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Phenological synchrony between Scaphoideus titanus (Hemiptera: Cicadellidae) hatchings and grapevine bud break: could this explain the insect's expansion?

Published online by Cambridge University Press:  23 October 2014

J. Chuche ,
E. Desvignes ,
O. Bonnard  and
D. Thiéry
J. Chuche*
Affiliation:
INRA, UMR1065, Santé et Agroécologie du Vignoble, ISVV, BP 81, 33883 Villenave d'Ornon cedex, France Université de Bordeaux, Bordeaux Sciences agro, UMR1065 Santé et agroécologie du vignoble, BP 81, 33883 Villenave d'Ornon cedex, France
E. Desvignes
Affiliation:
INRA, UMR1065, Santé et Agroécologie du Vignoble, ISVV, BP 81, 33883 Villenave d'Ornon cedex, France Université de Bordeaux, Bordeaux Sciences agro, UMR1065 Santé et agroécologie du vignoble, BP 81, 33883 Villenave d'Ornon cedex, France
O. Bonnard
Affiliation:
INRA, UMR1065, Santé et Agroécologie du Vignoble, ISVV, BP 81, 33883 Villenave d'Ornon cedex, France Université de Bordeaux, Bordeaux Sciences agro, UMR1065 Santé et agroécologie du vignoble, BP 81, 33883 Villenave d'Ornon cedex, France
D. Thiéry
Affiliation:
INRA, UMR1065, Santé et Agroécologie du Vignoble, ISVV, BP 81, 33883 Villenave d'Ornon cedex, France Université de Bordeaux, Bordeaux Sciences agro, UMR1065 Santé et agroécologie du vignoble, BP 81, 33883 Villenave d'Ornon cedex, France
*
*Author for correspondence Phone: +33 5 57 12 26 39 Fax: +33 5 57 12 26 21 E-mail: jchuche@bordeaux.inra.fr
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Abstract

Scaphoideus titanus is the invasive vector of the phytoplasma causing the Flavescence dorée in European vineyards. This epidemic is a serious threat to viticulture that has been increasing for more than 60 years in Europe. We studied the effect of synchrony with the plant phenology and the effect of plant-sap quality on the individual fitness. Thus, we conducted laboratory experiments to determine if insect hatchings were synchronized with grapevine bud break. We used two natural populations: one from a cold winter vineyard and one from a mild winter vineyard. In both cases, egg hatching was synchronized with bud break and leaf appearance. The phloem quality of the young and old leaves as a food source was analysed by high-performance liquid chromatography, and the effects on S. titanus growth were evaluated. Phloem composition varied with the grapevine cutting's age but also varied between leaves of different ages from the same plant. The older leaves were less nutritious because they had the highest carbon-to-nitrogen ratio and the lowest content of essential amino acids. Despite diverse phloem qualities, no fitness difference was observed. We found that the synchronization of egg hatchings with bud break is well regulated. However, the nymphs are not affected by the phloem-sap quality, suggesting that S. titanus may accept different food qualities and that egg hatching synchrony could contribute to population expansion in vineyards.

