Exploring the factors involved in the absence of parasitism of Chaetosiphon fragaefolii by generalist parasitoids in strawberry

Abstract

Chaetosiphon fragaefolii Cockerell (Hemiptera: Aphididae) is a worldwide strawberry pest with scarce records of parasitoids for its control. The parasitization rate of two generalist parasitoids, Aphidius colemani Viereck and Aphidius matricariae Haliday, their behavior and aphid defensive behaviors were evaluated with Aphis gossypii Glover (Hemiptera: Aphididae) as a comparative host. Defensive endosymbionts were also surveyed. C. fragaefolii was never parasitized in simple-choice tests, whereas in preference tests both parasitoids chose A. gossypii over C. fragaefolii. No contacts of A. matricariae with C. fragaefolii were observed while A. colemani made more antennal contacts and “stings” on A. gossypii than on C. fragaefolii with the latter exhibiting less defensive behaviors against the parasitoid. The bacterium Acinetobacter sp. was detected in all samples of C. fragaefolii, but with an unknown function. Further research on the possible defensive role of the glandular hairs covering the body of this aphid, the role of chemical signals and the existence of defensive internal mechanisms against parasitoids could provide plausible explanations for the absence of parasitism found.

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References

  1. Agresti A (2015) Foundations of linear and generalized linear models. Wiley, Hoboken

    Google Scholar 

  2. Arneodo JD, Ortego J (2014) Exploring the bacterial microbiota associated with native South-American species of Aphis (Hemiptera: Aphididae). Environ Entomol 43:589–594

    CAS  Google Scholar 

  3. Bernardi D, Araujo ES, Zawadneak MA, Botton M, Mogor AF, Garcia MS (2013) Aphid species and population dynamics associated with strawberry. Neotrop Entomol 42:628–633

    CAS  Google Scholar 

  4. Cédola C, Greco N (2010) Presence of the aphid, Chaetosiphon fragaefolii, on strawberry in Argentina. J Insect Sci 10:9

    PubMed  PubMed Central  Google Scholar 

  5. Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 64(5):1297–1304

    Google Scholar 

  6. Cingolani MF, Greco N (2018) Spatio-temporal variation of strawberry aphid populations and their parasitoid. Appl Entomol Zool 53:205–214

    Google Scholar 

  7. Cross JV, Easterbrook MA, Crook AM, Crook D, Fitzgerald JD, Innocenzi PJ, Jay CN, Solomon MG (2001) Review: natural enemies and biocontrol of pests of strawberry in Northern and Central Europe. Biocontrol Sci Tech 11:165–216

    Google Scholar 

  8. Dai B, Yang H, Dai X, Wang W, Wu S, Zhao X, Xiao Y (2019) Microbial composition changes on the surface of strawberries from the field and market by 16SrDNA sequencing. J Food Saf 39:e12630

    Google Scholar 

  9. Dassonville N, Thielemans T, Gosset V (2013) FresaProtect and BerryProtect: mixes of parasitoids to control all common aphid species on protected soft fruit crops Product development and case studies from three years of experience. Asp Appl Biol 119:79–87

    Google Scholar 

  10. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106:9063–9068

    CAS  Google Scholar 

  11. Desneux N, O’neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res 98:631–639

    CAS  Google Scholar 

  12. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398

    Google Scholar 

  13. Doyle JJ, Doyle JL (1990) Isolation of DNA from fresh plant tissue. Focus 12:13–15

    Google Scholar 

  14. Dughetti AC, Kirschbaum DS, Conci VC (2017) Especies de virus y pulgones encontrados en cultivos de frutilla en Argentina. RIA 43:36–50

    Google Scholar 

  15. Fakhour S, Ambroise J, Renoz F, Foray V, Gala J, Hance T (2018) A large-scale field study of bacterial communities in cereal aphid populations across morocco. FEMS Microbiol Ecol 94(3):fiy003

    Google Scholar 

  16. Francesena F, Rocca M, Rizzo E, Arneodo JD, Greco N (2019) Potential of predatory Neotropical ladybirds and minute pirate bug on strawberry aphid. An Acad Bras Ciênc 91(4):e20181001

    Google Scholar 

  17. Gómez-Marco F, Tena A, Jacas J, Urbaneja A (2015) Early arrival of predators controls Aphis spiraecola colonies in citrus clementines. J Pest Sci 5:189–203

    Google Scholar 

  18. Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Google Scholar 

  19. Hall ME, Wilcox WF (2019) Identification and frequencies of endophytic microbes within healthy grape berries. Am J Enol Vitic 70:212–219

    CAS  Google Scholar 

  20. Hatano E, Kunert G, Michaud JP, Weisser WW (2008) Chemical cues mediating aphid location by natural enemies. Eur J Entomol 105:797–806

    CAS  Google Scholar 

  21. Khan A, Shah M (2017) Records of aphids and their natural enemies in agro-ecosystem with special reference to horticultural ecosystem of Kashmir. J Entomol Zool Stud 5:189–203

    Google Scholar 

  22. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  23. Larocca A, Fanti P, Romano VA, Marsicovetere E, Isodoro N, Romani R, Ruschioni S, Pennacchio F, Battaglia D (2007) Functional bases of host-acceptance behaviour in the aphid parasitoid Aphidius ervi. Physiol Entomol 32:305–312

    Google Scholar 

  24. Latham D, Mills N (2012) Host instar preference and functional response of Aphidius transcaspicus, a parasitoid of mealy aphids (Hyalopterus species). BioControl 57:603–610

