User menu

Bottom-up regulation of a tritrophic system by Beet yellows virus infection: consequences for aphid-parasitoid foraging behaviour and development

  • Open access
  • PDF
  • 1.45 M
  1. ABISGOLD J. D., SIMPSON S. J., DOUGLAS A. E., Nutrient regulation in the pea aphid Acyrthosiphon pisum: application of a novel geometric framework to sugar and amino acid consumption, 10.1111/j.1365-3032.1994.tb01081.x
  2. AJAYI OLUPOMI, DEWAR A. M., The effect of barley yellow dwarf virus on honeydew production by the cereal aphids, Sitobion avenae and Metopolophium dirhodum, 10.1111/j.1744-7348.1982.tb01932.x
  3. ALBITTAR Loulou, ISMAIL Mohannad, BRAGARD Claude, HANCE Thierry, Host plants and aphid hosts influence the selection behaviour of three aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae), 10.14411/eje.2016.068
  4. Awmack Caroline S., Leather Simon R., Host Plant Quality and Fecundity in Herbivorous Insects, 10.1146/annurev.ento.47.091201.145300
  5. Balachandran S., Hurry V. M., Kelley S. E., Osmond C. B., Robinson S. A., Rohozinski J., Seaton G. G. R., Sims D. A., Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis, 10.1111/j.1399-3054.1997.tb04776.x
  6. Bell W J, Searching Behavior Patterns in Insects, 10.1146/annurev.en.35.010190.002311
  7. Blua Matthew J., Perring Thomas M., Effects of Zucchini Yellow Mosaic Virus on Colonization and Feeding Behavior of Aphis gossypii (Homoptera: Aphididae) Alatae, 10.1093/ee/21.3.578
  8. Blua Matthew J., Perring Thomas M., Madore Monica A., Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients, 10.1007/bf02059607
  9. Bosque-Pérez Nilsa A., Eigenbrode Sanford D., The influence of virus-induced changes in plants on aphid vectors: Insights from luteovirus pathosystems, 10.1016/j.virusres.2011.04.020
  10. Bozarth R.F., Diener T.O., Changes in concentration of free amino acids and amides induced in tobacco plants by potato virus X and potato virus Y, 10.1016/0042-6822(63)90256-3
  11. Bragard C., Caciagli P., Lemaire O., Lopez-Moya J.J., MacFarlane S., Peters D., Susi P., Torrance L., Status and Prospects of Plant Virus Control Through Interference with Vector Transmission, 10.1146/annurev-phyto-082712-102346
  12. Calvo D., Fereres A., The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus, 10.1007/s10526-011-9354-x
  13. Campbell Bruce C., Jones Kenneth C., Dreyer David L., Discriminative behavioral responses by aphids to various plant matrix Polysaccharides, 10.1111/j.1570-7458.1986.tb02166.x
  14. Carver Mary, Franzmann Bernard, LysiphlebusFörster (Hymenoptera: Braconidae: Aphidiinae) in Australia, 10.1046/j.1440-6055.2001.00218.x
  15. Castle S. J., Berger P. H., Rates of growth and increase of Myzus persicae on virus-infected potatoes according to type of virus-vector relationship, 10.1111/j.1570-7458.1993.tb01727.x
  16. Castle S. J., Mowry T. M., Berger P. H., Differential Settling by Myzus persicae (Homoptera: Aphididae) on Various Virus Infected Host Plants, 10.1093/aesa/91.5.661
  17. Christiansen-Weniger Petra, Powell Glen, Hardie Jim, Plant virus and parasitoid interactions in a shared insect vector/host, 10.1046/j.1570-7458.1998.00282.x
  18. Clover, Azam-Ali, Jaggard, Smith, The effects of beet yellows virus on the growth and physiology of sugar beet (Beta vulgaris), 10.1046/j.1365-3059.1999.00307.x
  19. Collett D., Modelling Survival Data in Medical Research, ISBN:9780412448904, 10.1007/978-1-4899-3115-3
  20. Cox DR (1972) Regression models and life tables. Biometrics 38:67–77
  21. Crawley M J, Insect Herbivores and Plant Population Dynamics, 10.1146/annurev.en.34.010189.002531
  22. Culver James N., Padmanabhan Meenu S., Virus-Induced Disease: Altering Host Physiology One Interaction at a Time, 10.1146/annurev.phyto.45.062806.094422
  23. Dáder Beatriz, Moreno Aránzazu, Viñuela Elisa, Fereres Alberto, Spatio-Temporal Dynamics of Viruses are Differentially Affected by Parasitoids Depending on the Mode of Transmission, 10.3390/v4113069
