Open Access Open Access  Restricted Access Subscription Access

Weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae) headspace volatiles deter oviposition in female Oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae)


Affiliations
1 Division of Entomology and Nematology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
 

Natural predator–prey interactions in the insect world provide interesting insights into how female herbivores avoid ovipositing in places where a predator’s presence can be perceived. Several insects show such innate behavioural traits that can be harnessed to formulate safe pest management strategies in agriculture. Using customized oviposition assays, we studied the innate ovi­position avoidance behaviour of the oriental fruit fly, Bactrocera dorsalis, a frugivorous pest. Fruit flies preferred to lay eggs in a test region smeared with g-octa­lactone (an oviposition stimulant used as a positive control) over one smeared with a mix of g-octalactone and headspace volatiles of the weaver ant, Oecophylla smaragdina, a generalist predator in orchard ecosystems. A combination of the electrophysiologically active odour cues n-undecane and n-tridecane from the headspace volatiles of weaver ants was found to deter female fruit flies from ovipositing. Using these behaviour-modifying chemicals in a blend as a pre-harvest spray could potentially prevent egg-laying by the oriental fruit flies in ready-to-harvest fruits

Keywords

Fruit fly, headspace volatiles, oviposition deterrent, predator–prey interactions, weaver ant.
User
Notifications
Font Size

  • Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A. and McGregor, I. S., The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobe-hav. Rev., 2005, 29, 1123–1144.
  • Takahashi, L. K., Nakashima, B. R., Hong, H. and Watanabe, K., The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci. Biobehav. Rev., 2005, 29, 1157–1167.
  • Amo, L., Galván, I., Tomás, G. and Sanz, J. J., Predator odour recognition and avoidance in a songbird. Funct. Ecol., 2008, 22, 289–293.
  • Liu, Z. et al., Predator-secreted sulfolipids induce defensive res-ponses in C. elegans. Nature Commun., 2018, 9, 1–13.
  • Pears, J. B., Emberts, Z. and Bateman, P. W., The scent of danger: the impact of predator chemical cues on emergence from refuge and willingness to autotomize limbs in the house cricket (Acheta domesticus). J. Insect Behav., 2018, 31, 416–426.
  • Lopez-Ortega, M. and Williams, T., Natural enemy defense, provi-sioning and oviposition site selection as maternal strategies to en-hance offspring survival in a sub-social bug. PLoS ONE, 2018, 13.
  • Paul, S. C., Stevens, M., Burton, J., Pell, J. K., Birkett, M. A. and Blount, J. D., Invasive egg predators and food availability interacti-vely affect maternal investment in egg chemical defense. Front. Ecol. Evol., 2018, 6, 1–10.
  • Clarke, A. R. et al., Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu. Rev. Entomol., 2005, 50, 293–319.
  • Dohino, T. et al., Phytosanitary treatments against Bactrocera dor-salis (Diptera: Tephritidae): current situation and future prospects. J. Econ. Entomol., 2017, 110, 67–79.
  • Greene, E., Orsak, L. J. and Whitman, D. W., A tephritid fly mimics the territorial displays of its jumping spider predators. Science, 1987, 236, 310–312.
  • Mather, M. H. and Roitberg, B. D., A sheep in wolf’s clothing: tephritid flies mimic spider predators. Science, 1987, 236, 308–310.
  • Thomas, D. B., Predation on the soil inhabiting stages of the Mexi-can fruit fly. Southwest. Entomol., 1995, 20, 61–71.
  • Hendrichs, J., Katsoyannos, B. I., Wornoayporn, V. and Hendrichs, M. A., Odour-mediated foraging by yellowjacket wasps (Hymenop-tera: Vespidae): predation on leks of pheromone-calling Mediterra-nean fruit fly males (Diptera: Tephritidae). Oecologia, 1994, 99, 88–94.
  • Mäntylä, E., Kleier, S., Lindstedt, C., Kipper, S. and Hilker, M., In-sectivorous birds are attracted by plant traits induced by insect egg deposition. J. Chem. Ecol., 2018, 44, 1127–1138.
  • Thomas, D. B., Survivorship of the pupal stages of the Mexican fruit fly Anastrepha ludens (Loew) (Diptera: Tephritidae) in an agri-cultural and a nonagricultural situation. J. Entomol. Sci., 1993, 28, 350–362.
  • Eskafi, F. M. and Kolbe, M. M., Predation on larval and pupal Cer-atitis capitata (Diptera: Tephritidae) by the ant Solenopsis gemina-ta (Hymenoptera: Formicidae) and other predators in Guatemala. Environ. Entomol., 1990, 19, 148–153.
  • Wong, T. T. Y., McInnis, D. O., Nishimoto, J. I., Ota, A. K. and Chang, V. C. S., Predation of the Mediterranean fruit fly (Diptera: Tephritidae) by the Argentine ant (Hymenoptera: Formicidae) in Hawaii. J. Econ. Entomol., 1984, 77, 1454–1458.
  • Van Mele, P., Vayssières, J. F., Tellingen, E., and Vrolijks, J., Ef-fects of an African weaver ant, Oecophylla longinoda, in control-ling mango fruit flies (Diptera: Tephritidae) in Benin. J. Econ. Entomol., 2007, 100, 695–701.
  • Van Mele, P., Vayssieres, J. F., Adandonon, A. and Sinzogan, A., Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa. Physiol. Entomol., 2009. 34, 256–261.
  • Adandonon, A., Vayssières, J. F., Sinzogan, A. and Van Mele, P., Density of pheromone sources of the weaver ant Oecophylla longi-noda affects oviposition behaviour and damage by mango fruit flies (Diptera: Tephritidae). Int. J. Pest Manage., 2009, 55, 285–292.
  • Kamala Jayanthi, P. D., Woodcock, C. M., Caulfield, J., Birkett, M. A. and Bruce, T. J. A., Isolation and identification of host cues from mango, Mangifera indica, that attract gravid female oriental fruit fly, Bactrocera dorsalis. J. Chem. Ecol., 2012, 38, 361–369.
  • Pettersson, J., An aphid sex attractant. Insect Syst. Evol., 2010, 2, 6–93.
  • Kamala Jayanthi, P. D. et al., Specific volatile compounds from mango elicit oviposition in gravid Bactrocera dorsalis females. J. Chem. Ecol., 2014, 40, 259–266.
  • Shivaramu, S., Jayanthi, P. D. K., Kempraj, V., Anjinappa, R., Nandagopal, B. and Chakravarty, A. K., What signals do herbivore-induced plant volatiles provide conspecific herbivores? Arthro-pod – Plant Interact., 2017, 11, 815–823.
  • Skelton, A. C., Cameron, M. M., Pickett, J. A. and Birkett, M. A., Identification of neryl formate as the airborne aggregation phero-mone for the American house dust mite and the European house dust mite (Acari: Epidermoptidae). J. Med. Entomol., 2010, 47, 798–804.
  • Damodaram, K. J. P. et al., Centuries of domestication has not im-paired oviposition site-selection function in the silkmoth, Bombyx mori. Sci. Rep., 457 2014, 4, 1–6.
  • Weeks, E. N. I. et al., Electrophysiologically and behaviourally ac-tive semiochemicals identified from bed bug refuge substrate. Sci. Rep., 2020, 10, 1–14.
  • Mitra, A., Function of the Dufour’s gland in solitary and social Hymenoptera. J. Hymenopt. Res., 2013, 35, 33–58.
  • Attygalle, A. B. and Morgan, E. D., Chemicals from the glands of ants. R. Soc. Chem. London, 1984, 13, 245–278.
  • Regnier, F. E., Nieh, M. and Hölldobler, B., The volatile Dufour’s gland components of the harvester ants Pogonomyrmex rugosus and P. barbatus. J. Insect Physiol., 1973, 19, 981–992.