Keywords

phloem qualitysynchronygrapevineVitis viniferaFlavescence dorée
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 1 , February 2015 , pp. 82 - 91
Copyright
Copyright © Cambridge University Press 2014 

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References

Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Araya, T., Noguchi, K. & Terashima, I. (2006) Effects of carbohydrate accumulation on photosynthesis differ between sink and source leaves of Phaseolus vulgaris L. Plant and Cell Physiology 47, 644–652.CrossRefGoogle ScholarPubMed
Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817–844.CrossRefGoogle ScholarPubMed
Bi, J., Castle, S. & Toscano, N. (2007) Amino acid fluctuations in young and old orange trees and their influence on glassy-winged sharpshooter (Homalodisca vitripennis) population densities. Journal of Chemical Ecology 33, 1692–1706.CrossRefGoogle Scholar
Bird, J.M. & Hodkinson, I.D. (2005) What limits the altitudinal distribution of Craspedolepta species (Sternorrhyncha: Psylloidea) on fireweed? Ecological Entomology 30, 510–520.CrossRefGoogle Scholar
Bonfils, J. & Schvester, D. (1960) Les cicadelles (Homoptera Auchenorhyncha) dans leurs rapports avec la vigne dans le Sud-Ouest de la France. Annales des Epiphyties 3, 325–336.Google Scholar
Cates, R.G. (1980) Feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores: The effect of resource abundance and plant chemistry. Oecologia 46, 22–31.CrossRefGoogle ScholarPubMed
Caudwell, A., Kuszala, C., Bachelier, J.C. & Larrue, J. (1970) Transmission de la Flavescence dorée de la vigne aux plantes herbacées par l'allongement du temps d'utilisation de la cicadelle Scaphoideus littoralis BALL et l’étude de sa survie sur un grand nombre d'espèces végétales. Annales de Phytopathologie 2, 415–428.Google Scholar
Caudwell, A. & Larrue, J. (1979) Examen du problème de la Flavescence dorée dans le cadre de la sélection sanitaire des bois et plants de vigne. Le Progrès Agricole et Viticole 96, 128–134.Google Scholar
Chandler, S.M., Wilkinson, T.L. & Douglas, A.E. (2008) Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proceedings of the Royal Society B: Biological Sciences 275, 565–570.CrossRefGoogle ScholarPubMed
Chuche, J. & Thiéry, D. (2009) Cold winter temperatures condition the egg-hatching dynamics of a grape disease vector. Naturwissenschaften 96, 827–834.CrossRefGoogle ScholarPubMed
Chuche, J. & Thiéry, D. (2012) Egg incubation temperature differently affects female and male hatching dynamics and larval fitness in a leafhopper. Ecology and Evolution 2, 732–739.CrossRefGoogle Scholar
Chuche, J. & Thiéry, D. (2014) Biology and ecology of the Flavescence dorée vector Scaphoideus titanus. A review. Agronomy for Sustainable Development 34, 381–403.CrossRefGoogle Scholar
Crotti, E., Damiani, C., Pajoro, M., Gonella, E., Rizzi, A., Ricci, I., Negri, I., Scuppa, P., Rossi, P., Ballarini, P., Raddadi, N., Marzorati, M., Sacchi, L., Clementi, E., Genchi, M., Mandrioli, M., Bandi, C., Favia, G., Alma, A. & Daffonchio, D. (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environmental Microbiology 11, 3252–3264.CrossRefGoogle ScholarPubMed
Crotti, E., Rizzi, A., Chouaia, B., Ricci, I., Favia, G., Alma, A., Sacchi, L., Bourtzis, K., Mandrioli, M., Cherif, A., Bandi, C. & Daffonchio, D. (2010) Acetic acid bacteria, newly emerging symbionts of insects. Applied and Environmental Microbiology 76, 6963–6970.CrossRefGoogle ScholarPubMed
Della Giustina, W., Hogrel, R. & Della Giustina, M. (1992) Description des différents stades larvaires de Scaphoideus titanus Ball (Homoptera, Cicadellidae). Bulletin de la Societe Entomologique de France 97, 269–276.Google Scholar