  24. de Oliveira Camila F., Long Elizabeth Y., Finke Deborah L., A negative effect of a pathogen on its vector? A plant pathogen increases the vulnerability of its vector to attack by natural enemies, 10.1007/s00442-013-2854-x
  25. Donaldson Jack R., Gratton Claudio, Antagonistic Effects of Soybean Viruses on Soybean Aphid Performance, 10.1603/0046-225x(2007)36[918:aeosvo];2
  26. Douglas A.E., Parallels and contrasts between symbiotic bacteria and bacterial-derived organelles: evidence from Buchnera, the bacterial symbiont of aphids, 10.1111/j.1574-6941.1997.tb00418.x
  27. Douglas A. E., Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic BacteriaBuchnera, 10.1146/annurev.ento.43.1.17
  28. Douglas AE, Minto LB, Wilkinson TL (2001) Quantifying nutrient production by the microbial symbionts in an aphid. J Exp Biol 204:349
  29. Engelsdorf Timo, Horst Robin J., Pröls Reinhard, Pröschel Marlene, Dietz Franziska, Hückelhoven Ralph, Voll Lars M., Reduced Carbohydrate Availability Enhances the Susceptibility of Arabidopsis toward Colletotrichum higginsianum, 10.1104/pp.112.209676
  30. Febvay G�rard, Liadouze Isabelle, Guillaud Josette, Bonnot Guy, Analysis of energetic amino acid metabolism inAcyrthosiphon pisum: A multidimensional approach to amino acid metabolism in aphids, 10.1002/arch.940290106
  31. Febvay G, Rahbé Y, Rynkiewicz M et al (1999) Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. J Exp Biol 202:2639–2652
  32. Fereres Alberto, Moreno Aranzazu, Behavioural aspects influencing plant virus transmission by homopteran insects, 10.1016/j.virusres.2008.10.020
  33. Fereres A, Araya JE, Housley TL, Foster JE (1990) Carbohydrate composition of wheat infected with Barley yellow dwarf virus. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-J Plant Dis Prot 97:600–608
  34. Fiebig M., Poehling H.-M., Borgemeister C., Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions, 10.1111/j.0013-8703.2004.00115.x
  35. Finke Deborah L., Contrasting the consumptive and non-consumptive cascading effects of natural enemies on vector-borne pathogens : Predator effects on vector-borne pathogens, 10.1111/j.1570-7458.2012.01258.x
  36. Firlej Annabelle, Lucas Éric, Coderre Daniel, Boivin Guy, Impact of host behavioral defenses on parasitization efficacy of a larval and adult parasitoid, 10.1007/s10526-009-9262-5
  37. Flick Andrew J., Acevedo Miguel A., Elderd Bret D., The negative effects of pathogen-infected prey on predators: a meta-analysis, 10.1111/oik.03458
  38. FORAY VINCENT, PELISSON PIERRE-FRANCOIS, BEL-VENNER MARIE-CLAUDE, DESOUHANT EMMANUEL, VENNER SAMUEL, MENU FREDERIC, GIRON DAVID, REY BENJAMIN, A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited, 10.1111/j.1365-3032.2012.00831.x
  39. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton
  40. GOODMAN P. J., WATSON M. A., HILL A. R. C., Sugar and fructosan accumulation in virus-infected plants: rapid testing by circular-paper chromatography, 10.1111/j.1744-7348.1965.tb01216.x
  41. Hajek Ann E., van Nouhuys Saskya, Fatal diseases and parasitoids: from competition to facilitation in a shared host, 10.1098/rspb.2016.0154
  42. Harvey Jeffrey A., Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity, 10.1111/j.1570-7458.2005.00348.x
  43. Harvey Jeffrey A., Gols Rieta, Development of Mamestra brassicae and its solitary endoparasitoid Microplitis mediator on two populations of the invasive weed Bunias orientalis, 10.1007/s10144-011-0267-4
  44. Harvey Jeffrey A., Gols Rieta, Effects of plant-mediated differences in host quality on the development of two related endoparasitoids with different host-utilization strategies, 10.1016/j.jinsphys.2018.03.006
  45. Harvey Jeffrey A., Gumovsky Alex, Gols Rieta, Effect of host-cocoon mass on adult size in the secondary hyperparasitoid wasp, Pteromalus semotus (Hymenoptera: Pteromalidae) : Development in a secondary hyperparasitoid, 10.1111/j.1744-7917.2011.01475.x
