Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-03T10:01:57.928Z Has data issue: false hasContentIssue false
  • English
  • Français

Diapause incidence and duration in the pest mango blossom gall midge, Procontarinia mangiferae (Felt), on Reunion Island

Published online by Cambridge University Press:  25 June 2014

P. Amouroux ,
F. Normand ,
H. Delatte ,
A. Roques  and
S. Nibouche
P. Amouroux
Affiliation:
CIRAD, UPR HortSys, 97455 Saint-Pierre, La Réunion, France Université de la Réunion, UMR PVBMT, 97410 Saint-Pierre, La Réunion, France
F. Normand
Affiliation:
CIRAD, UPR HortSys, 97455 Saint-Pierre, La Réunion, France
H. Delatte
Affiliation:
CIRAD, UMR PVBMT, 97410 Saint-Pierre, La Réunion, France
A. Roques
Affiliation:
INRA, UR633 Zoologie Forestière, 45075 Orléans, France
S. Nibouche*
Affiliation:
CIRAD, UMR PVBMT, 97410 Saint-Pierre, La Réunion, France
*
*Author for correspondence Fax: +262 262 499 293 E-mail: samuel.nibouche@cirad.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

The mango blossom gall midge, Procontarinia mangiferae, is a multivoltine species that induces galls in inflorescences and leaves of the mango tree, Mangifera indica. In subtropical Reunion Island, populations of P. mangiferae are observed all-year round, but the pattern and the role of dormancy in their life cycle have never been documented. We performed field and laboratory experiments using more than 15,000 larvae. We demonstrated that a larval diapause may affect a part of the midge population, regardless of the season. The total duration of the diapause varied from 6 weeks to more than 1 year. One year of field monitoring showed that the highest incidence of diapause was observed in larvae collected during the summer from mango leaves, where it affected approximately one-third of the individuals. This facultative diapause allows the permanent presence of P. mangiferae in the orchards. By recording diapause duration during 22 weeks under controlled conditions, we showed that high temperatures (26 °C) increased diapause duration and extended the range of the dates of diapause emergence, whereas cool temperatures (20 °C) shortened diapause duration and shortened the range of the dates of emergence from diapause. A temperature decrease from 26 to 20 °C triggered the emergence of diapausing individuals. These mechanisms ensure the synchronization of the emergence of diapausing individuals with the appearance of mango inflorescences, which is also induced by cool winter temperatures.

Keywords

facultative diapausetropical gall midgeCecidomyiidaeMangifera indica
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 5 , October 2014 , pp. 661 - 670
Copyright
Copyright © Cambridge University Press 2014 

