plants: Induced and Constitutive Emission of Volatiles. , 1998, Angewandte Chemie.

[25]  I. Baldwin,et al.  Plant responses to insect herbivory: the emerging molecular analysis. , 2002, Annual review of plant biology.

[26]  L. Wadhams,et al.  Habitat Management Strategies for the Control of Cereal Stemborers and Striga in Maize in Kenya , 2001 .

[27]  Mary Finlay-Doney,et al.  Ecological Engineering for Pest Management: Advances in Habitat Manipulation for Arthropods , 2005 .

[28]  M. Hilker,et al.  Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. , 2002, The Journal of experimental biology.

[29]  K. Dhileepan,et al.  Effects of gall damage by the introduced biocontrol agent Epiblema strenuana (Lep., Tortricidae) on the weed Parthenium hysterophorus (Asteraceae) , 2001 .

[30]  J. Gershenzon,et al.  The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. G. James,et al.  Further Field Evaluation Of Synthetic Herbivore-Induced Plan Volatiles As Attractants For Beneficial Insects , 2005, Journal of Chemical Ecology.

[32]  M. Hunter A breath of fresh air: beyond laboratory studies of plant volatile–natural enemy interactions , 2002 .

[33]  D. Landis,et al.  Habitat management to conserve natural enemies of arthropod pests in agriculture. , 2000, Annual review of entomology.

[34]  Zeyaur R. Khan,et al.  On-farm evaluation of the 'push-pull' technology for the control of stemborers and striga weed on maize in western Kenya , 2008 .

[35]  P. Barbosa Conservation biological control. , 1998 .

[36]  W. Takken,et al.  Chemical ecology: from gene to ecosystem. , 2006 .

[37]  E. F. Dwumfour Volatile substances evoking orientation in the predatory flowerbug Anthocoris nemorum (Heteroptera: Anthocoridae) , 1992 .

[38]  J. Pickett,et al.  The use of push-pull strategies in integrated pest management. , 2007, Annual review of entomology.

[39]  Peeter Päts,et al.  Activity of Chilo partellus (Lepidoptera: Pyralidae): eclosion, mating and oviposition time , 1991 .

[40]  Ilya Raskin,et al.  Airborne signalling by methyl salicylate in plant pathogen resistance , 1997, Nature.

[41]  D. G. James,et al.  Field-Testing of Methyl Salicylate for Recruitment and Retention of Beneficial Insects in Grapes and Hops , 2004, Journal of Chemical Ecology.

[42]  K. Chamberlain,et al.  Electrophysiological Responses of the Lepidopterous Stemborers Chilo partellus and Busseola fusca to Volatiles from Wild and Cultivated Host Plants , 2006, Journal of Chemical Ecology.

[43]  I. Baldwin,et al.  Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. VII. Changes in the Plant's Proteome1[W] , 2006, Plant Physiology.

[44]  M. Sabelis,et al.  Location of distant spider-mite colonies by Phytoseiulus persimilis: localisation and extraction of a kairomone , 1984 .

[45]  W. Boland,et al.  Biosynthesis of C11 and C16 homoterpenes in higher plants; stereochemistry of the CC-bond cleavage reaction , 1998 .

[46]  L. Wadhams,et al.  Evaluation of Napier grass (Pennisetum purpureum) varieties for use as trap plants for the management of African stemborer (Busseola fusca) in a push–pull strategy , 2007 .

[47]  S. Wratten,et al.  Ecological Engineering for Pest Management , 2004 .

[48]  Jim Hardie,et al.  Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants , 1999 .

[49]  K. Chamberlain,et al.  Diel Periodicity in the Production of Green Leaf Volatiles by Wild and Cultivated Host Plants of Stemborer Moths, Chilo partellus and Busseola fusca , 2006, Journal of Chemical Ecology.

[50]  Richard M. Wilkins,et al.  Assessment of the potential of Napier grass (Pennisetum purpureum) varieties as trap plants for management of Chilo partellus , 2006 .

[51]  W. Overholt,et al.  Behaviour and biology of Chilo partellus (Lepidoptera: Pyralidae) on maize and wild gramineous plants , 2004 .

[52]  Ted C. J. Turlings,et al.  An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion , 1997 .

[53]  N. Kidd,et al.  Use of a sprayed L‐tryptophan solution to concentrate numbers of the green lacewing Chrysoperla carnea in olive tree canopy , 1994 .

[54]  R. B. Root Organization of a Plant-Arthropod Association in Simple and Diverse Habitats: The Fauna of Collards (Brassica Oleracea) , 1973 .

[55]  J. Pickett,et al.  Effects of Molasses Grass, Melinis minutiflora Volatiles on the Foraging Behavior of the Cereal Stemborer Parasitoid, Cotesia sesamiae , 2003, Journal of Chemical Ecology.

[56]  J. Tumlinson,et al.  Airborne signals prime plants against insect herbivore attack. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[57]  C. Midega,et al.  Impact of a Habitat Management System on Diversity and Abundance of Maize Stemborer Predators in Western Kenya , 2003 .

[58]  M. Dicke,et al.  beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[59]  D. G. James,et al.  Field Evaluation of Herbivore-Induced Plant Volatiles as Attractants for Beneficial Insects: Methyl Salicylate and the Green Lacewing, Chrysopa nigricornis , 2003, Journal of Chemical Ecology.

