1932

Abstract

Conservation biological control aims to enhance populations of natural enemies of insect pests in crop habitats, typically by intentional provision of flowering plants as food resources. Ideally, these flowering plants should be inherently attractive to natural enemies to ensure that they are frequently visited. We review the chemical ecology of floral resources in a conservation biological control context, with a focus on insect parasitoids. We highlight the role of floral volatiles as semiochemicals that attract parasitoids to the food resources. The discovery that nectar-inhabiting microbes can be hidden players in mediating parasitoid responses to flowering plants has highlighted the complexity of the interactions between plants and parasitoids. Furthermore, because food webs in agroecosystems do not generally stop at the third trophic level, we also consider responses of hyperparasitoids to floral resources. We thus provide an overview of floral compounds as semiochemicals from a multitrophic perspective, and we focus on the remaining questions that need to be addressed to move the field forward.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-120220-124357
2023-01-23
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/ento/68/1/annurev-ento-120220-124357.html?itemId=/content/journals/10.1146/annurev-ento-120220-124357&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aartsma Y, Cusumano A, de Bobadilla MF, Rusman Q, Vosteen I, Poelman EH. 2019. Understanding insect foraging in complex habitats by comparing trophic levels: insights from specialist host-parasitoid-hyperparasitoid systems. Curr. Opin. Insect Sci. 32:54–60
    [Google Scholar]
  2. 2.
    Aizenberg-Gershtein Y, Izhaki I, Halpern M. 2013. Do honeybees shape the bacterial community composition in floral nectar?. PLOS ONE 8:e67556
    [Google Scholar]
  3. 3.
    Álvarez-Pérez S, Herrera CM, de Vega C. 2012. Zooming-in on floral nectar: a first exploration of nectar associated bacteria in wild plant communities. FEMS Microbiol. Ecol. 80:591–602
    [Google Scholar]
  4. 4.
    Araj SE, Wratten S, Lister A, Buckley H. 2008. Floral diversity, parasitoids and hyperparasitoids—a laboratory approach. Basic Appl. Ecol. 9:588–97
    [Google Scholar]
  5. 5.
    Araj SE, Wratten S, Lister A, Buckley H. 2009. Adding floral nectar resources to improve biological control: potential pitfalls of the fourth trophic level. Basic Appl. Ecol. 10:554–62
    [Google Scholar]
  6. 6.
    Araj SE, Wratten S, Lister A, Buckley H, Ghabeish I. 2011. Searching behavior of an aphid parasitoid and its hyperparasitoid with and without floral nectar. Biol. Control 57:79–84
    [Google Scholar]
  7. 7.
    Ayelo PM, Pirk CWW, Yusuf AA, Chailleux A, Mohamed SA, Deletre E. 2021. Exploring the kairomone-based foraging behaviour of natural enemies to enhance biological control: a review. Front. Ecol. Evol. 9:641974
    [Google Scholar]
  8. 8.
    Baker HG, Baker I 1983. A brief historical review of the chemistry of floral nectar. The Biology of Nectaries B Bentley, T Elias 126–52 New York: Columbia Univ. Press
    [Google Scholar]
  9. 9.
    Barloggio G, Tamm L, Nagel P, Luka H. 2019. Selective flowers to attract and enhance Telenomus laeviceps (Hymenoptera: Scelionidae): a released biocontrol agent of Mamestra brassicae (Lepidoptera: Noctuidae). Bull. Entomol. Res. 109:160–68
    [Google Scholar]
  10. 10.
    Belz E, Kölliker M, Balmer O. 2013. Olfactory attractiveness of flowering plants to the parasitoid Microplitis mediator: potential implications for biological control. BioControl 58:163–73
    [Google Scholar]
  11. 11.
    Berndt LA, Wratten SD. 2005. Effects of alyssum flowers on the longevity, fecundity, and sex ratio of the leafroller parasitoid Dolichogenidea tasmanica. Biol. Control 32:65–69
    [Google Scholar]
  12. 12.
    Bianchi FJ, Wäckers FL. 2008. Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids. Biol. Control 46:400–8
    [Google Scholar]
  13. 13.
    Bloemhard CM, Wielen M, Messelink GJ. 2014. Seasonal abundance of aphid hyperparasitoids in organic greenhouse crops in the Netherlands. IOBC/WPRS Bull 102:15–19
    [Google Scholar]
  14. 14.