Dewar, R.C. & Watt, A.D. (1992) Predicted changes in the synchrony of larval emergence and budburst under climatic warming. Oecologia 89, 557–559.CrossRefGoogle ScholarPubMed
Dixon, A.F.G. (1976) Timing of egg hatch and viability of sycamore aphid, Drepanosiphum platanoidis (Schr.), at bud burst of sycamore, Acer pseudoplatanus L. Journal of Animal Ecology 45, 593–603.CrossRefGoogle Scholar
Douglas, A.E. (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecological Entomology 18, 31–38.CrossRefGoogle Scholar
Douglas, A.E. (1998) Nutritional interactions in insect–microbial symbioses: Aphids and their symbiotic bacteria Buchnera . Annual Review of Entomology 43, 17–37.CrossRefGoogle ScholarPubMed
Douglas, A.E. (2009) The microbial dimension in insect nutritional ecology. Functional Ecology 23, 38–47.CrossRefGoogle Scholar
Douglas, A.E., Price, D.R.G., Minto, L.B., Jones, E., Pescod, K.V., Francois, C., Pritchard, J. & Boonham, N. (2006) Sweet problems: insect traits defining the limits to dietary sugar utilisation by the pea aphid, Acyrthosiphon pisum . Journal of Experimental Biology 209, 1395–1403.CrossRefGoogle ScholarPubMed
Duchêne, E. & Schneider, C. (2005) Grapevine and climatic changes: a glance at the situation in Alsace. Agronomy for Sustainable Development 25, 93–99.CrossRefGoogle Scholar
Ellers, J. & van Alphen, J.J.M. (2002) A trade-off between diapause duration and fitness in female parasitoids. Ecological Entomology 27, 279–284.CrossRefGoogle Scholar
Feldhaar, H. & Gross, R. (2009) Insects as hosts for mutualistic bacteria. International Journal of Medical Microbiology 299, 1–8.CrossRefGoogle ScholarPubMed
Frago, E., Dicke, M. & Godfray, H.C.J. (2012) Insect symbionts as hidden players in insect–plant interactions. Trends in Ecology & Evolution 27, 705–711.CrossRefGoogle ScholarPubMed
Garcia-Berthou, E. (2001) On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology 70, 708–711.CrossRefGoogle Scholar
Gould, G.G., Jones, C.G., Rifleman, P., Perez, A. & Coleman, J.S. (2007) Variation in eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behavior of the aphid, Chaitophorous populicola Thomas (Homoptera : Aphididae). Environmental Entomology 36, 1212–1225.CrossRefGoogle ScholarPubMed
Hopper, K.R. (1999) Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535–560.CrossRefGoogle ScholarPubMed
Horvath, D.P., Anderson, J.V., Chao, W.S. & Foley, M.E. (2003) Knowing when to grow: signals regulating bud dormancy. Trends in Plant Science 8, 534–540.CrossRefGoogle ScholarPubMed
Hunt, E.J., Pritchard, J., Bennett, M.J., Zhu, X., Barrett, D.A., Allen, T., Bale, J.S. & Newbury, H.J. (2006) The Arabidopsis thaliana Myzus persicae model system demonstrates that a single gene can influence the interaction between a plant and a sap-feeding insect. Molecular Ecology 15, 4203–4213.CrossRefGoogle Scholar
Hunter, M.D. & McNeil, J.N. (1997) Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78, 977–986.CrossRefGoogle Scholar
Jonas, J.L. & Joern, A. (2008) Host-plant quality alters grass/forb consumption by a mixed-feeding insect herbivore, Melanoplus bivittatus (Orthoptera: Acrididae). Ecological Entomology 33, 546–554.CrossRefGoogle Scholar
Jones, B.N., Pääbo, S. & Stein, S. (1981) Amino acid analysis and enzymatic sequence determination of peptides by an improved o-phthaldialdehyde precolumn labeling procedure. Journal of Liquid Chromatography 4, 565–586.CrossRefGoogle Scholar
Karley, A.J., Douglas, A.E. & Parker, W.E. (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. Journal of Experimental Biology 205, 3009–3018.CrossRefGoogle ScholarPubMed
King, R.W. & Zeevaart, J.A.D. (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiology 53, 96–103.CrossRefGoogle ScholarPubMed
