Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-28T18:23:15.198Z Has data issue: false hasContentIssue false

Temperature-dependent development of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) and its larval parasitoid, Habrobracon hebetor (Say) (Hymenoptera: Braconidae): implications for species interactions

Published online by Cambridge University Press:  24 August 2017

M. Noor-ul-Ane*
Affiliation:
Institute of Pure and Applied Biology (Zoology Division), Bahauddin Zakariya University (BZU), Multan, Punjab, Pakistan
M. Ali Mirhosseini
Affiliation:
Department of Entomology, College of Agriculture, Tarbiat Modares University, Tehran, Iran
N. Crickmore
Affiliation:
School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK
S. Saeed
Affiliation:
Department of Entomology, Muhammad Nawaz Shareef University of Agriculture, Multan, Punjab, Pakistan
I. Noor
Affiliation:
Department of Statistics, Bahauddin Zakariya University (BZU), Multan, Punjab, Pakistan
M.P. Zalucki
Affiliation:
School of Biological Sciences, The University of Queensland, 4072, Australia
*
*Author for correspondence: Tel: +92-61-9210071-74 Ext. 2504 Fax: +92-61-9210098 E-mail: [email protected]

Abstract

Habrobracon hebetor (Say) is a parasitoid of various Lepidoptera including Helicoverpa armigera (Hübner), a key pest of different crops and vegetables. The development of both H. armigera and H. hebetor were simultaneously evaluated against a wide range of constant temperatures (10, 15, 17.5, 20, 25, 27.5, 30, 35, 37.5 and 40 °C). Helicoverpa armigera completed its development from egg to adult within a temperature range of 17.5–37.5 °C and H. hebetor completed its life cycle from egg to adult within a temperature range of 15–40 °C. Based on the Ikemoto and Takai model the developmental threshold (To) and thermal constant (K) to complete the immature stages, of H. armigera were calculated as 11.6 °C and 513.6 DD, respectively, and 13 °C and 148 DD, respectively, for H. hebetor. Analytis/Briere-2 and Analytis/Briere-1 were adjudged the best non-linear models for prediction of phenology of H. armigera and H. hebetor, respectively and enabled estimation of the optimum (Topt) and maximum temperature (Tmax) for development with values of 34.8, 38.7, 36.3, and 43 °C for host and the parasitoid, respectively. Parasitisation by H. hebetor was maximal at 25 °C but occurred even at 40 °C. This study suggests although high temperature is limiting to insects, our estimates of the upper thermal limits for both species are higher than previously estimated. Some biological control of H. armigera by H. hebetor may persist in tropical areas, even with increasing temperatures due to climate change.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, M., Arif, M.I. & Ahmad, Z. (1995) Monitoring insecticide resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) in Pakistan. Journal of Economic Entomology 88, 771776.Google Scholar
Ahmad, M.S.H., Al-Maliky, S.K., Al-Taweel, A.A., Jabo, N.F. & Al-Hakkak, Z.S. (1985) Effects of three temperature regimes on rearing and biological activities of Bracon hebetor (Say) (Hymenoptera: Braconidae). Journal of Stored Products Research 2, 6568.Google Scholar
Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716723.Google Scholar
Ashfaq, M., Khan, R.R. & Farooq, M.A. (2011) Refinement of rearing technique of a potent larval parasitiod Bracon hebetor (Say), (Braconidae: Hymenoptera). Proceedings of the Pakistan Academy of Science 48, 8388.Google Scholar
Bahar, M.H., Soroka, J.J., Grenkow, L. & Dosdall, L.M. (2014) New threshold temperatures for the development of a North American Diamondback Moth (Lepidoptera: Plutellidae) population and its larval parasitoid, Diadegma insulare (Hymenoptera: Ichneumonidae). Environmental Entomology 43, 14431452.Google Scholar
Bartekova, A. & Praslicka, J. (2006) The effect of ambient temperature on the development of Cotton Bollworm (Helicoverpa armigera Hübner, 1808). Plant Protection Science 42, 135138.Google Scholar
Bashi, S.U. & Tunc, I. (2008) Development, survival and reproduction of Orius niger (Hemiptera: Anthocoridae) under different photoperiod and temperature regimes. Biocontrol Science and Technology 18, 767778.Google Scholar
Brower, J.H. & Press, J.W. (1990) Interaction of Bracon hebetor (Say) (Hymenoptera: Brachoidae) and Trichogramma pretiosum (Hymenoptera; Trichogrammatidae) in suppressing stored-product moth populations in small in shell peanut storages. Journal of Economic Entomology 83, 10961101.Google Scholar