    Brysch-Herzberg M. 2004. Ecology of yeasts in plant bumblebee mutualism in Central Europe. FEMS Microbiol. Ecol. 50:87–100
    [Google Scholar]
  15. 15.
    Canto A, Herrera CM. 2012. Micro-organisms behind the pollination scenes: microbial imprint on floral nectar sugar variation in a tropical plant community. Ann. Bot. 110:1173–83
    [Google Scholar]
  16. 16.
    Cardé RT, Millar JG, eds. 2004. Advances in Insect Chemical Ecology Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  17. 17.
    Chen Y, Mao J, Reynolds OL, Chen W, He W et al. 2020. Alyssum (Lobularia maritima) selectively attracts and enhances the performance of Cotesia vestalis, a parasitoid of Plutella xylostella. Sci. Rep. 10:6447
    [Google Scholar]
  18. 18.
    Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF et al. 2013. Herbivore exploits orally secreted bacteria to suppress plant defenses. PNAS 110:15728–33
    [Google Scholar]
  19. 19.
    Colazza S, Cusumano A, Giudice DL, Peri E 2014. Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59:1–17
    [Google Scholar]
  20. 20.
    Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F 2004. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207:47–53
    [Google Scholar]
  21. 21.
    Colazza S, McElfresh JS, Millar JG. 2004. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30:945–64
    [Google Scholar]
  22. 22.
    Cray JA, Bell ANW, Bhaganna P, Mswaka AY, Timson DJ, Hallsworth JE. 2013. The biology of habitat dominance: Can microbes behave as weeds?. Microb. Biotechnol. 6:453–92
    [Google Scholar]
  23. 23.
    Cusumano A, Harvey JA, Bourne ME, Poelman EH, de Boer JG. 2020. Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests. Pest Manag. Sci. 76:432–43
    [Google Scholar]
  24. 24.
    Cusumano A, Volkoff AN. 2021. Influence of parasitoid-associated viral symbionts on plant-insect interactions and biological control. Curr. Opin. Insect Sci. 44:64–71
    [Google Scholar]
  25. 25.
    Cusumano A, Zhu F, Volkoff AN, Verbaarschot P, Bloem J et al. 2018. Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores. Ecol. Lett. 21:957–67
    [Google Scholar]
  26. 26.
    Dharampal PS, Carlson C, Currie CR, Steffan SA. 2019. Pollen-borne microbes shape bee fitness. Proc. R. Soc. B 286:190420182894
    [Google Scholar]
  27. 27.
    Dharampal PS, Hetherington MC, Steffan SA. 2020. Microbes make the meal: Oligolectic bees require microbes within their host pollen to thrive. Ecol. Entomol. 45:1418–27
    [Google Scholar]
  28. 28.
    Dicke M, Cusumano A, Poelman EH. 2020. Microbial symbionts of parasitoids. Annu. Rev. Entomol. 65:171–90
    [Google Scholar]
  29. 29.
    Dobson HE. 2017. Floral volatiles in insect biology. Insect-Plant Interactions EA Bernays 3–36 Boca Raton, FL: CRC Press
    [Google Scholar]
  30. 30.
    Douglas AE. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17–34
    [Google Scholar]
  31. 31.
    Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–68
    [Google Scholar]
  32. 32.
    Eichhorn O. 1996. Experimental studies upon the parasitoid complex of the gypsy moth (Lymantria dispar L.) (Lep., Lymantriidae) in lower host populations in eastern Austria. J. Appl. Entomol. 120:205–12
    [Google Scholar]
  33. 33.
    Fand BB, Amala U, Yadav DS, Rathi G, Mhaske SH et al. 2020. Bacterial volatiles from mealybug honeydew exhibit kairomonal activity toward solitary endoparasitoid Anagyrus dactylopii. J. Pest Sci. 93:195–206
    [Google Scholar]
  34. 34.
    Fataar S, Kahmen A, Luka H. 2019. Innate and learned olfactory attraction to flowering plants by the parasitoid Cotesia rubecula (Marshall, 1885) (Hymenoptera: Braconidae): potential impacts on conservation biological control. Biol. Control 132:16–22
    [Google Scholar]
  35. 35.
    Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19:677–89
    [Google Scholar]
  36. 36.
    Fatouros NE, Van Loon JJA, Hordijk KA, Smid HM, Dicke M. 2005. Herbivore-induced plant volatiles mediate in-flight host discrimination by parasitoids. J. Chem. Ecol. 31:2033–47
    [Google Scholar]
  37. 37.
    Foti MC, Peri E, Wajnberg E, Colazza S, Rostás M 2019. Contrasting olfactory responses of two egg parasitoids to buckwheat floral scent are reflected in field parasitism rates. J. Pest Sci. 92:747–56
    [Google Scholar]
  38. 38.
    Foti MC, Rostás M, Peri E, Park KC, Slimani T et al. 2017. Chemical ecology meets conservation biological control: identifying plant volatiles as predictors of floral resource suitability for an egg parasitoid of stink bugs. J. Pest Sci. 90:299–310
    [Google Scholar]
  39. 39.
    Frago E. 2016. Interactions between parasitoids and higher order natural enemies: intraguild predation and hyperparasitoids. Curr. Opin. Insect Sci. 14:81–86
    [Google Scholar]
  40. 40.
    Fridman S, Izhaki I, Gerchman Y, Halpern M. 2012. Bacterial communities in floral nectar. Environ. Microbiol. Rep. 4:97–104
    [Google Scholar]
  41. 41.
    Furlong MJ, Ang GC, Silva R, Zalucki MP. 2018. Bringing ecology back: How can the chemistry of indirect plant defenses against herbivory be manipulated to improve pest management?. Front. Plant Sci. 9:1436
    [Google Scholar]
  42. 42.
    Garcia MA, Sanz J. 2001. Analysis of Origanum vulgare volatiles by direct thermal desorption coupled to gas chromatography-mass spectrometry. J. Chromatogr. 918:189–94
    [Google Scholar]
  43. 43.
    Géneau CE, Wäckers FL, Luka H, Balmer O. 2013. Effects of extrafloral and floral nectar of Centaurea cyanus on the parasitoid wasp Microplitis mediator: olfactory attractiveness and parasitization rates. Biol. Control 66:16–20
    [Google Scholar]
  44. 44.
    Géneau CE, Wäckers FL, Luka H, Daniel C, Balmer O. 2012. Selective flowers to enhance biological control of cabbage pests by parasitoids. Basic Appl. Ecol. 13:85–93
    [Google Scholar]
  45. 45.
    Giron D, Dedeine F, Dubreuil G, Huguet E, Mouton L et al. 2017. Influence of microbial symbionts on plant–insect interactions. Adv. Bot. Res. 81:225–57
    [Google Scholar]
  46. 46.
    Goelen T, Baets D, Kos M, Paulussen C, Lenaerts M et al. 2018. Gustatory response and longevity in Aphidius parasitoids and their hyperparasitoid Dendrocerus aphidum. J. Pest Sci. 91:351–60
    [Google Scholar]
  47. 47.
    Goelen T, Sobhy IS, Vanderaa C, de Boer JG, Delvigne F et al. 2019. Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid. Funct. Ecol. 34:507–20
    [Google Scholar]
  48. 48.
    Goelen T, Sobhy IS, Vanderaa C, Wäckers F, Rediers H et al. 2020. Bacterial phylogeny predicts volatile organic compound composition and olfactory response of an aphid parasitoid. Oikos 129:1415–28
    [Google Scholar]
  49. 49.
    Golonka AM, Johnson BO, Freeman J, Hinson DW. 2014. Impact of nectarivorous yeasts on Silene caroliniana’s scent. East. Biol. 3:1–26
    [Google Scholar]
  50. 50.
    Gómez-Marco F, Urbaneja A, Jaques JA, Rugman-Jones PF, Stouthamer R, Tena A. 2015. Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control?. Biol. Control 81:111–21
    [Google Scholar]
  51. 51.
    Good AP, Gauthier L-PL, Vannette RL, Fukami T. 2014. Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PLOS ONE 9:e86494
    [Google Scholar]
  52. 52.
    Gurr GM, Wratten SD, Landis DA, You M. 2017. Habitat management to suppress pest populations: progress and prospects. Annu. Rev. Entomol. 62:91–109
    [Google Scholar]
  53. 53.