  • Brand, J. M. and Mpuru, S. P., Dufour’s gland and poison gland chemistry of the myrmicine ant, Messor capensis (Mayr). J. Chem. Ecol., 1993, 19, 1315–1321.
  • Fujiwara-Tsujii, N., Yamagata, N., Takeda, T., Mizunami, M. and Yamaoka, R., Behavioral responses to the alarm pheromone of the ant Camponotus obscuripes (Hymenoptera: Formicidae). Zool. Sci., 2006, 23, 353–358.
  • Hölldobler, B., Morgan, E. D., Oldham, N. J., Liebig, J. and Liu, Y., Dufour gland secretion in the harvester ant genus Pogonomyr-mex. Chemoecology, 2004, 14, 101–106.
  • Lenz, E. L., Krasnec, M. O. and Breed, M. D., Identification of un-decane as an alarm pheromone of the ant Formica argentea. J. In-sect Behav., 2013, 26, 101–108.
  • Mizunami, M., Yamagata, N. and Nishino, H., Alarm pheromone processing in the ant brain: an evolutionary perspective. Front. Be-hav. Neurosci., 2010, 4, 1–9.
  • Torres-Contreras, H., Olivares-Donoso, R. and Niemeyer, H. M., Solitary foraging in the ancestral South American ant, Pogo-nomyrmex vermiculatus. Is it due to constraints in the production or perception of trail pheromones? J. Chem. Ecol., 2007, 33, 435–440.
  • Welzel, K. F., Lee, S. H., Dossey, A. T., Chauhan, K. R. and Choe, D. H., Verification of Argentine ant defensive compounds and their behavioral effects on heterospecific competitors and conspecific nestmates. Sci. Rep., 2018, 8, 1–15.
  • Kempraj, V., Park, S. J., Cameron, D. and Taylor, P. W., Decoding an ancient biological control: the kairomonal basis of fruit fly re-pellence from weaver ants. Res. Square, 2022; https://doi.org/ 10.21203/rs.3.rs-1331132/v1.
  • Andriamaharavo, N. R., Retention data NIST Mass Spectrometry Data Center. Retrieved March, 2014, p. 2015.
  • Ansorena, D., Gimeno, O., Astiasaran, I. and Bello, J., Analysis of volatile compounds by GC–MS of a dry fermented sausage: Chori-zo de Pamplona. Food Res. Int., 2001, 34(1), 67–75.
  • Bailly, S., Jerkovic, V., Meuree, A., Timmermans, A. and Collin, S., Fate of key odorants in Sauternes wines through aging. J. Agric. Food Chem., 2009, 57(18), 8557–8563.
  • Bradshaw, J. W., Baker, R. and Howse, P. E., Chemical composi-tion of the poison apparatus secretions of the African weaver ant, Oecophylla longinoda, and their role in behaviour. Physiol. Ento-mol., 1979, 4(1), 39–46.
  • Deng, C., Li, N. and Zhang, X., Rapid determination of essential oil in Acorus tatarinowii Schott. by pressurized hot water extraction followed by solid-phase microextraction and gas chromatography–mass spectrometry. J. Chromatogr. A., 2004, 1059(1–2), 149–155.
  • Dzhemilev, U. M., Fakhretdinov, R. N. and Tolstikov, G. A., Linear dimerization of 1,3,6-octatriene and 2,6-dimethyl-1,3,6-octatriene in the presence of nickel complexes. Bull. Acad. Sci. USSR Div. Chem. Sci., 1977, 26, 840–841.
  • Gonçalves, E., Figueiredo, A. C., Barroso, J. G., Henriques, J., Sousa, E. and Bonifácio, L., Effect of monochamus galloprovin-cialis feeding on Pinus pinaster and Pinus pinea, oleoresin and in-sect volatiles. Phytochemistry, 2020, 169, 112159.
  • He, M., Yang, Z. Y., Guan, W. N., Vicente Gonçalves, C. M., Nie, J. and Wu, H., GC–MS analysis and volatile profile comparison for the characteristic smell from Liang-wai Gan Cao (Glycyrrhiza ura-lensis) and honey-roasting products. J. Chromatogr. Sci., 2016, 54(6), 879–887.
  • Höckelmann, C. and Jüttner, F., Volatile organic compound (VOC) analysis and sources of limonene, cyclohexanone and straight chain aldehydes in axenic cultures of Calothrix and Plectonema. Water Sci. Technol., 2004, 49(9), 47–54.
  • Joshi, A., Prakash, O., Pant, A. K., Kumar, R. and Negi, M. S., Chemical analysis and antioxidant activity of essential oils of two morphotypes of Lippia alba (Mill.) N.E. Br. ex Britton & P. Wilson (Verbenaceae). J. Essent. Oil-Bearing Plants, 2018, 21, 687–700.
  • Kempraj, V., Park, S. J., Faveri, S. and Taylor, P. W., Overlooked scents: chemical profile of soma, volatile emissions and trails of the green tree ant, Oecophylla smaragdina. Molecules, 2020, 25(9), 2112.
  • Kurashov, Y. A., Krylova, Y. V. and Mitrukova, G. G., Dynamics of essential oil composition in Potamogeton pusillus (Potamogeto-naceae) shoots during vegetation. Rastit. Resur., 2013, 49, 85–103.
  • Lalel, H. J., Singh, Z. and Tan, S. C., Glycosidically-bound aroma volatile compounds in the skin and pulp of ‘Kensington Pride’ mango fruit at different stages of maturity. Postharvest Biol. Technol., 2003, 29(2), 205–218.
  • Mohebat, R. and Bidoki, M. Z., Comparative chemical analysis of volatile compounds of Echinops ilicifolius using hydrodistillation and headspace solid-phase microextraction and the antibacterial ac-tivities of its essential oil. R. Soc. Open Sci., 2018, 5(2), 171424.
  • Pino, J. A., Mesa, J., Muñoz, Y., Martí, M. P. and Marbot, R., Vola-tile components from mango (Mangifera indica L.) cultivars. J. Agric. Food Chem., 2005, 53(6), 2213–2223.
  • Radulović, N. S., Đorđević, N. D. and Palić, R. M., Volatiles of Ple-urospermum austriacum (L.) Hoffm. (Apiaceae). J. Serbian Chem. Soc., 2010, 75, 1653–1660.
  • Saeed, T., Redant, G. and Sandra, P., Kovats indices of monoterpene hydrocarbons on glass capillary columns. J. High Resolut. Chroma-togr., 1979, 2, 75–76.
  • Sakai, T., Maarse, H., Kepner, R. E., Jennings, W. G. and Long-hurst, W. M., Volatile components of Douglas fir needles. J. Agric. Food Chem., 1967, 15(6), 1070–1072.
  • Shivashankar, S., Roy, T. and Krishna, P., Headspace solid phase micro extraction and GC/MS analysis of the volatile components in seed and cake of Azaridachta indica A. juss. Chem. Bull. Politech. Univ. Timisoara, 2012, 57, 1–6.