  46. Herbers K., Takahata Y., Melzer M., Mock H.-P., Hajirezaei M., Sonnewald U., Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco, 10.1046/j.1364-3703.2000.00007.x
  47. HEUVEL J. F. J. M. VAN DEN, PETERS D., Transmission of potato leafroll virus in relation to the honeydew excretion of Myzus persicae, 10.1111/j.1744-7348.1990.tb06632.x
  48. Hodge Simon, Powell Glen, Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection, 10.1007/s00442-008-1083-1
  49. Hodge Simon, Hardie Jim, Powell Glen, Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector, 10.1111/j.1461-9563.2010.00493.x
  50. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top down forces in natural communities. Ecology 73:24–732
  51. Ismail Mohannad, Compton Stephen G., Brooks Margot, Interaction between temperature and water nutrient levels on the fitness of Eccritotarsus catarinensis (Hemiptera: Miridae), a biological control agent of water hyacinth, 10.1016/j.biocontrol.2017.01.001
  52. Jang E. B., Messing R. H., Klungness L. M., Carvalho L. A., 10.1023/a:1007811602140
  53. Jeger M.J., Chen Z., Powell G., Hodge S., van den Bosch F., Interactions in a host plant-virus–vector–parasitoid system: Modelling the consequences for virus transmission and disease dynamics, 10.1016/j.virusres.2011.04.027
  54. Jensen Stanley G., Metabolism and Carbohydrate Composition in Barley Yellow Dwarf Virus-Infected Wheat, 10.1094/phyto-62-587
  55. Jiménez Jaime, Tjallingii W. Fred, Moreno Aránzazu, Fereres Alberto, Newly Distinguished Cell Punctures Associated with Transmission of the Semipersistent Phloem-Limited Beet Yellows Virus, 10.1128/jvi.01076-18
  56. Jiménez-Martínez Edgardo S., Bosque-Pérez Nilsa A., Life history of the bird cherry-oat aphid,Rhopalosiphum padi, on transgenic and non-transformed wheat challenged with Wheat streak mosaic virus, 10.1111/j.1570-7458.2009.00905.x
  58. Kaplan Ian, Carrillo Juli, Garvey Michael, Ode Paul J, Indirect plant–parasitoid interactions mediated by changes in herbivore physiology, 10.1016/j.cois.2016.03.004
  59. Kassanis B., Some Effects of Sucrose and Phosphorus in increasing the Multiplication of Tobacco Mosaic Virus in detached Tobacco Leaves, 10.1099/00221287-9-3-467
  60. Knight Tiffany M., McCoy Michael W., Chase Jonathan M., McCoy Krista A., Holt Robert D., Trophic cascades across ecosystems, 10.1038/nature03962
  61. Li S., Falabella P., Giannantonio S., Fanti P., Battaglia D., Digilio M.C., Völkl W., Sloggett J.J., Weisser W., Pennacchio F., Pea aphid clonal resistance to the endophagous parasitoid Aphidius ervi, 10.1016/s0022-1910(02)00176-2
  62. Lohaus Gertrud, Schwerdtfeger Michael, Comparison of Sugars, Iridoid Glycosides and Amino Acids in Nectar and Phloem Sap of Maurandya barclayana, Lophospermum erubescens, and Brassica napus, 10.1371/journal.pone.0087689
  63. Lohaus Gertrud, Winter Heike, Riens Burgi, Heldt H. W., Further Studies of the Phloem Loading Process in Leaves of Barley and Spinach. The Comparison of Metabolite Concentrations in the Apoplastic Compartment with those in the Cytosolic Compartment and in the Sieve Tubes1, 10.1111/j.1438-8677.1995.tb00860.x
  65. Magyarosy A. C., Mittler T. E., Aphid feeding rates on healthy and beet curly top virus-infected plants, 10.1007/bf02979549
  66. Markkula M, Laurema S (1964) Changes in concentration of free amino acids in plants induced by virus diseases and the reproduction of aphids. Ann Bot Fenn 3:265–271
  67. Mauck Kerry E., De Moraes Consuelo M., Mescher Mark C., Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts, 10.1073/pnas.0907191107
  68. Mauck Kerry, Bosque-Pérez Nilsa A., Eigenbrode Sanford D., De Moraes Consuelo M., Mescher Mark C., Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses, 10.1111/j.1365-2435.2012.02026.x