[60]  K. Hagen,et al.  Tryptophan in Artificial Honeydews as a Source of an Attractant for Adult Chrysopa carnea , 1976 .

[61]  C. Midega,et al.  Field boundaries of Panicum maximum as a reservoir for predators and a sink for Chilo partellus , 2007 .

[62]  M. Sabelis,et al.  UvA-DARE ( Digital Academic Repository ) Do anthocorid predators respond to synomones from Psylla-infested pear trees in field conditions ? , 2006 .

[63]  M. J. Rice,et al.  Large-Scale Field Trial to Test the Push Pull Strategy Against Heliothis spp in Cotton , 1988 .

[64]  G. Fry,et al.  Field margins: can they enhance natural enemy population densities and general arthropod diversity on farmland? , 1992 .

[65]  J. Napier,et al.  Plant volatiles yielding new ways to exploit plant defence , 2006 .

[66]  T. Baker,et al.  Olfactory Reactions of the Twelve-Spotted Lady Beetle, Coleomegilla maculata and the Green Lacewing, Chrysoperla carnea to Semiochemicals Released from Their Prey and Host Plant: Electroantennogram and Behavioral Responses , 2004, Journal of Chemical Ecology.

[67]  Anthony R. Ives,et al.  Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem , 2003 .

[68]  C. Pickett,et al.  Enhancing biological control: habitat management to promote natural enemies of agricultural pests. , 1998 .

[69]  M. Sabelis,et al.  Behavioural responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications , 1999 .

[70]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[71]  Beat Wermelinger,et al.  Ecology and management of the spruce bark beetle Ips typographus—a review of recent research , 2004 .

[72]  Kongming Wu,et al.  Field-Testing of Synthetic Herbivore-Induced Plant Volatiles as Attractants for Beneficial Insects , 2008, Environmental entomology.

[73]  James R. Miller,et al.  Stimulo-deterrent diversion: A concept and its possible application to onion maggot control , 1990, Journal of Chemical Ecology.

[74]  J. Kean,et al.  The population consequences of natural enemy enhancement, and implications for conservation biological control , 2008 .

[75]  J. Ton,et al.  Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. , 2006, Current opinion in plant biology.

[76]  M. Dicke,et al.  Impact of Botanical Pesticides Derived from Melia azedarach and Azadirachta indica Plants on the Emission of Volatiles that Attract Parasitoids of the Diamondback Moth to Cabbage Plants , 2006, Journal of Chemical Ecology.

[77]  T. C. Turlings,et al.  The Effects of Abiotic Factors on Induced Volatile Emissions in Corn Plants1 , 2002, Plant Physiology.

[78]  James H. Tumlinson,et al.  Plant Volatile Signals in Response to Herbivore Feeding , 1996 .

[79]  A. Aharoni,et al.  Genetic Engineering of Terpenoid Metabolism Attracts Bodyguards to Arabidopsis , 2005, Science.

[80]  W. J. Lewis,et al.  Semiochemicals for use with parasitoids: Status and future , 1990, Journal of Chemical Ecology.

[81]  K. Chamberlain,et al.  Plant signalling and induced defence in insect attack. , 2000, Molecular plant pathology.

[82]  J. van den Berg,et al.  Maize stemborer predator activity under ‘push – pull’ system and Bt-maize: A potential component in managing Bt resistance , 2006 .

[83]  W. Lewis,et al.  Exploitation of Herbivore-Induced Plant Odors by Host-Seeking Parasitic Wasps , 1990, Science.

[84]  W. J. Lewis,et al.  Semiochemicals, their role in pest control , 1981 .

[85]  T. C. Turlings,et al.  Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte) , 2001, CHEMOECOLOGY.

[86]  J. Takabayashi,et al.  Response of Predatory Insect Scolothrips takahashii Toward Herbivore-Induced Plant Volatiles Under Laboratory and Field Conditions , 1997, Journal of Chemical Ecology.

[87]  F. Pennacchio,et al.  Effect of Adult Experience on in-Flight Orientation to Plant and Plant–Host Complex Volatiles inAphidius erviHaliday (Hymenoptera, Braconidae) , 1997 .

[88]  T. Nishioka,et al.  Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. , 2000, Plant & cell physiology.

[89]  I. Baldwin,et al.  Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. , 2001, Plant physiology.

[90]  W. Boland,et al.  BIOSYNTHESIS OF C11 AND C16 HOMOTERPENES IN HIGHER PLANTS; STEREOCHEMISTRYOF THE C-C-BOND CLEAVAGE REACTION , 1999 .

[91]  I. Raskin,et al.  Airborne signalling by methyl salicylate in plant pathogen resistance , 1997, Nature.

[92]  Wopke van der Werf,et al.  Model evaluation of the function of prey in non-crop habitats for biological control by ladybeetles in agricultural landscapes , 2004 .

[93]  W. Lewis,et al.  Learning of Host-Finding Cues by Hymenopterous Parasitoids , 1993 .

[94]  D. G. James,et al.  Synthetic Herbivore-Induced Plant Volatiles as Field Attractants for Beneficial Insects , 2003 .