Campbell, A., Frazer, B.D., Gilbert, N., Gutierrez, A.P. & Mackauer, M. (1974) Temperature requirements of some aphids and their parasites. Journal of Applied Ecology 11, 431438.Google Scholar
Chen, H., Zhang, H., Zhu, K.Y. & James, C. (2013) Performance of diapausing parasitoid wasps, Habrobracon hebetor, after cold storage. Biological Control 64, 186194.Google Scholar
Damos, P. & Savopoulou-Soultani, M. (2011) Temperature-driven models for insect development and vital thermal requirements. Psyche 12, 113.Google Scholar
Dhillon, M.K. & Sharma, H.C. (2009) Temperature influences the performance and effectiveness of field and laboratory strains of the ichneumonid parasitoid, Ampoletis chlorideae. Biological Control 54, 743750.Google Scholar
Dixon, A.F.G. (2006) Insect predator–prey dynamics. Ladybird beetles and biological control. Journal of Insect Conservation 10, 375376.Google Scholar
Downes, S., Kriticos, D., Parry, H., Paull, C., Schellhorn, N. & Zalucki, M.P. (2016) A perspective on management of Helicoverpa armigera: transgenic Bt cotton, IPM, and landscapes. Pest Management Sciences 73, 485492. doi: 10.1002/ps.4461.Google Scholar
Engroff, B.W. & Watson, T.F. (1975) Influence of temperature on adult biology and population growth of Bracon kirkpatricki. Annal of the Entomological Society of America 68, 11211125.Google Scholar
Foley, D.H. (1981) Pupal development rate of Heliothis armigera (Hübner) (Lepidoptera: Noctuidae) under constant and fluctuating temperatures. Journal of the Australian Entomological Society 20, 1320.Google Scholar
Forouzan, M., Amirmaafi, M. & Sahragard, A. (2008) Temperature-dependent development of Habrobracon hebetor (Hym.: Braconidae) reared on larvae of Galleria mellonella (Lep.: Pyralidae). Journal of Entomological Society of Iran 28, 6778.Google Scholar
Furlong, M.J. & Zalucki, M.P. (2017) Climate change and biological control: the consequences of increasing temperatures on host–parasitoid interactions. Current Opinion in Insect Science 20, 3944. http://dx.doi.org/10.1016/j.cois.2017.03.006.Google Scholar
Furlong, M.J., Zalucki, M.P., Shabir, A. & Adamson, D.C. (2016) Biological control of diamondback moth in a climate of change. In Proceedings of 7th Workshop on the Management of DBM and other Crucifer Pests March 2326. 2015 Organized by University of Agricultural Sciences, Bangalore, India.Google Scholar
Golizadeh, A., Kamali, K., Fathipour, Y. & Abbasipour, H. (2008) Life table and temperature-dependent development of Diadegma anurum (Hymenoptera: Ichneumonidae) on its host Plutella xylostella (Lepidoptera: Plutellidae). Environmental Entomology 37, 3844.Google Scholar
Hance, T., van Baaren, J., Vernon, P. & Boivin, G. (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107126.Google Scholar
Ikemoto, T. & Takai, K. (2000) A new linearized formula for the law of total effective temperature and the evaluation of line-ftting methods with both variables subject to error. Environmental Entomology 29, 671682.Google Scholar
Imam, M., Uwais, A., Namat, U., Akbar, A. & Ahmat, T. (2007) Influence of Habrobracon hebetor on H. armigera armigera in southern Xinjiang. Natural Enemies of Insect 29, 1215.Google Scholar
Jallow, M.F.A. & Matsumura, M. (2001) Influence of temperature on the rate of development of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Applied Entomology and Zoology 36, 427430.Google Scholar
Kay, I.R. (1981) The effect of constant temperatures on the development time of eggs of Heliothis armiger (Hübner) (Lepidoptera: Noctuidae). Journal of the Australian Entomological Society 20, 155156.Google Scholar
Khan, R.R., Ashfaq, M., Ahmed, S. & Sahi, S.T. (2011) Mortality responses in Bracon hebetor (say) (Braconidae: Hymenoptera) against some new chemistry and conventional insecticides under laboratory conditions. Pakistan Journal of Agriculture and Science 46, 3033.Google Scholar
Kriticos, D.J., Ota, N., Hutchison, W.D., Beddow, J., Walsh, T., Tay, W.T., Paula-Moreas, S.V., Czepak, C. & Zalucki, M.P. (2015) The potential distribution of invading Helicoverpa armigera in North America: is It just a matter of time? PLoS ONE, 10, e0119618. doi: 10.1371/journal.pone.0119618.Google Scholar
Logan, J.D., Wolesensky, W. & Joern, A. (2006) Temperature-dependent phenology and predation in arthropod systems. Ecological Modelling 196, 471482.Google Scholar
Malina, R. & Praslicka, J. (2008) Effect of temperature on the developmental rate, longevity and parasitism of Aphidiu servi Haliday (Hymenoptera: Aphidiidae). Plant Protection Science 44, 1924.Google Scholar