  69. Mauck Kerry E., De Moraes Consuelo M., Mescher Mark C., Infection of host plants by Cucumber mosaic virus increases the susceptibility of Myzus persicae aphids to the parasitoid Aphidius colemani, 10.1038/srep10963
  70. Clavijo McCormick Andrea, Unsicker Sybille B., Gershenzon Jonathan, The specificity of herbivore-induced plant volatiles in attracting herbivore enemies, 10.1016/j.tplants.2012.03.012
  71. Joffrey Moiroux, Chesnais Quentin, Spicher Fabien, Verrier Elise, Ameline Arnaud, Couty Aude, Plant virus infection influences bottom-up regulation of a plant-aphid-parasitoid system, 10.1007/s10340-017-0911-7
  72. Nemec V, Stary P (1985) Population diversity in deuterotokous Lysiphlebus species, parasitoids of aphids (Hymenoptera: Aphidiidae). Acta Entomol Bohem 82:170–174
  73. Ng James C. K., Falk Bryce W., Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses, 10.1146/annurev.phyto.44.070505.143325
  74. Ode Paul J., PLANT CHEMISTRY AND NATURAL ENEMY FITNESS: Effects on Herbivore and Natural Enemy Interactions, 10.1146/annurev.ento.51.110104.151110
  75. Park Jungan, Kim Soyeon, Choi Eunseok, Auh Chung-Kyun, Park Jong-Bum, Kim Dong-Giun, Chung Young-Jae, Lee Taek-Kyun, Lee Sukchan, Altered invertase activities of symptomatic tissues on Beet severe curly top virus (BSCTV) infected Arabidopsis thaliana, 10.1007/s10265-013-0562-6
  76. PESCOD K. V., QUICK W. P., DOUGLAS A. E., Aphid responses to plants with genetically manipulated phloem nutrient levels, 10.1111/j.1365-3032.2007.00577.x
  77. Pierre Jean-Sebastien, Masson Jean-Pierre, Wajnberg Eric, Patch leaving rules: A stochastic version of a well-known deterministic motivational model, 10.1016/j.jtbi.2012.08.003
  78. Poelman EH, Dicke M (2014) Plant-mediated interactions among insects within a community ecological perspective. In: Annual plant reviews. Insect‐plant interactions, vol 47. Wiley, Oxford, UK, pp 309–338
  79. Price Peter W., The Plant Vigor Hypothesis and Herbivore Attack, 10.2307/3545270
  80. Price P W, Bouton C E, Gross P, McPheron B A, Thompson J N, Weis A E, Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies, 10.1146/
  81. Rasekh Arash, Michaud J. P., Allahyari Hossein, Sabahi Qodratollah, The Foraging Behavior of Lysiphlebus fabarum (Marshall), a Thelytokous Parasitoid of the Black Bean Aphid in Iran, 10.1007/s10905-010-9201-4
  82. Rasekh Arash, Michaud J.P., Kharazi-Pakdel Aziz, Allahyari Hossein, Ant Mimicry by an Aphid Parasitoid,Lysiphlebus fabarum, 10.1673/031.010.12601
  83. Riens Burgi, Lohaus Gertrud, Heineke Dieter, Heldt Hans Walter, Amino Acid and Sucrose Content Determined in the Cytosolic, Chloroplastic, and Vacuolar Compartments and in the Phloem Sap of Spinach Leaves, 10.1104/pp.97.1.227
  84. Russell Calum W., Poliakov Anton, Haribal Meena, Jander Georg, van Wijk Klaas J., Douglas Angela E., Matching the supply of bacterial nutrients to the nutritional demand of the animal host, 10.1098/rspb.2014.1163
  85. SARFRAZ Rana M., DOSDALL Lloyd M., KEDDIE Andrew B., Bottom-up effects of host plant nutritional quality on Plutella xylostella (Lepidoptera: Plutellidae) and top-down effects of herbivore attack on plant compensatory ability, 10.14411/eje.2009.073
  86. Sasaki Tetsuhiko, Ishikawa Hajime, Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum, 10.1016/0022-1910(94)00080-z
  87. SELMAN I. W., BRIERLEY M. R., PEGG G. F., HILL T. A., Changes in the free amino acids and amides in tomato plants inoculated with tomato spotted wilt virus, 10.1111/j.1744-7348.1961.tb03657.x
  88. Sequeira R., Mackauer M., Covariance of adult size and development time in the parasitoid waspAphidius ervi in relation to the size of its host,Acyrthosiphon pisum, 10.1007/bf02285332
  89. Sequeira R., MacKauer M., Seasonal Variation in Body Size and Offspring Sex Ratio in Field Populations of the Parasitoid Wasp, Aphidius ervi (Hymenoptera: Aphidiidae), 10.2307/3544848