Kliewer, W.M. & Soleimani, A. (1972) Effect of chilling on budbreak in ‘Thompson Seedless’ and ‘Carignane’ grapevines. American Journal of Enology and Viticulture 23, 31–34.CrossRefGoogle Scholar
Kroon, A. & Veenendaal, R.L. (1998) Trade-off between diapause and other life-history traits in the spider mite Tetranychus urticae . Ecological Entomology 23, 298–304.CrossRefGoogle Scholar
Lavee, S. & May, P. (1997) Dormancy of grapevine buds – facts and speculation. Australian Journal of Grape and Wine Research 3, 31–46.CrossRefGoogle Scholar
Lawrence, R.K., Mattson, W.J. & Haack, R.A. (1997) White spruce and the spruce budworm: Defining the phenological window of susceptibility. Canadian Entomologist 129, 291–318.CrossRefGoogle Scholar
Malausa, J.C. & Sentenac, G. (2011) Parasitoïdes de Scaphoideus titanus . pp. 143–146 in Sentenac, G. (Ed.) La faune Auxiliaire des vignobles de France. Paris, France Agricole.Google Scholar
Marchi, S., Tognetti, R., Minnocci, A., Borghi, M. & Sebastiani, L. (2008) Variation in mesophyll anatomy and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus persica) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea). Trees – Structure and Function 22, 559–571.CrossRefGoogle Scholar
Marzorati, M., Alma, A., Sacchi, L., Pajoro, M., Palermo, S., Brusetti, L., Raddadi, N., Balloi, A., Tedeschi, R., Clementi, E., Corona, S., Quaglino, F., Bianco, P.A., Beninati, T., Bandi, C. & Daffonchio, D. (2006) A novel bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of flavescence dorée in Vitis vinifera . Applied and Environmental Microbiology 72, 1467–1475.CrossRefGoogle ScholarPubMed
Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11, 119–161.CrossRefGoogle Scholar
Merritt, S.Z. (1996) Within-plant variation in concentrations of amino acids, sugar, and sinigrin in phloem sap of black mustard, Brassica nigra (L) Koch (Cruciferae). Journal of Chemical Ecology 22, 1133–1145.CrossRefGoogle ScholarPubMed
Mooney, H.A. & Gulmon, S.L. (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32, 198–206.CrossRefGoogle Scholar
Moreau, J., Arruego, X., Benrey, B. & Thiery, D. (2006) Differences in nutritional quality of parts of Vitis vinifera berries affect fitness of the European grapevine moth. Entomologia Experimentalis Et Applicata 119, 93–99.CrossRefGoogle Scholar
Moreau, J., Thiéry, D., Troussard, J.P. & Benrey, B. (2007) Grape variety affects female but also male reproductive success in wild European grapevine moths. Ecological Entomology 32, 747–753.CrossRefGoogle Scholar
Oliver, K.M., Degnan, P.H., Burke, G.R. & Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology 55, 247–266.CrossRefGoogle ScholarPubMed
Pescod, K.V., Quick, W.P. & Douglas, A.E. (2007) Aphid responses to plants with genetically manipulated phloem nutrient levels. Physiological Entomology 32, 253–258.CrossRefGoogle Scholar
Quental, T.B., Trigo, J.R. & Oliveira, P.S. (2005) Host-plant flowering status and the concentration of sugar in phloem sap: Effects on an ant-treehopper interaction. European Journal of Entomology 102, 201–208.CrossRefGoogle Scholar
Rajon, E., Venner, S. & Menu, F. (2009) Spatially heterogeneous stochasticity and the adaptive diversification of dormancy. Journal of Evolutionary Biology 22, 2094–2103.CrossRefGoogle ScholarPubMed
R Development Core Team (2007) R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna, Available online at http://www.R-project.org.Google Scholar
Rossi, A.M. & Strong, D.R. (1991) Effects of host-plant nitrogen on the preference and performance of laboratory populations of Carneocephala floridana (Homoptera, Cicadellidae). Environmental Entomology 20, 1349–1355.CrossRefGoogle Scholar
