Skip to main content
Log in

Influence of Temperature on Flight, Walking and Oviposition Capacities of two Aphid Parasitoid Species (Hymenoptera: Aphidiinae)

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae) is one of the major pests of many greenhouse crops. The aphid parasitoids, Aphidius colemani Viereck and Aphidius matricariae (Haliday) (Hymenoptera: Braconidae: Aphidiinae) have been considered good agents for the biological control of A. gossypii. In Mediterranean area, these parasitoids can currently be released under elevated temperature conditions. However, few findings on their behavior changes with temperature are available. In this study, we analyze the consequence of constant temperatures ranging from 20 to 32 °C on the flight, walking and oviposition capacities of Aphidius colemani and Aphidius matricariae. Our results revealed that flight capacity is clearly influenced by temperature. The optimal temperatures for flying are 20 and 25 °C for A. colemani and A. matricariae, respectively. For both species, we observed an increase in the walking capacity but a decrease in the reproductive potential at higher temperatures. Furthermore, regardless of the tested temperature, the mummy production rate was always higher in A. colemani than in A. matricariae. These results indicate that A. colemani is more suitable than A. matricariae for the biological control of A. gossypii in Mediterranean environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

References

  • Aldyhim YN, Khalil AF (1993) Influence of temperature and daylength on population development of Aphis gossypii on Cucurbita pepo. Entomol Exp Appl 67(2):167–172

    Article  Google Scholar 

  • Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994

    Article  CAS  PubMed  Google Scholar 

  • Ben Halima Kamel M, Ben Hamouda MH (1993) Les pucerons des cultures protégées et leurs ennemis en Tunisie. Tropicultura 11:50–53

    Google Scholar 

  • Bennison JA (1992) Biological control of aphid on cucumber, use of open systems or banker plants to aid establishment Aphidius matricariae and Aphidoletes aphidomyza. Meded Fac Landbouwwet Univ Gent 57:457–466

    Google Scholar 

  • Blackmer JL, Cross D (2001) Response of Eretmocerus eremicus to skylight and plant cues in a vertical flight chamber. Entomol Exp Appl 100:295–300

    Article  Google Scholar 

  • Boivin G, Kölliker-Ott UM, Bale J, Bigler F (2006) Assessing the establishment potential of inundative biological control agents. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publication, Wallingford, pp 98–113

    Chapter  Google Scholar 

  • Boivin G, Hance T, Brodeur J (2012) Aphid parasitoids in biological control. Can J Plant Sci 92:1–12

    Article  Google Scholar 

  • Boldt PE (1974) Temperature, humidity, and host: effect on rate of search of Trichogramma evanescens and T. minutum Auctt. Ann Entomol Soc Am 67:706–708

    Article  Google Scholar 

  • Boukhris-Bouhachem S (2011) Aphid enemies reported from Tunisian citrus orchards. Tunis J Plant Prot 6:21–27

    Google Scholar 

  • Bourchier RS, Smith SM (1996) Influence of environmental conditions and parasitoid quality on field performance of Trichogramma minutum. Entomol Exp Appl 80:461–468

    Article  Google Scholar 

  • Cambier V, Hance T, Hoffmann E (2001) Effects of 1,4-benzoxazin-3-one derivatives from maize on survival and fecundity of Metopolophium dirhodum (Walker) on artificial diet. J Chem Ecol 27:59–370

    Article  Google Scholar 

  • Campolo O, Chiera E, Malacrinò A, Laudani F, Fontana A, Albanese GR, Palmeri V (2014) Acquisition and transmission of selected CTV isolates by Aphis gossypii. J Asia Pac Entomol 17:493–498

    Article  Google Scholar 

  • Carletto J, Lombaert E, Chavigny P, Brevault T, Lapchin L, Vanlerberghe-Masutti F (2009) Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Mol Ecol 18(10):2198–2212

    Article  CAS  PubMed  Google Scholar 

  • Chown SL, Terblanche JS (2006) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:51–55

    Google Scholar 

  • Colinet H, Hance T (2009) Male reproductive potential of Aphidius colemani (Hymenoptera: Aphidiinae) exposed to constant or fluctuating thermal regimens. Environ Entomol 38:242–249