  90. SHAW M. J. P., Effects of population density on alienicolae of Aphis fabae Scop.: The expression of migratory urge among alatae in the field, 10.1111/j.1744-7348.1973.tb07716.x
  91. SMITH HELEN G., HALLSWORTH PHILIPPA B., The effects of yellowing viruses on yield of sugar beet in field trials, 1985 and 1987, 10.1111/j.1744-7348.1990.tb06633.x
  92. Srinivasan Rajagopalbabu, Alvarez Juan M., Bosque-Pérez Nilsa A., Eigenbrode Sanford D., Novy Richard G., Effect of an Alternate Weed Host, Hairy Nightshade, Solanum sarrachoides, on the Biology of the Two Most Important Potato Leafroll Virus (Luteoviridae: Polerovirus) Vectors, Myzus persicae and Macrosiphum euphorbiae (Aphididae: Homoptera), 10.1603/0046-225x(2008)37[592:eoaawh];2
  93. Stary P (1986) Specificity of parasitoids (Hymenoptera: Aphidiidae) to the black bean aphid Aphis fabae complex in agrosystems. Acta Entomol Bohem 83:24–29
  94. Stevens M., Hull R., Smith H.G., Comparison of ELISA and RT-PCR for the detection of beet yellows closterovirus in plants and aphids, 10.1016/s0166-0934(97)00103-1
  95. Tauzin Alexandra S., Giardina Thierry, Sucrose and invertases, a part of the plant defense response to the biotic stresses, 10.3389/fpls.2014.00293
  96. R Core Team (2018) A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0. . Accessed 15 July 2018
  97. Turlings Ted C. J., Benrey Betty, Effects of plant metabolites on the behavior and development of parasitic wasps, 10.1080/11956860.1998.11682472
  98. Van handel E (1985) Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc 1:302–304
  99. Visser Bertanne, Ellers Jacintha, Lack of lipogenesis in parasitoids: A review of physiological mechanisms and evolutionary implications, 10.1016/j.jinsphys.2008.07.014
  100. Visser J. H., Piron P. G. M., Hardie J., The aphids' peripheral perception of plant volatiles, 10.1111/j.1570-7458.1996.tb00880.x
  101. Visser B., Le Lann C., den Blanken F. J., Harvey J. A., van Alphen J. J. M., Ellers J., Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle, 10.1073/pnas.1001744107
  102. Volkl Wolfgang, Aphids or Their Parasitoids: Who Actually Benefits from Ant-Attendance?, 10.2307/5320
  103. Wajnberg Eric, Multi-objective behavioural mechanisms are adopted by foraging animals to achieve several optimality goals simultaneously : Multi-objective behaviours in parasitoids, 10.1111/j.1365-2656.2011.01926.x
  104. Wajnberg Eric, Fauvergue Xavier, Pons Odile, Patch leaving decision rules and the Marginal Value Theorem: an experimental analysis and a simulation model, 10.1093/beheco/11.6.577
  106. Weber Cheryl A., Godfrey Larry D., Mauk Peggy A., Effects of Parasitism by Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) on Transmission of Beet Yellows Closterovirus by Bean Aphid (Homoptera: Aphididae), 10.1093/jee/89.6.1431
  107. Weibull Jens, Host Plant Discrimination in the Polyphagous Aphid Rhopalosiphum padi: The Role of Leaf Anatomy and Storage Carbohydrate, 10.2307/3565936
  108. Williams Caroline M., Thomas Raymond H., MacMillan Heath A., Marshall Katie E., Sinclair Brent J., Triacylglyceride measurement in small quantities of homogenised insect tissue: Comparisons and caveats, 10.1016/j.jinsphys.2011.08.008
  109. Wu G.-M., Barrette M., Boivin G., Brodeur J., Giraldeau L.-A., Hance T., Temperature Influences the Handling Efficiency of an Aphid Parasitoid Through Body Size-Mediated Effects, 10.1603/en11018
  110. Wu Ying, Davis Thomas Seth, Eigenbrode Sanford D., Aphid behavioral responses to virus-infected plants are similar despite divergent fitness effects, 10.1111/eea.12246
Bibliographic reference Albittar, Loulou ; Ismail, Mohannad ; Lohaus, Gertrud ; Ameline, Arnaud ; Visser, Bertanne ; et. al. Bottom-up regulation of a tritrophic system by Beet yellows virus infection: consequences for aphid-parasitoid foraging behaviour and development. In: Oecologia, Vol. 191, no.1, p. 113-125 (2019)
Permanent URL