Sacchi, L., Genchi, M., Clementi, E., Bighardi, E., Avanzati, A.M., Pajoro, M., Negri, I., Marzorati, M., Gonella, E., Alma, A., Daffonchio, D. & Bandi, C. (2008) Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera : Cicadellidae): details of transovarial transmission of Cardinium sp and yeast-like endosymbionts. Tissue and Cell 40, 231–242.CrossRefGoogle ScholarPubMed
Sandstrom, J., Telang, A. & Moran, N.A. (2000) Nutritional enhancement of host plants by aphids – a comparison of three aphid species on grasses. Journal of Insect Physiology 46, 33–40.CrossRefGoogle ScholarPubMed
Sasaki, T. & Ishikawa, H. (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum . Journal of Insect Physiology 41, 41–46.CrossRefGoogle Scholar
Schvester, D., Moutous, G., Bonfils, J. & Carle, P. (1962) Étude biologique des cicadelles de la vigne dans le Sud-Ouest de la France. Annales des Epiphyties 13, 205–237.Google Scholar
Scriber, J.M. & Slansky, F. (1981) The nutritional ecology of immature insects. Annual Review of Entomology 26, 183–211.CrossRefGoogle Scholar
Snedecor, G.W. & Cochran, W.G. (1967) Stastistical Methods. 6th edn. Ames, Iowa, Iowa State Univ. Press.Google Scholar
Turgeon, R. & Wolf, S. (2009) Phloem transport: cellular pathways and molecular trafficking. Annual Review of Plant Biology 60, 207–221.CrossRefGoogle ScholarPubMed
van Asch, M. & Visser, M.E. (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annual Review of Entomology 52, 37–55.CrossRefGoogle ScholarPubMed
van Leeuwen, C., Garnier, C., Agut, C., Baculat, B., Bersnard, E., Bois, B., Boursiquot, J.-M., Chuine, I., Dessup, T., Dufrourcq, T., Garcia-Cortazar, I., Merguerite, E., Monamy, C., Koundouras, S., Payan, J.-C., Parker, A., Renouf, A., Rodriguez-Lovelle, B., Roby, J.-P., Tonietto, J. & Trambouze, W.I.l. (2008) Heat requirements for grapevine varieties is essential information to adapt plant material in changing climate VIIth International terroir Congress. Changins, Switzerland, 20–23 May 2008.Google Scholar
van Wijk, M.T., Williams, M. & Shaver, G.R. (2005) Tight coupling between leaf area index and foliage N content in arctic plant communities. Oecologia 142, 421–427.CrossRefGoogle ScholarPubMed
Vidano, C. (1964) Scoperta in Italia dello Scaphoideus littoralis Ball cicalina americana collegata alla «Flavescence dorée» della Vite. L'Italia agricola 101, 1031–1049.Google Scholar
Wang, X.P., Xue, F.S., Hua, A. & Ge, F. (2006) Effects of diapause duration on future reproduction in the cabbage beetle, Colaphellus bowringi: positive or negative? Physiological Entomology 31, 190–196.CrossRefGoogle ScholarPubMed
Watt, A.D. & McFarlane, A.M. (1991) Winter moth on Sitka spruce: synchrony of egg hatch and budburst, and its effect on larval survival. Ecological Entomology 16, 387–390.CrossRefGoogle Scholar
Wilkinson, T.L. & Douglas, A.E. (2003) Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae . Entomologia Experimentalis Et Applicata 106, 103–113.CrossRefGoogle Scholar
Wu, D., Daugherty, S.C., Van Aken, S.E., Pai, G.H., Watkins, K.L., Khouri, H., Tallon, L.J., Zaborsky, J.M., Dunbar, H.E., Tran, P.L., Moran, N.A. & Eisen, J.A. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. Plos Biology 4, 1079–1092.CrossRefGoogle ScholarPubMed
Yao, I. & Akimoto, S.I. (2002) Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola . Ecological Entomology 27, 745–752.CrossRefGoogle Scholar
Yukawa, J. & Akimoto, K. (2006) Influence of synchronization between adult emergence and host plant phenology on the population density of Pseudasphondylia neolitseae (Diptera: Cecidomyiidae) inducing leaf galls on Neolitsea sericea (Lauraceae). Population Ecology 48, 13–21.CrossRefGoogle Scholar
Zar, J.H. (2010) Biostatistical Analysis. 5th edn. Upper Saddle River, NJ, Prentice Hall.Google Scholar