Open Access Open Access  Restricted Access Subscription Access

Volatile Cues from Corcyra cephalonica Larva Elicit Behavioural Responses in Parasitoid, Habrobracon hebetor


Affiliations
1 Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
2 Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
 

The rice moth, Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae), is a serious pest of grains in storage systems resulting in immense losses but is also widely used as a factitious host for mass rearing of many important natural enemies of crop pests. Given the role of kairomones, the aim of this study was to isolate and identify potential cues from the larval body wash of C. cephalonica, which could attract its gregarious ecto-parasitoid, Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Gas chromatography with electroantennography (GC-EAG) and olfactory assays were used to demonstrate the attraction of female H. hebetor to different larval body volatiles. A total of 15 EAG-active compounds were discovered in the body wash of C. cephalonica larvae that triggered a response in female H. hebetor. Among them, four compounds (p-xylene, naphthalene, n-eicosane and n-tricosane) were bioassayed for the behavioural response of parasitoids and found that n-eicosane significantly attracted a higher number of parasitoids than others. Our work establishes the attraction of H. hebetor to volatile kairomone cues emanating from the factitious host larval body, which offers an opportunity for its parasitoid, H. hebetor to improve the mass rearing efficiency

Keywords

Behavioural Assays, GC-EAG, GC-MS, Larval Volatiles, Olfactometer.
User
Notifications
Font Size