    Haverkamp A, Smid HM. 2020. A neuronal arms race: the role of learning in parasitoid-host interactions. Curr. Opin. Insect Sci. Sep 42:47–54
    [Google Scholar]
  54. 54.
    Heimpel GE, Jervis MA 2005. Does floral nectar improve biological control by parasitoids?. Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and Its Applications FL Wäckers, PCJ van Rijn, J Bruin 267–304 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  55. 55.
    Herrera CM, de Vega C, Canto A, Pozo MI. 2009. Yeasts in floral nectar: a quantitative survey. Ann. Bot. 103:1415–23
    [Google Scholar]
  56. 56.
    Herrera CM, García IM, Pérez R. 2008. Invisible floral larcenies: Microbial communities degrade floral nectar of bumble bee-pollinated plants. Ecology 89:2369–76
    [Google Scholar]
  57. 57.
    Höller C, Micha SG, Schulz S, Francke W, Pickett JA. 1994. Enemy-induced dispersal in a parasitic wasp. Experientia 50:182–85
    [Google Scholar]
  58. 58.
    Holt RD, Hochberg ME. 1998. The coexistence of competing parasites. Part II—hyperparasitism and food chain dynamics. J. Theor. Biol. 193:485–95
    [Google Scholar]
  59. 59.
    Irvin NA, Hoddle MS. 2007. Evaluation of floral resources for enhancement of fitness of Gonatocerus ashmeadi, an egg parasitoid of the glassy-winged sharpshooter, Homalodisca vitripennis. Biol. Control 40:80–88
    [Google Scholar]
  60. 60.
    Jacquemyn H, Lenaerts M, Brys R, Willems KA, Lievens B. 2013. Among-population variation in microbial community structure in the floral nectar of the bee pollinated forest herb Pulmonaria officinalis L. PLOS ONE 8:e56917
    [Google Scholar]
  61. 61.
    Jacquemyn H, Lenaerts M, Tyteca D, Lievens B. 2013. Microbial diversity in the floral nectar of seven Epipactis (Orchidaceae) species. Microbiol. Open 2:644–58
    [Google Scholar]
  62. 62.
    Jado RH, Araj SE, Abu-Irmaileh B, Shields MW, Wratten SD. 2019. Floral resources to enhance the potential of the parasitoid Aphidius colemani for biological control of the aphid Myzus persicae. J. Appl. Entomol. 143:34–42
    [Google Scholar]
  63. 63.
    Jervis MA, Kidd NEC, Fitton MG, Huddleston T, Dawah HA. 1993. Flower-visiting by hymenopteran parasitoids. J. Nat. Hist. 27:67–105
    [Google Scholar]
  64. 64.
    Kafle BD, Morawo T, Fadamiro H. 2020. Host-induced plant volatiles mediate ability of the parasitoid Microplitis croceipes to discriminate between unparasitized and parasitized Heliothis virescens larvae and avoid superparasitism. J. Chem. Ecol. 46:967–77
    [Google Scholar]
  65. 65.
    Kaiser L, Ode P, van Nouhuys S, Calatayud PA, Colazza S et al. 2017. The plant as a habitat for entomophagous insects. Adv. Bot. Res. 81:179–223
    [Google Scholar]
  66. 66.
    Karp DS, Chaplin-Kramer R, Meehan TD, Martin EA, DeClerck F et al. 2018. Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. PNAS 115:E7863–70
    [Google Scholar]
  67. 67.
    Klaps J, Lievens B, Álvarez-Pérez S. 2020. Towards a better understanding of the role of nectar-inhabiting yeasts in plant–animal interactions. Fungal Biol. Biotech. 7:1
    [Google Scholar]
  68. 68.
    Knudsen JT, Tollsten L, Bergstrom LG. 1993. Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–80
    [Google Scholar]
  69. 69.
    Kugimiya S, Uefune M, Shimoda T, Takabayashi J. 2010. Orientation of the parasitic wasp, Cotesia vestalis (Haliday) (Hymenoptera: Braconidae), to visual and olfactory cues of field mustard flowers, Brassica rapa L. (Brassicaceae), to exploit food sources. Appl. Entomol. Zool. 45:369–75
    [Google Scholar]
  70. 70.