Abstract Views: 162

PDF Views: 82




  • Weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae) headspace volatiles deter oviposition in female Oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae)

Abstract Views: 162  |  PDF Views: 82

Authors

P. D. Kamala Jayanthi
Division of Entomology and Nematology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
P. Saravan Kumar
Division of Entomology and Nematology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India
Meenal Vyas
Division of Entomology and Nematology, ICAR-Indian Institute of Horticultural Research, Bengaluru 560 089, India

Abstract


Natural predator–prey interactions in the insect world provide interesting insights into how female herbivores avoid ovipositing in places where a predator’s presence can be perceived. Several insects show such innate behavioural traits that can be harnessed to formulate safe pest management strategies in agriculture. Using customized oviposition assays, we studied the innate ovi­position avoidance behaviour of the oriental fruit fly, Bactrocera dorsalis, a frugivorous pest. Fruit flies preferred to lay eggs in a test region smeared with g-octa­lactone (an oviposition stimulant used as a positive control) over one smeared with a mix of g-octalactone and headspace volatiles of the weaver ant, Oecophylla smaragdina, a generalist predator in orchard ecosystems. A combination of the electrophysiologically active odour cues n-undecane and n-tridecane from the headspace volatiles of weaver ants was found to deter female fruit flies from ovipositing. Using these behaviour-modifying chemicals in a blend as a pre-harvest spray could potentially prevent egg-laying by the oriental fruit flies in ready-to-harvest fruits

Keywords


Fruit fly, headspace volatiles, oviposition deterrent, predator–prey interactions, weaver ant.

References





DOI: https://doi.org/10.18520/cs%2Fv123%2Fi5%2F694-702