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

Amouroux, P., Normand, F., Nibouche, S. & Delatte, H. (2013) Invasive mango blossom gall midge, Procontarinia mangiferae (Felt) (Diptera: Cecidomyiidae) in Reunion Island: ecological plasticity, permanent and structured populations. Biological Invasions 15(8), 1677–1693.CrossRefGoogle Scholar
Annila, E. (1981) Fluctuations in cone and seed insect populations in Norway spruce. Communicationes Instituti Forestalis Fenniae 101, 1–32.Google Scholar
Auger-Rozenberg, M.A. & Roques, A. (2012) Seed wasp invasions promoted by unregulated seed trade affect vegetal and animal biodiversity. Integrative Zoology 7, 228–246.CrossRefGoogle ScholarPubMed
Baxendale, F.P. & Teetes, G.L. (1983) Factors influencing adult emergence from Diapausing Sorghum Midge, Contarinia sorghicola (Diptera: Cecidomyiidae). Environmental Entomology 12, 1064–1067.CrossRefGoogle Scholar
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate - a pratical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B - Methodological 57(1), 289–300.Google Scholar
Benoit, J.B., Morton, P.K., Cambron, S.E., Patrick, K.R. & Schemerhorn, B.J. (2010) Aestivation and diapause syndromes reduce the water balance requirements for pupae of the Hessian fly, Mayetiola destructor. Entomologia Experimentalis et Applicata 136(1), 89–96.CrossRefGoogle Scholar
Dambreville, A., Lauri, P.E., Trottier, C., Guédon, Y. & Normand, F. (2013) Deciphering structural and temporal interplays during the architectural development of mango trees. Journal of Experimental Botany 64, 2467–2480.CrossRefGoogle ScholarPubMed
Danks, H.V. (1987) Insect Dormancy: an Ecological Perspective. Biological Survey of Canada Monographs. Biological Survey of Canada.Google Scholar
Danks, H.V. (2007) The elements of seasonal adaptations in insects. Entomological Society of Canada 139, 1–44.CrossRefGoogle Scholar
Denlinger, D.L. (1986) Dormancy in tropical insects. Annual Review of Entomology 31, 239–264.CrossRefGoogle ScholarPubMed
Denlinger, D.L. (2002) Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
Freeman, B.E. & Geoghagen, A. (1989) A population study in Jamaica on the gall-midge Asphondylia boerhaaviae: a contribution to spatial dynamics. Journal of Animal Ecology 58(2), 367–382.CrossRefGoogle Scholar
Gagné, R.J. (2010) Update for a catalog of the Cecidomyiidae (Diptera) of the world. Digital version 1. USDA, Washington. Available online at http://www.ars.usda.gov/SP2UserFiles/Place/12754100/Gagne_2010_World_Catalog_Cecidomyiidae.pdf (accessed 2013-04-02).Google Scholar
Hanski, I. (1988) Four kinds of extra long diapause in insects: a review of theory and observation. Annales Zoologici Fennici 25, 37–53.Google Scholar
Hao, Y.J., Li, W.S., He, Z.B., Si, F.L., Ishikawa, Y. & Chen, B. (2012) Differential gene expression between summer and winter diapause pupae of the onion maggot Delia antiqua, detected by suppressive subtractive hybridization. Journal of Insect Physiology 58(11), 1444–1449.CrossRefGoogle Scholar
He, H.-M., Xian, Z.-H., Huang, F., Liu, X.-P. & Xue, F.-S. (2009) Photoperiodism of diapause induction in Thyrassia penangae (Lepidoptera: Zygaenidae). Journal of Insect Physiology 55(11), 1003–1008.CrossRefGoogle ScholarPubMed
Hedlin, A.F. (1964) A six-year plot study on Douglas-fir cone insect population fluctuations. Forest Science 10, 124–128.Google Scholar
Higaki, M. & Toyama, M. (2012) Evidence for reversible change in intensity of prolonged diapause in the chestnut weevil Curculio sikkimensis. Journal of Insect Physiology 58(1), 56–0.CrossRefGoogle ScholarPubMed
Hong Kong Observatory (2012) Available online at http://www.weather.gov.hk/wxinfo/climat/world/eng/asia/india/hyderabad_e.htm (accessed 2013-04-02).Google Scholar
Hunter, M.D. & McNeil, J.N. (1997) Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78(4), 977–986.CrossRefGoogle Scholar
Jiang, X.F., Huang, S.H., Luo, L.Z., Liu, Y. & Zhang, L. (2010) Diapause termination, post-diapause development and reproduction in the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). Journal of Insect Physiology 56(9), 1325–1331.CrossRefGoogle Scholar
Kelly, D. (1994) The evolutionary ecology of mast seeding. Trends in Ecology and Evolution 9(12), 465–470.CrossRefGoogle ScholarPubMed
Kelly, D., Turnbull, M.H., Pharis, R.P. & Sarfati, M.S. (2008) Mast seeding, predator satiation, and temperature cues in Chionochloa (Poaceae). Population Ecology 50(4), 343–355.CrossRefGoogle Scholar
Kolesik, P., Rice, A.D., Bellis, G.A. & Wirthensohn, M.G. (2009) Procontarinia pustulata, a new gall midge species (Diptera: Cecidomyiidae) feeding on mango, Mangifera indica (Anarcadiaceae), in northern Australia and Papua New Guinea. Australian Journal of Entomology 48, 310–316.CrossRefGoogle Scholar
Kolesik, P., Sarfati, M.S., Brockerhoff, E.G. & Kelly, D. (2007) Description of Eucalyptodiplosis chionochloae sp nov, a cecidomyiid feeding on inflorescences of Chionochloa (Poaceae) in New Zealand. New Zealand Journal of Zoology 34(2), 107–115.CrossRefGoogle Scholar