  • Hagstrum, D. and Subramanyam, B., Fundamentals of Stored-Product Entomology, St Paul. Woodhead Publishing and AACC International Press, 2006.
  • Anukiruthika, T., Jian, F. and Jayas, D. S., Movement and behavioral response of stored product insects under stored grain environments-A review. J. Stored Prod. Res., 2021, 90, 101752; https://doi.org/10.1016/j.jspr.2020.101752.
  • Coelho, M. B., Marangoni, S. and Macedo, M. L. R., Insecticidal action of Annona coriacea lectin against the flour moth Anagasta kuehniella and the rice moth Corcyra cephalonica (Lepidoptera: Pyralidae). Comp. Biochem. Physiol. Part C, 2007, 146(3), 406–414; https://doi.org/10.1016/j.cbpc.2007.05.001.
  • Rani, A., Chand, S., Thakur, N. and Nath, A. K., Alpha-amylase inhibitor from local common bean selection: effect on growth and development of Corcyra cephalonica. J. Stored Prod. Res., 2018, 75, 35–37; https://doi.org/10.1016/j.jspr.2017.10.009.
  • Allotey, J. and Azalekor, W., Some aspects of the biology and control using botanicals of the rice moth, Corcyra cephalonica (Stainton), on some pulses. J. Stored Prod. Res., 2000, 36(3), 235–243; https://doi.org/10.1016/S0022-474X(99)00045-4.
  • Gowda, G. B. et al., Insecticide-induced hormesis in a factitious host, Corcyra cephalonica, stimulates the development of its gregarious ecto-parasitoid, Habrobracon hebetor. Biol. Control, 2021, 160, 104680; https://doi.org/10.1016/j.biocontrol.2021.104680.
  • Hashem, M. Y., Ahmed, A. A., Ahmed, S. S., Mahmoud, Y. A. and Khalil, S. S., Impact of modified atmospheres on respiration of last instar larvae of the rice moth, Corcyra cephalonica (Lepidoptera: Pyralidae). Arch. Phytopathol. Plant Prot., 2018, 51(19–20), 1090–1105; https://doi.org/10.1080/03235408.2018.1560022.
  • Osman, N. (ed.), Assessment of damage by the rice moth Corcyra cephalonica (St.) on different grains at four levels of moisture content. In Proceedings of 7th ASEAN Tech Seminar on Grain Post Harvest Technology, 1984.
  • Champ, B. and Dyte, C., FAO global survey of pesticide susceptibility of stored grain pests. FAO Plant Prot. Bull., 1977, 25(2), 49–67.
  • Adarkwah, C. et al., Effectiveness of the egg parasitoid Trichogramma evanescens preventing rice moth from infesting stored bagged commodities. J. Stored Prod. Res., 2015, 61, 102–107; https://doi.org/10.1016/j.jspr.2015.01.002.
  • Adarkwah, C., Obeng‐Ofori, D., Opuni‐Frimpong, E., Ulrichs, C. and Schöller, M., Predator–parasitoid–host interaction: biological control of Rhyzopertha dominica and Sitophilus oryzae by a combination of Xylocoris flavipes and Theocolax elegans in stored cereals. Entomol. Exp. Appl., 2019, 167(2), 118–128; https://doi.org/10.1111/eea.12760.
  • Stejskal, V., Kosina, P. and Kanyomeka, L., Arthropod pests and their natural enemies in stored crops in northern Namibia. J. Pest Sci., 2006, 79(1), 51–55; https://doi.org/10.1007/s10340-005-0109-2.
  • Vincent, A., Singh, D. and Mathew, I. L., Corcyra cephalonica: a serious pest of stored products or a factitious host of biocontrol agents? J. Stored Prod. Res., 2021, 1(94), 101876.
  • Akinkurolere, R., Boyer, S., Chen, H. and Zhang, H., Parasitism and host-location preference in Habrobracon hebetor (Hymenoptera: Braconidae): role of refuge, choice and host instar. J. Econ. Entomol., 2009, 102(2), 610–615; https://doi.org/10.1603/029.102.0219.
  • Mbata, G. N., Eason, J., Payton, M. and Davis, M., Putative host volatiles used by Habrobracon hebetor (Hymenoptera: Braconidae) to locate larvae of Plodia interpunctella (Lepidoptera: Pyralidae). J. Insect Behav., 2017, 30(3), 287–299; https://doi.org/10.1007/s10905-017-9619-z.
  • Ghimire, M. N. and Phillips, T. W., Mass rearing of Habrobracon hebetor Say (Hymenoptera: Braconidae) on larvae of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae): effects of host density, parasitoid density, and rearing containers. J. Stored Prod. Res., 2010, 46(4), 214–220; https://doi.org/10.1016/j.jspr.2010.05.003.
  • Antolin, M. F., Ode, P. J. and Strand, M. R., Variable sex ratios and ovicide in an outbreeding parasitic wasp. Anim. Behav., 1995, 49(3), 589–600; https://doi.org/10.1016/0003-3472(95)80192-8.
  • Cox, P., Potential for using semiochemicals to protect stored products from insect infestation. J. Stored Prod. Res., 2004, 40(1), 1–25; https://doi.org/10.1016/S0022-474X(02)00078-4.
  • Sharma, A., Sandhi, R. K. and Reddy, G. V., A review of interactions between insect biological control agents and semiochemicals. Insects, 2019, 10(12), 439; https://doi.org/10.3390/insects10120439.
  • Lockey, K. and Metcalfe, N., Cuticular hydrocarbons of adult Himatismus species and a comparison with 21 other species of adult Tenebrionid beetle using multivariate analysis. Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol., 1988, 91(2), 371–382; https://doi.org/10.1016/0305-0491(88)90156-3.
  • Tumlinson, J. H., Lewis, W. J. and Vet, L. E., How parasitic wasps find their hosts. Sci. Am., 1993, 268(3), 100–106; https://www.jstor.org/stable/24941408.
  • Darwish, E., El-Shazly, M. and El-Sherif, H., The choice of probing sites by Bracon hebetor Say (Hymenoptera: Braconidae) foraging for Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). J. Stored Prod. Res., 2003, 39(3), 265–276; https://doi.org/10.1016/S0022-474X(02)00078-4.