    Landis DA, Wratten SD, Gurr GM. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45:175–201
    [Google Scholar]
  71. 71.
    Lee JC, Heimpel GE. 2008. Floral resources impact longevity and oviposition rate of a parasitoid in the field. J. Anim. Ecol. 77:565–72
    [Google Scholar]
  72. 72.
    Lenaerts M, Goelen T, Paulussen C, Herrera-Malaver B, Steensels J et al. 2017. Nectar bacteria affect life history of a generalist aphid parasitoid by altering nectar chemistry. Funct. Ecol. 31:2061–69
    [Google Scholar]
  73. 73.
    Lenaerts M, Pozo MI, Wäckers F, Van den Ende W, Jacquemyn H, Lievens B. 2016. Impact of microbial communities on floral nectar chemistry: potential implications for biological control of pest insects. Basic Appl. Ecol. 17:189–98
    [Google Scholar]
  74. 74.
    Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G et al. 2011. Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat. Commun. 2:348
    [Google Scholar]
  75. 75.
    Lievens B, Hallsworth JE, Pozo MI, Belgacem ZB, Stevenson A et al. 2015. Microbiology of sugar-rich environments: diversity, ecology and system constraints. Environ. Microbiol. 17:278–98
    [Google Scholar]
  76. 76.
    Miall JH, Abram PK, Cappuccino N, Bennett AM, Fernández-Triana JL et al. 2021. Addition of nectar sources affects a parasitoid community without improving pest suppression. J. Pest Sci. 94:335–47
    [Google Scholar]
  77. 77.
    Nafziger JTD, Fadamiro HY. 2011. Suitability of some farmscaping plants as nectar sources for the parasitoid wasp, Microplitis croceipes (Hymenoptera: Braconidae): effects on longevity and body nutrients. Biol. Control 56:225–29
    [Google Scholar]
  78. 78.
    Nagasaka K, Takahasi N, Okabayashi T. 2010. Impact of secondary parasitism on Aphidius colemani in the banker plant system on aphid control in commercial greenhouses in Kochi, Japan. Appl. Entomol. Zool. 45:541–50
    [Google Scholar]
  79. 79.
    Nepi M. 2014. Beyond nectar sweetness: the hidden ecological role of non-protein amino acids in nectar. J. Ecol. 102:108–15
    [Google Scholar]
  80. 80.
    Nicolson SW, Thornburg RW 2007. Nectar chemistry. Nectaries and Nectar SW Nicolson, M Nepi, E Pacini 215–64 Berlin: Springer
    [Google Scholar]
  81. 81.
    Olson DM, Rains GC, Meiners T, Takasu K, Tertuliano M et al. 2003. Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors. Chem. Senses 28:545–49
    [Google Scholar]
  82. 82.
    Olson DM, Wäckers FL. 2007. Management of field margins to maximize multiple ecological services. J. Appl. Ecol. 44:13–21
    [Google Scholar]
  83. 83.
    Oren A, Hallsworth JE. 2014. Microbial weeds in hypersaline habitats: the enigma of the weed-like Haloferax mediterranei. FEMS Microbiol. Lett. 359:134–42
    [Google Scholar]
  84. 84.
    Peay KG, Belisle M, Fukami T. 2012. Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proc. Biol. Sci. 279:749–58
    [Google Scholar]
  85. 85.
    Peri E, Moujahed R, Wajnberg E, Colazza S 2018. Applied chemical ecology to enhance insect parasitoid efficacy in the biological control of crop pests. Chemical Ecology of Insects: Applications and Associations with Plants and Microbes J Tabata 234–67 Boca Raton, FL: CRC Press
    [Google Scholar]
  86. 86.
    Petersen G, Matthiesen C, Francke W, Wyss U. 2000. Hyperparasitoid volatiles as possible foraging behaviour determinants in the aphid parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiidae). Eur. J. Entomol. 97:545–50
    [Google Scholar]
  87. 87.
    Pineda A, Zheng SJ, van Loon JJ, Pieterse CM, Dicke M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–14
    [Google Scholar]
  88. 88.
    Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE et al. 2012. Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLOS Biol 10:e1001435
    [Google Scholar]
  89. 89.
    Poelman EH, Cusumano A, de Boer JG. 2021. The ecology of hyperparasitoids. Annu. Rev. Entomol. 67:143–61
    [Google Scholar]
  90. 90.