Kostal, V. (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52(2), 113–127.CrossRefGoogle ScholarPubMed
Lehmann, P., Lyytinen, A., Sinisalo, T. & Lindstrom, L. (2012) Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata). Journal of Insect Physiology 58(8), 1146–1158.CrossRefGoogle Scholar
Liu, Z., Gong, P., Li, D. & Wei, W. (2010) Pupal diapause of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) mediated by larval host plants: pupal weight is important. Journal of Insect Physiology 56(12), 1863–1870.CrossRefGoogle ScholarPubMed
Liu, Z.D., Gong, P.Y., Wu, K.J., Sun, J.H. & Li, D.M. (2006) A true summer diapause induced by high temperatures in the cotton bollworm, Helicoverpa armigera (Lepidoptera : Noctuidae). Journal of Insect Physiology 52(10), 1012–1020.CrossRefGoogle ScholarPubMed
Masaki, S. (1980) Summer Diapause. Annual Review of Entomology 25(1), 1–25.CrossRefGoogle Scholar
Mironidis, G.K. & Savopoulou-Soultani, M. (2012) Effects of constant and changing temperature conditions on diapause induction in Helicoverpa armigera (Lepidoptera: Noctuidae). Bulletin of Entomological Research 102(2), 139–147.CrossRefGoogle ScholarPubMed
Nibouche, S. (1998) High temperature induced diapause in the cotton bollworm shape Helicoverpa armigera. Entomologia Experimentalis et Applicata 87(3), 271–274.CrossRefGoogle Scholar
Nuñez-Elisea, R. & Davenport, T.L. (1994) Flowering of mango trees in containers as influenced by seasonal temperature and water stress. Scientia Horticulturae 58, 57–66.CrossRefGoogle Scholar
Pezhman, H. & Askari, M. (2004) A study on the biology of mango inflorescence midge in Hormozgan province. Applied Entomology and Phytopathology 72(1), 19–29.Google Scholar
Prasad, S.N. (1971) The Mango Midge Pests. Allahabad, India, Cecidological Society of India, 172 pp.Google Scholar
Prasad, S.N. & Grover, P. (1974) Population fluctuation of Erosomyia indica Grover. Cecidologia indica IX(1&2), 1–38.Google Scholar
Ragland, G.J., Egan, S.P., Feder, J.L., Berlocher, S.H. & Hahn, D.A. (2011) Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. Journal of Experimental Biology 214(23), 3948–3959.CrossRefGoogle ScholarPubMed
Raman, A. (2012) Adaptive radiation and diversification in gall-inducing insects in the Indian subcontinent: search for a pattern. Deutsche Entomologische Zeitschrift 59(2), 177–187.Google Scholar
R Development Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. Website http://www.R-project.org /.Google Scholar
Roux, G. & Roques, A. (1997) Effect of photoperiod and temperature on induction and termination of prolonged diapause of the seed chalcid Megastigmus spermotrophus (Hym., Torymidae). Oecologia 111, 172–177.Google Scholar
Satake, A. & Bjornstad, O.N. (2004) Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants. American Naturalist 163(4), 591–605.CrossRefGoogle ScholarPubMed
Saulich, A. (2010) Long life cycles in insects. Entomological Review 90(9), 1127–1152.CrossRefGoogle Scholar
Shintani, Y., Hirose, Y. & Terao, M. (2011) Effects of temperature, photoperiod and soil humidity on induction of pseudopupal diapause in the bean blister beetle Epicauta gorhami. Physiological Entomology 36(1), 14–20.CrossRefGoogle Scholar
Soula, B. & Menu, F. (2005) Extended life cycle in the chestnut weevil: prolonged or repeated diapause? Entomologia Experimentalis et Applicata 115(2), 333–340.CrossRefGoogle Scholar
Takagi, S. & Miyashita, T. (2008) Host plant quality influences diapause induction of Byasa alcinous (Lepidoptera : Papilionidae). Annals of the Entomological Society of America 101(2), 392–396.CrossRefGoogle Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. Oxford, Oxford University Press, 414 pp.Google Scholar
Terao, M., Hirose, Y. & Shintani, Y. (2012) Effects of temperature and photoperiod on termination of pseudopupal diapause in the bean blister beetle, Epicauta gorhami. Journal of Insect Physiology 58(5), 737–742.CrossRefGoogle ScholarPubMed
Turgeon, J., Roques, A. & De Groot, P. (1994) Insect fauna of coniferous seed cones: diversity, host plant interactions, impact and management. Annual Review of Entomology 39, 179–212.CrossRefGoogle Scholar
Uechi, N. & Yukawa, J. (2006) Life history patterns and host ranges of the genus Asphondylia (Diptera: Cecidomyiidae). pp. 275–285in Ozaki, K., Yukawa, J., Ohgushi, T. & Price, P.W. (Eds) Galling Arthropods and Their Associates. Tokyo, Japan, Springer.CrossRefGoogle Scholar
Vincenot, D. & Normand, F. (2009) Guide de production intégrée de mangues à la Réunion. Saint-Pierre, Ile de la Réunion, France, CIRAD et Chambre d'Agriculture, 121 pp.Google Scholar
Xiao, H.J., Mou, F.C., Zhu, X.F. & Xue, F.S. (2010) Diapause induction, maintenance and termination in the rice stem borer Chilo suppressalis (Walker). Journal of Insect Physiology 56(11), 1558–1564.CrossRefGoogle ScholarPubMed
Yukawa, J. (2000) Synchronization of gallers with host plant phenology. Population Ecology 42(2), 105–113.CrossRefGoogle Scholar