  • Lewis, W., Jones, R. L., Nordlund, D. A. and Gross, H., Kairomones and their use for management of entomophagous insects: II. mechanisms causing increase in rate of parasitization by Trichogramma spp. J. Chem. Ecol., 1975, 1(3), 349–360.
  • Tilden, R. and Ferkovich, S., Kairomonal stimulation of oviposition into an artificial substrate by the endoparasitoid Microplitis croceipes (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am., 1988, 81(1), 152–156; https://doi.org/10.1093/aesa/81.1.152.
  • Lalitha, Y. and Ballal, C. R., Influence of seasons and inoculum dosages on the production efficiency of Corcyra cephalonica Stainton. J. Biol. Control, 2015, 29(1), 25–30.
  • Chaudhuri, N. and Senapati, S., Development and reproductive performance of rice moth Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) in different rearing media. J. Saudi. Soc. Agric. Sci., 2017, 16(4), 337–343; https://doi.org/10.1016/j.jssas.2015.11.004.
  • Gadratagi, B. G. et al., Performance of Trichogramma japonicum under field conditions as a function of the factitious host species used for mass rearing. PLoS ONE, 2021, 16(8), e0256246; https://doi.org/10.1371/journal.pone.0256246.
  • Hagstrum, D. W. and Smittle, B. J., Host-finding ability of Bracon hebetor and its influence upon adult parasite survival and fecundity. Environ. Entomol., 1977, 6(3), 437–439; https://doi.org/10.1093/ee/6.3.437.
  • Basana Gowda, G. et al., Insecticide-induced hormesis in a factitious host, Corcyra cephalonica, stimulates the development of its gregarious ecto-parasitoid, Habrobracon hebetor. Biol. Control, 2021, 160, 104680; https://doi.org/10.1016/j.biocontrol.2021.104680.
  • Venugopal, U., Jayanthi, P. D. K., Kumar, P., Jagadeesh, K. and Mohan, K. M., Host larval body odours AID host location of Apanteles machaeralis, a braconid larval endoparasitoid of cucumber moth Diaphania Indica. Indian J. Entomol., 2021, 83(3), 315–320; http://dx.doi.org/10.5958/0974-8172.2021.00107.3.
  • Subramani, V. et al., Volatile chemical signals underlying the host plant preferences of Tuta absoluta. Entomol. Exp. Appl., 2021, 169(11), 997–1007; https://doi.org/10.1111/eea.13099.
  • Das, S., Koner, A. and Barik, A., A beetle biocontrol agent of rice-field weeds recognizes its host plants by surface wax long-chain alkanes and free fatty acids. Chemoecology, 2019, 29(4), 155–170; https://doi.org/10.1007/s00049-019-00285-1.
  • Mitra, S., Sarkar, N. and Barik, A., Long-chain alkanes and fatty acids from Ludwigia octovalvis weed leaf surface waxes as shortrange attractant and ovipositional stimulant to Altica cyanea (Weber) (Coleoptera: Chrysomelidae). Bull. Entomol. Res., 2017, 107(3), 391–400; https://doi.org/10.1017/S0007485316001012.
  • Kamala Jayanthi, P. D. et al., Specific volatile compounds from mango elicit oviposition in gravid Bactrocera dorsalis females. J. Chem. Ecol., 2014, 40(3), 259–266; https://doi.org/10.1007/s10886-014-0403-7.
  • Bertschy, C., Turlings, T. C. J., Bellotti, A. C. and Dorn, S., Chemically-mediated attraction of three parasitoid species to mealybug-infested cassava leaves. Fla. Entomol., 1997, 80(3), 1–14.
  • Murali-Baskaran, R. K. et al., Role of kairomone in biological control of crop pests – a review. Physiol. Mol. Plant Pathol., 2018, 101, 3–15; https://doi.org/10.1016/j.pmpp.2017.07.004.
  • Rani, P. U., Sambangi, P. and Sandhyarani, K., Impact of plant phenolics as semiochemicals on the performance of Trichogramma chilonis Ishii. J. Insect Behav., 2017, 30(1), 16–31; https://doi.org/10.1007/s10905-016-9595-8.
  • Dweck, H. K., Svensson, G. P., Gündüz, E. A. and Anderbrant, O., Kairomonal response of the parasitoid, Bracon hebetor Say, to the male-produced sex pheromone of its host, the greater waxmoth, Galleria mellonella (L.). J. Chem. Ecol., 2010, 36(2), 171–178; https://doi.org/10.1007/s10886-010-9746-x.
  • Ram, A., Tiwari, L. D., Dass, R. and Mehrotra, K. N., Evidence for the presence of a kairomone in Corcyra cephalonica Staint. larvae for Bracon brevicornis Wesm. (Hymen., Braconidae). J. Appl. Entomol., 1982, 93(1–5), 338–341.
  • Strand, M. R., Williams, H. J., Vinson, S. B. and Mudd, A., Kairomonal activities of 2-acylcyclohexane-1,3 diones produced by Ephestia kuehniella Zeller in eliciting searching behavior by the parasitoid Bracon hebetor (Say). J. Chem. Ecol., 1989, 15, 1491–1500.
  • Shonouda, M. L. and Nasr, F. N., Impact of larval‐extract (kairomone) of Ephestia kuehniella Zell. (Lep., Pyralidae), on the behaviour of the parasitoid Bracon hebetor Say. (Hym., Braconidae). J. Appl. Entomol., 1998, 122(1–5), 33–35.
  • Zhu, G. et al., Chemical investigations of volatile kairomones produced by Hyphantria cunea (Drury), a host of the parasitoid Chouioia cunea Yang. Bull. Entomol. Res., 2017, 107(2), 234–240; https://doi.org/10.1017/S0007485316000833.
  • Mohanasundaram, A. et al., Electroantennography and behavioral studies of Eublemma amabilis [Moore] and Pseudohypatopa pulverea [Meyr] in relation to volatiles of lac insect (Kerria lacca Kerr.) and its associated products. Int. J. Trop. Insect Sci., 2022, 42(3), 2313–2324; https://doi.org/10.1007/s42690-022-00754-1.