    Pozo MI, Herrera CM, Bazaga P. 2011. Species richness of yeast communities in floral nectar of southern Spanish plants. Microb. Ecol. 61:82–91
    [Google Scholar]
  91. 91.
    Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69
    [Google Scholar]
  92. 92.
    Rering CC, Beck JJ, Hall GW, McCartney MM, Vannette RL. 2018. Nectar-inhabiting microorganisms influence nectar volatile composition and attractiveness to a generalist pollinator. New Phytol 220:750–59
    [Google Scholar]
  93. 93.
    Rering CC, Vannette RL, Schaeffer RN, Beck JJ. 2020. Microbial co-occurrence in floral nectar affects metabolites and attractiveness to a generalist pollinator. J. Chem. Ecol. 46:659–67
    [Google Scholar]
  94. 94.
    Rohrig E, Sivinski J, Holler T. 2008. Comparison of parasitic Hymenoptera captured in malaise traps baited with two flowering plants, Lobularia maritima (Brassicales, Brassicaceae) and Spermacoce verticillata (Gentianales, Rubiaceae). Fla. Entomol. 91:621–27
    [Google Scholar]
  95. 95.
    Root RB. 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol. Monogr. 43:95–124
    [Google Scholar]
  96. 96.
    Russell AL, Ashman T-L. 2019. Associative learning of flowers by generalist bumble bees can be mediated by microbes on the petals. Behav. Ecol. 30:746–55
    [Google Scholar]
  97. 97.
    Schaeffer RN, Rering CC, Maalouf I, Beck JJ, Vannette RL. 2019. Microbial metabolites elicit distinct olfactory and gustatory preferences in bumblebees. Biol. Lett. 15:20190132
    [Google Scholar]
  98. 98.
    Shackelford G, Steward PR, Benton TG, Kunin WE, Potts SG et al. 2013. Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol. Rev. 88:1002–21
    [Google Scholar]
  99. 99.
    Shade A, McManus PS, Handelsman J 2013. Unexpected diversity during community succession in the apple flower microbiome. MBio 4:e00602–12
    [Google Scholar]
  100. 100.
    Shields MW, Johnson AC, Pandey S, Cullen R, González-Chang M et al. 2019. History, current situation and challenges for conservation biological control. Biol. Control 131:25–35
    [Google Scholar]
  101. 101.
    Shikano I, Rosa C, Tan CW, Felton GW. 2017. Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu. Rev. Phytopathol. 55:313–31
    [Google Scholar]
  102. 102.
    Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG et al. 2011. Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J. Appl. Ecol. 48:580–90
    [Google Scholar]
  103. 103.
    Smid HM, Vet LEM. 2016. The complexity of learning, memory and neural processes in an evolutionary ecological context. Curr. Opin. Insect Sci. 15:61–69
    [Google Scholar]
  104. 104.
    Sobhy IS, Baets D, Goelen T, Herrera-Malaver B, Bosmans L et al. 2018. Sweet scents: Nectar specialist yeasts enhance nectar attraction of a generalist aphid parasitoid without affecting survival. Front. Plant Sci. 9:1009
    [Google Scholar]
  105. 105.
    Sobhy IS, Goelen T, Herrera-Malaver B, Verstrepen KJ, Wäckers F et al. 2019. Associative learning and memory retention of nectar yeast volatiles in a generalist parasitoid. Anim. Behav. 153:137–46
    [Google Scholar]
  106. 106.
    Srinatha HS, Jalali SK, Sriram S, Chakravarthy AK. 2015. Isolation of microbes associated with field-collected populations of the egg parasitoid, Trichogramma chilonis capable of enhancing biotic fitness. Biocontrol Sci. Technol. 25:789–802
    [Google Scholar]
  107. 107.
    Steppuhn A, Wäckers FL. 2004. HPLC sugar analysis reveals the nutritional state and the feeding history of parasitoids. Funct. Ecol. 18:812–19
    [Google Scholar]
  108. 108.
    Takasu K, Lewis WJ. 1995. Importance of adult food sources to host searching of the larval parasitoid Microplitis croceipes. Biol. Control 5:25–30
    [Google Scholar]
  109. 109.