    Article  CAS  PubMed  Google Scholar 

  • Danks HV (2000) Dehydration in dormant insects. J Insect Physiol 46:837–852

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105(18):6668–6672

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edney EB (1977) Water balance in land arthropods. Zoophysiology and Ecology.282 pp

  • Elzen GW, Williams HJ, Vinson SB, Powell JE (1987) Comparative flight behavior of parasitoids Campoletis sonorensis and Microplitis croceipes. Entomol Exp Appl 45:175–180

    Article  Google Scholar 

  • Fasolo AG, Kerbs RA (2004) A comparison of behavioural change in Drosophila during exposure to thermal stress. Biol J Linn Soc 83:197–205

    Article  Google Scholar 

  • Feder ME, Kerbs RA (1998) Natural and genetic engineering of heat –shock protein Hsp 70 in Drosophila melanogaster: consequences for thermotolerance. Amer Zool 38:503–571

    CAS  Google Scholar 

  • Fournier F, Boivin G (2000) Comparative dispersal of Trichogramma evanescens and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in relation to environmental conditions. Environ Entomol 29:55–63

    Article  Google Scholar 

  • Goh HG, Yoo JK (1997) Controlling cotton aphid, Aphis gossypii with the parasitoid Aphidius colemani, on banker plant in greenhouse. In: proceedings of the 6th European congress of Entomology, Ceske Budejovice, P 754

  • Gu H, Dorn S (2001) How do wind velocity and light intensity influence host-location success in Cotesia glomerata (Hym., Braconidae)? J Appl Entomol 125:115–120

    Article  Google Scholar 

  • Gwennan EH, Alford L, Sterk G, Jeffrey SB (2010) Thermal activity thresholds of the predatory mired Nesidiocoris tenuis: implications for its efficacy as a biological control agent. Biocontrol 55:493–501

    Article  Google Scholar 

  • Hance T, Van Baareen J, Vernon P, Boivin G (2007) Impact of extreme temperature on parasitoids in a climate change perspective. Ann Rev Entomol 52:107–126

    Article  CAS  Google Scholar 

  • Havelka J (1978) Carnivorous gall midge Aphidoletes aphidomyza (Diptera: Cecidomyiidae): The bionomic, mass laboratory rearing and use against aphids on greenhouses crops. Ph. D.Thesis, pp 259

  • Heinz KM, Van Driesche RG, Parrella MP (2004) Biocontrol in protected culture. Ball Publishing, Batavia

    Google Scholar 

  • Juillet JA (1964) Influences of weather on flight activity of parasitic Hymenoptera. Can J Zool 43:1133–1141

    Article  Google Scholar 

  • Kersting US, Satar S, Uyum U (1999) Effect of temperature on development rate fecundity of apterous Aphis gossypii reared on Cossypium hirsutum. J Appl Entomol 123:23–27

    Article  Google Scholar 

  • Langer A, Boivin G, Hance T (2004) Oviposition, flight and walking capacity at low temperatures of four aphid parasitoid species (Hymenoptera: Aphidiinae). Eur J Entomol 101:473–479

    Article  Google Scholar 

  • Messing RH, Klungness LM, Jang EB (1997) Effects of wind on movement of Diachasmimorpha longicaudata, a parasitoid of tephritid fruit flies, in a laboratory flight tunnel. Entomol Exp Appl 82:147–152

    Article  Google Scholar 

  • Miller JC, Gerth WJ (1994) Temperature-dependent development of Aphidius matricariae (Hymenoptera: Aphidiidae), as a parasitoid of the Russian wheat aphid. Environ Entomol 23:1304–1307

    Article  Google Scholar 

  • Parrella MP, Hansen LS, Van Lenteren JC (1999) Greenhouse environments. In: Fisher TW, Ellows TS, Caltagirone LE, Dahlstein DL, Huffaker CB, Gordh G (eds) Handbook of bilogical control. Academic, New York, pp 819–839

    Chapter  Google Scholar 

  • Pickett CH, Pitcairn MJ (1999) Classical biological control of ash whitefly: factors contributing to its success in California. BioControl 44:143–158

    Article  Google Scholar 

  • Prinsloo GJ, Hewitt PH, Van Der Westhuizen MC (1993) The effect of temperature on oviposition behaviour and success of two parasitoids of the Russian Wheat Aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae). Afr Entomol 1:189–193