  • Paul, A., Madhu, S. and Singh, D. B., Kairomonal effects of different host body washings on parasitism by Trichogramma brasiliensis and T. japonicum. Int. J. Trop. Insect Sci., 1997, 17(3–4), 373–377; https://doi.org/10.1017/S1742758400019214.
  • Trang, T. T. and Dey, D., Electroantennogram responses of Chelonus blackburni Cameron, egg-larval parasitoid of spotted boll worm Earias vitella to infochemicals on cotton ecosystem. Omonrice, 2013, 19, 118–130.
  • Xiu, C.-L. et al., Perception of and behavioral responses to host plant volatiles for three Adelphocoris species. J. Chem. Ecol., 2019, 45(9), 779–788; https://doi.org/10.1007/s10886-019-01102-3.
  • Li, M., Xia, S., Zhang, T., Williams III, L., Xiao, H. and Lu, Y., Volatiles from cotton plants infested by Agrotis segetum (Lep.: Noctuidae) attract the larval parasitoid Microplitis mediator (Hym.: Braconidae). Plants, 2022, 11(7), 863; https://doi.org/10.3390/plants11070863.
  • Chi, D., Li, X., Yu, J., Xie, X. and Wang, G., The EAG response and behavior of the Saperda populnea L. to volatiles from poplar branches. Acta Ecol. Sin., 2011, 31(6), 334–340; https://doi.org/10.1016/j.chnaes.2011.09.003.
  • Guleria, N., Nebapure, S. M., Jayanthi, P. K., Suby, S. and Kumar, P. S., Identification of male-specific active host plant volatiles for maize stem borer, Chilo partellus Swinhoe. Curr. Sci., 2021, 121(4), 578.
  • Barth, R., Bau und Funktion der Flugel drusen einiger Mikrolepidopteren. Untersuhungen an den Pyraliden: Aphomia gularis, Galleria mellonella, Plodia interpunctella, Ephestia elutella und E. kuehniella. Z. Wiss Zool., 1937, 150, 1–37.
  • Roller, H., Bieman, K., Bjerke, J. S., Norgard, D. W. and Mcshan, W. H., Sex pheromone of pyralid moth. I. Isolation and identification of the sex-attractant of Galleria mellonella L. (Greater wax moth). Acta Entomol. Bohemoslo., 1968, 65, 208–211.
  • Dweck, H. K., Svensson, G. P., Gündüz, E. A. and Anderbrant, O., Kairomonal response of the parasitoid, Bracon hebetor Say, to the male-produced sex pheromone of its host, the greater waxmoth, Galleria mellonella (L.). J. Chem. Ecol., 2010, 36, 171–178.
  • Silberbush, A., Tsurim, I., Margalith, Y. and Blaustein, L., Interactive effects of salinity and a predator on mosquito oviposition and larval performance. Oecologia, 2014, 175(2), 565–575; https://doi.org/10.1007/s00442-014-2930-x.
  • Nakashima, Y., Birkett, M. A., Pye, B. J., Pickett, J. A. and Powell, W., The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J. Chem. Ecol., 2004, 30(6), 1103–1116; https://doi.org/10.1023/B:JOEC.0000030266.81665.19.
  • Parthiban, P., Chinniah, C., Kalyanasundarm, M. and Baskaran, R., Kairomonal effect of acetone extracts of groundnut on foraging activities of Trichogramma chilonis (Ishii) and Chrysoperla zastrowi sillemi (Esben-Peterson). Legume Res., 2017, 40(2), 393–396; http://10.0.73.117/lr.v0iOF.11191.
  • Nakashima, Y., Birkett, M. A., Pye, B. J. and Powell, W., Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. J. Chem. Ecol., 2006, 32(9), 1989–1998; https://doi.org/10.1007/s10886-006-9123-y.
  • Hung, K. Y., McElfresh, J. S., Zou, Y., Wayadande, A. and Gerry, A. C., Identification of volatiles from plants infested with honeydew-producing insects, and attraction of house flies (Diptera: Muscidae) to these volatiles. J. Med. Entomol., 2020, 57(3), 667–676; https://doi.org/10.1093/jme/tjz232.
  • Yasukawa, S., Kato, H., Yamaoka, R., Tanaka, H., Arai, H. and Kawano, S., Reproductive and pollination biology of Magnolia and its allied genera (Magnoliaceae): I. Floral volatiles of several Magnolia and Michelia species and their roles in attracting insects. Plant Spec. Biol., 1992, 7, 121.
  • Sarkar, N., Mukherjee, A. and Barik, A., Long-chain alkanes: allelochemicals for host location by the insect pest, Epilachna dodecastigma (Coleoptera: Coccinellidae). Appl. Entomol. Zool., 2013, 48(2), 171–179; https://doi.org/10.1007/s13355-013-0168-4.
  • Schoonhoven, L. M., Van Loon, J. J. and Dicke, M., Insect-Plant Biology, Oxford University Press on Demand, 2005.
  • Giunti, G. et al., Parasitoid learning: current knowledge and implications for biological control. Biol. Control, 2015, 90, 208–219; https://doi.org/10.1016/j.biocontrol.2015.06.007.
  • Kruidhof, H. M., Kostenko, O., Smid, H. M. and Vet, L. E., Integrating parasitoid olfactory conditioning in augmentative biological control: potential impact, possibilities, and challenges. Front Ecol. Evol., 2019, 7, 84; https://doi.org/10.3389/fevo.2019.00084.
  • Ayelo, P. M., Pirk, C. W., Yusuf, A. A., Chailleux, A., Mohamed, S. A. and Deletre, E., Exploring the kairomone-based foraging behaviour of natural enemies to enhance biological control: a review. Front. Ecol. Evol., 2021, 9, 641974; https://doi.org/10.3389/fevo. 2021.641974.
  • Randlkofer, B., Obermaier, E., Hilker, M. and Meiners, T., Vegetation complexity – the influence of plant species diversity and plant structures on plant chemical complexity and arthropods. Basic Appl. Ecol., 2010, 11(5), 383–395; https://doi.org/10.1016/j.baae. 2010.03.003.
  • Rodriguez-Saona, C. R. and Stelinski, L. L., Behavior-modifying strategies in IPM: theory and practice. In Integrated pest management: Innovation-Development Process, Springer, Berlin, Germany, 2009, pp. 263–315.