    Takasu K, Lewis WJ. 1996. The role of learning in adult food location by the larval parasitoid, Microplitis croceipes. J. Insect Behav. 9:265–81
    [Google Scholar]
  110. 110.
    Tougeron K, Tena A. 2019. Hyperparasitoids as new targets in biological control in a global change context. Biol. Control 130:164–71
    [Google Scholar]
  111. 111.
    Tucker CM, Fukami T. 2014. Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes. Proc. Biol. Sci. 281:20132637
    [Google Scholar]
  112. 112.
    Turlings TC, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63:433–52
    [Google Scholar]
  113. 113.
    van Nouhuys S, Hanski I. 2000. Apparent competition between parasitoids mediated by a shared hyperparasitoid. Ecol. Lett. 3:82–84
    [Google Scholar]
  114. 114.
    van Rijn PC, Wäckers FL. 2016. Nectar accessibility determines fitness, flower choice and abundance of hoverflies that provide natural pest control. J. Appl. Ecol. 53:925–33
    [Google Scholar]
  115. 115.
    Vannette RL. 2020. The floral microbiome: plant, pollinator, and microbial perspectives. Annu. Rev. Ecol. Evol. Syst. 51:363–86
    [Google Scholar]
  116. 116.
    Vannette RL, Fukami T. 2018. Contrasting effects of yeasts and bacteria on floral nectar traits. Ann. Bot. 121:1343–49
    [Google Scholar]
  117. 117.
    Vannette RL, Gauthier M-PL, Fukami T. 2013. Nectar bacteria, but not yeast, weaken a plant-pollinator mutualism. Proc. R. Soc. B 280:20122601
    [Google Scholar]
  118. 118.
    von Arx M, Moore A, Davidowitz G, Arnold AE. 2019. Diversity and distribution of microbial communities in floral nectar of two night-blooming plants of the Sonoran Desert. PLOS ONE 14:e0225309
    [Google Scholar]
  119. 119.
    Wäckers FL. 2001. A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata. J. Insect Physiol. 47:1077–84
    [Google Scholar]
  120. 120.
    Wäckers FL. 2004. Assessing the suitability of flowering herbs as parasitoid food sources: flower attractiveness and nectar accessibility. Biol. Control 29:307–14
    [Google Scholar]
  121. 121.
    Wäckers FL, Bonifay C, Lewis WJ. 2002. Conditioning of appetitive behavior in the Hymenopteran parasitoid Microplitis croceipes. Entomol. Exp. Appl. 103:135–38
    [Google Scholar]
  122. 122.
    Wäckers FL, Romeis J, van Rijn P. 2007. Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu. Rev. Entomol. 52:301–23
    [Google Scholar]
  123. 123.
    Wäckers FL, van Rijn PC 2012. Pick and mix: selecting flowering plants to meet the requirements of target biological control insects. Biodiversity and Insect Pests: Key Issues for Sustainable Management GM Gurr, SD Wratten, WE Snyder, DMY Read 139–65 Hoboken, NJ: Wiley
    [Google Scholar]
  124. 124.
    Wajnberg E, Colazza S, eds. 2013. Chemical Ecology of Insect Parasitoids Hoboken, NJ: Wiley
    [Google Scholar]
  125. 125.
    Winkler K, Wäckers F, Bukovinszkine-Kiss G, van Lenteren J. 2006. Sugar resources are vital for Diadegma semiclausum fecundity under field conditions. Basic Appl. Ecol. 7:133–40
    [Google Scholar]
  126. 126.
    Witting-Bissinger BE, Orr DB, Linker HM. 2008. Effects of floral resources on fitness of the parasitoids Trichogramma exiguum (Hymenoptera: Trichogrammatidae) and Cotesia congregata (Hymenoptera: Braconidae). Biol. Control 47:180–86
    [Google Scholar]
  127. 127.
    Zhu F, Cusumano A, Bloem J, Weldegergis BT, Villela A et al. 2018. Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids. PNAS 5:5205–10
    [Google Scholar]
  128. 128.
    Zhu F, Poelman EH, Dicke M. 2014. Insect herbivore-associated organisms affect plant responses to herbivory. New Phytol 204:315–21
    [Google Scholar]
/content/journals/10.1146/annurev-ento-120220-124357
Loading
/content/journals/10.1146/annurev-ento-120220-124357
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error