    Google Scholar 

  • Rabasse JM, Shalaby FF (1980) Laboratory studies on the development of Myzus persicae (Homoptera: Aphididae) and its primary parasite, Aphidius matricariae (Hymenoptera:Aphidiidae) at constant temperatures. Oecologia 1:21–28

    Google Scholar 

  • Sørensen JG, Loeschcke V (2007) Studying stress responses in the post-genomic era: its ecological and evolutionary role. J Biosci 32:447–456

    Article  PubMed  Google Scholar 

  • Suverkropp BP, Bigler F, Van Lenteren JC (2001) Temperature influences walking speed and walking activity of Trichogramma brassicae (Hym., Trichogrammatidae). J App Ent 125:303–307

    Article  Google Scholar 

  • Taylor LRB (1963) Analysis of the effect of temperature on insects in flight. J Anim Ecol 32:99–117

    Article  Google Scholar 

  • Toussidou M, Williams M, Leather S (1999) Life history parameters of Aphidius colemani on sweet pepper in different temperatures regimes. IOBC/ WPRS Bull 22:255–258

    Google Scholar 

  • Van Lenteren JC, Woets J (1988) Biological and integrate pest control in greenhouse. Ann Rev Entomol 33:239–269

    Article  Google Scholar 

  • Van Lenteren JC, Bale J, Bigler E, Hokkanen HMT, Loomans AM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634

    Article  PubMed  Google Scholar 

  • Van Steenis MJ (1993) Suitability of Aphis gossypii, Macrosiphum euphorbiae and Myzus persicae as host for several aphid parasitoid species. IOBC/WPRS Bull 16:157–160

    Google Scholar 

  • Van Steenis MJ, El- Khawass KAM (1995) Life history of Aphis gossypii on cucumber: influence of temperature, host plant and parasitism. Entomol Exp Appl 76:121–131

    Article  Google Scholar 

  • Walter KFA, Dixon AFG (1984) The effect of temperature and wind on the flight activity of cereal aphids. Ann App Biol 104:17–26

    Article  Google Scholar 

  • Wharton GW (1985) Water balance of insects pp 565–603. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Vol.4. Pergamon Press, Oxford

    Google Scholar 

  • Wu GM, Barrette M, Boivin G, Brodeur J, Giraldeau LA, Hance T (2011) Temperature influences the handling efficiency of an aphid parasitoid through body size-mediated effects. Environ Entomol 40(3):737–742

    Article  PubMed  Google Scholar 

  • Xia JY, Van Der Werf W, Rabbinge R (1999) Influence of temperature on bionomics of cotton aphid, Aphis gossypii, on cotton. Entomol Exp Appl 90:25–35

    Article  Google Scholar 

  • Zamani AA, Talebi AA, Fathipour Y, Baniameri V (2006) Temperature- dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. J Pest Sci 79:183–188

    Article  Google Scholar 

  • Zamani AA, Talebi A, Fathipour Y, Baniameri A (2007) Effect of temperature on life history of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae), two Parasitoids of Aphis gossypii and Myzus persicae (Homoptera: Aphididae). Environ Entomol 36:263–271

    Article  PubMed  Google Scholar 

  • Zamani AA, Mostafa H, Keradmands K (2012) Effect of temperature on reproductive parameters of Aphidius colemani and Aphidius matricariae (Hemoptera: Aphididae) in laboratory conditions. J Crop Prot 1:35–40

    Google Scholar 

  • Zappalà L, Campolo O, Grande S, Saraceno F, Biondi A, Siscaro G, Palmeri V (2012) Dispersal of Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards. Eur J Entomol 109:561–568

    Article  Google Scholar 

Download references

Acknowledgments

The present study was supported by a grant from the Ministry of High Education of Tunisia. Aphidius colemani was provided by Viridaxis S.A. This manuscript is publication number XXX of the Biodiversity Research Centre.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mey Jerbi-Elayed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jerbi-Elayed, M., Lebdi-Grissa, K., Le Goff, G. et al. Influence of Temperature on Flight, Walking and Oviposition Capacities of two Aphid Parasitoid Species (Hymenoptera: Aphidiinae). J Insect Behav 28, 157–166 (2015). https://doi.org/10.1007/s10905-015-9490-8

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-015-9490-8

Keywords

Navigation