Abstract Views: 300

PDF Views: 167




  • Volatile Cues from Corcyra cephalonica Larva Elicit Behavioural Responses in Parasitoid, Habrobracon hebetor

Abstract Views: 300  |  PDF Views: 167

Authors

G. Basana Gowda
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
Totan Adak
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
P. D. Kamala Jayanthi
Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
P. Saravan Kumar
Division of Crop Protection, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
G. GuruPirasanna-Pandi
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
Naveenkumar B. Patil
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
A. Annamalai
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India
P. C. Rath
Division of Crop Protection, ICAR-National Rice Research Institute, Cuttack 753 006, India

Abstract


The rice moth, Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae), is a serious pest of grains in storage systems resulting in immense losses but is also widely used as a factitious host for mass rearing of many important natural enemies of crop pests. Given the role of kairomones, the aim of this study was to isolate and identify potential cues from the larval body wash of C. cephalonica, which could attract its gregarious ecto-parasitoid, Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Gas chromatography with electroantennography (GC-EAG) and olfactory assays were used to demonstrate the attraction of female H. hebetor to different larval body volatiles. A total of 15 EAG-active compounds were discovered in the body wash of C. cephalonica larvae that triggered a response in female H. hebetor. Among them, four compounds (p-xylene, naphthalene, n-eicosane and n-tricosane) were bioassayed for the behavioural response of parasitoids and found that n-eicosane significantly attracted a higher number of parasitoids than others. Our work establishes the attraction of H. hebetor to volatile kairomone cues emanating from the factitious host larval body, which offers an opportunity for its parasitoid, H. hebetor to improve the mass rearing efficiency

Keywords


Behavioural Assays, GC-EAG, GC-MS, Larval Volatiles, Olfactometer.

References





DOI: https://doi.org/10.18520/cs%2Fv125%2Fi2%2F183-190