Messenger, P.S. & Bosch, R. (1971) The adaptability of introduced biological control agents. pp. 6892 in Huffaker, C.B. (Ed.) Biological Control. New York, USA, Plenum Press.Google Scholar
Mironidis, G.K. & Savopoulou-Soultani, M. (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environmental Entomology 37, 1628.Google Scholar
Nikam, P.K. & Pawar, C.V. (1993) Life tables and intrinsic rate of increase of Bracon hebetor Say (Hym., Braconidae) population on Corcyra cephalonica Staint. (Lep., Pyralidae), a key parasitoid of Helicoverpa armigera (Hb.) (Lep., Noctuidae). Journal of Applied Entomology 115, 210213.Google Scholar
Obrycki, J.J. & Kring, T.J. (1998) Predaceous Coccinellidae in biological control. Annual Review of Entomology 43, 295321.Google Scholar
Ode, P.J., Antolin, M.F. & Storand, M.R. (1996) Sex allocation and sexual asymmetries in intrabrood competition in the parasitic wasp Bracon hebetor. Journal of Animal Ecology, 65, 690700.Google Scholar
Perdikis, D.C. & Lykouressis, D.P. (2002) Thermal requirements of the polyphagous predator Macrolophus pygmaeus (Hemiptera: Miridae). Environmental Entomology 31, 661667.Google Scholar
Powell, J.A. & Logan, J.A. (2005) Insect seasonality: circle map analysis of temperature driven life cycles. Theoretical Population Biology 67, 161179.Google Scholar
Room, P.M. (1983) Calculations of temperature-driven development by Heliothis species (Lepidoptera: Noctuidae) in the Namoi Valley, New South Wales. Journal of Australian Entomological Society 22, 211215.Google Scholar
Saxena, H., Ponnusamy, D. & Iquebal, M.A. (2012) Seasonal parasitism and biological characteristics of Habrobracon hebetor (Hymenoptera: Braconidae), a potential larval ectoparasitoid of Helicoverpa armigera (Lepidoptera: Noctuidae) in a chickpea ecosystem. Biocontrol Science and Technology 22, 305318.Google Scholar
Shi, P., Ge, F., Sun, Y. & Chen, C. (2011) A simple model for describing the effect of temperature on insect developmental rate. Journal of Asia Pacific Entomology 14, 1520.Google Scholar
Sinha, S. & Sanyal, S. (2013) Acclimatization to heat stress in Nistari Race of Bombyx mori. Journal of Entomology and Zoology Studies 1, 6165.Google Scholar
Snyder, W.E. & Ives, A.R. (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid. Biological Control 84, 91107.Google Scholar
Spanoudis, C.G. & Andreadis, S.S. (2012) Temperature-dependent survival, development, and adult longevity of the koinobiontendo-parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing Plodia interpunctella (Lepidoptera: Pyralidae). Journal Pest Science 85, 7580.Google Scholar
Thanavendan, S. & Jeyarani, S. (2010) Effect of different temperature regimes on the biology of Bracon brevicornis Wesmael (Braconidae: Hymenoptera) on different host larvae. Journal of Biopestisides 3, 441444.Google Scholar
Torres, J.B., Musolin, D.L. & Zanuncio, J.C. (2002) Thermal requirements and parasitism capacity of Trissolcus brochymenae (Ashmead) (Hymenoptera: Scelionidae) under constant and fluctuating temperatures, and assessment of development in field conditions. Biocontrol of Science and Technology 12, 583593.Google Scholar
Tran, L.T., Worner, S.P., Hale, R.J. & Teulon, D.A.J. (2012) Estimating development rate and thermal requirements of Bactericera Cockerelli (Hemiptera: Triozidae) reared on potato and tomato by using linear and nonlinear models. Environmental Entomology 41, 11901198.Google Scholar
Tsoukanas, V.I., Papadopoulos, G.D., Fantinou, A.A. & Papadoulis, G.T. (2006) Temperature-dependent development and life table of Iphiseius degenerans (Acari: Phytoseiidae). Environmental Entomology 35, 212218.Google Scholar
Vingradova, E.B. & Reznik, S.Y. (2015) Influence of constant and changing temperatures on the larval development of Calliphora vicina (Diptera: Calliphoridae). Acta Societatis Zoologicae Bohemicae 79, 149154.Google Scholar
Visser, M.E. & Both, C. (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society of B 2 72, 25612569.Google Scholar
Walgama, R.S. & Zalucki, M.P. (2006) Evaluation of different models to describe egg and pupal development of Xyleborus fornicatus Eichh. (Coleoptera: Scolytidae), the shot-hole borer of tea in Sri Lanka. Insect Science 13, 109118.Google Scholar
Zahiri, B., Fathipour, Y., Khanjani, M., Moharramipour, S. & Zalucki, M.P. (2010) Preimaginal development response to constant temperatures in Hypera postica (Coleoptera: Curculionidae): picking the best model. Environmental Entomology 39, 177189.Google Scholar