    Google Scholar 

  25. Mackauer M, Michaud JP, Völkl W (1996) Host choice by aphid parasitoids (Hymenoptera: Aphidiidae): Host recognition, host quality and host value. Can Entomol 128:959–980

    Google Scholar 

  26. Manly BFJ (1974) A model for certain types of selection experiments. Biometrics 30:281–294

    Google Scholar 

  27. Michaud JP (1996) The oviposition behavior of Aphidius ervi and Monoctonus paulensis (Hymenoptera: Aphidiidae) encountering different host species (Homoptera: Aphididae) in sequential patches. J Insect Behav 9:683–694

    Google Scholar 

  28. Milenkovic S (1994) Bioecology of the strawberry aphid, Chaetosiphon fragaefolii Cockerell (Homoptera: Aphididae). Rev Res Work Fac Agr 39:21–27

    Google Scholar 

  29. Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    CAS  Google Scholar 

  30. Oatman ER, Trumble JT, Voth V (1983) Composition and relative abundance of parasites associated with aphid populations on strawberry in Southern California. Environ Entomol 12:1714–1717

    Google Scholar 

  31. Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185

    CAS  Google Scholar 

  32. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    CAS  Google Scholar 

  33. Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800

    CAS  Google Scholar 

  34. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266

    CAS  Google Scholar 

  35. Perdikis DCH, Lykouressis DP, Garantonakis NG, Iatrou SA (2004) Instar preference and parasitisation of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by the parasitoid Aphidius colemani (Hymenoptera: Aphidiidae). Eur J Entomol 101:333–336

    Google Scholar 

  36. Powell W (1986) Enhancing parasitoid activity in crops. In: Waage J, Greathead D (eds) Insect parasitoids. Acad. Press, London, pp 319–340

    Google Scholar 

  37. R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. https://www.r-project.org

  38. Rabasse JM, Trouve C, Geria AM, Quignou A (2001) Aphid pests of strawberry crops and their parasitoids in France. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent 66:293–301

    CAS  Google Scholar 

  39. Rehman A, Powell W (2010) Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera). J Plant Breed Crop Sci 2:299–311

    Google Scholar 

  40. Rondon SI, Cantliffe DJ (2004) Chaetosiphon fragaefolii (Homoptera: Aphididae): a potential new pest in Florida? Fla Entomol 87:612–615

    Google Scholar 

  41. Rondon S, Cantliffe D, Price J (2005) Population dynamics of the cotton aphid, Aphis gossypii (Homoptera: Aphididae), on strawberries grown under protected structure. Fla Entomol 88:152–158

    Google Scholar 

  42. Sampaio MV, Bueno VHP, van Lenteren JC (2001) Preferência de Aphidius colemani Viereck (Hymenoptera: Aphidiidae) por Myzus persicae (Sulzer) e Aphis gossypii Glover (Hemiptera: Aphididae). Neotrop Entomol 30:655–660

    Google Scholar 

  43. Tahiriri S, Talebi AA, Fathipour Y, Zamani AA (2007) Host stage preference, functional response and mutual interference of Aphidius matricariae (Hym.: Braconidae: Aphidiinae) on Aphis fabae (Hom.: Aphididae). Entomol Sci 10:323–331

    Google Scholar 

  44. Talebi AA, Zamani AA, Fathipour Y, Baniameri V, Kheradmand K, Haghani M (2006) Host stage preference by Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae) as parasitoids of Aphis gossypii (Hemiptera: Aphididae) on greenhouse cucumber. IOBC/WPRS Bull 29:173–177

    Google Scholar 

  45. Underwood N (2009) Effect of genetic variance in plant quality on the population dynamics of a herbivorous insect. J Animal Ecol 78:839–847

    Google Scholar 

  46. van Steenis MJ (1993) Suitability of Aphis gossypii Glov., Macrosiphum euphorbiae (Thom.) and Myzus persicae Sulz. (Hom.: Aphididae) as host for several aphid parasitoid species (Hym.: Braconidae). Bull IOBC/WPRS 26:157–160

    Google Scholar 

  47. van Steenis MJ (1995) Evaluation of four aphidiine parasitoids for biological control of Aphis gossypii. Entomol Exp Appl 75:151–157

    Google Scholar 

  48. van Driesche RG, Hauschild K (1987) Potential for increased use of biological control agents in small fruit crops in Massachusetts. Bull Mass Agric Exp Stn 718:22–34

    Google Scholar 

  49. Vorburger C, Gehrer L, Rodriguez P (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 6:109–111

    Google Scholar 

  50. Weldon SR, Strand MR, Oliver KM (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc R Soc B 280:2012103

    Google Scholar 

  51. Zamani AA, Talebi A, Fathipour Y, Baniameri V (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

    Google Scholar 

  52. Zamani AA, Haghani M, Kheradmand K (2012) Effect of temperature on reproductive parameters of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae) on Aphis gossypii (Hemiptera: Aphididae) in laboratory conditions. J Crop Prot 1:35–40

    Google Scholar 

  53. Zumoffen L, Rodriguez M, Gerding M, Salto CE, Salvo A (2015) Plantas, áfidos y parasitoides: interacciones tróficas en agroecosistemas de la provincia de Santa Fe, Argentina y clave para la identificación de los Aphidiinae y Aphelinidae (Hymenoptera) conocidos de la región. Rev Soc Entomol Arg 74:133–144

    Google Scholar 

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Acknowledgements

This study was supported by the National Agency for Promotion of Science and Technology of Argentina, grant PICT 2015-1427, the Program of Incentives for Professors-Researchers of the National Ministry of Culture and Education of Argentina, grant N834, and the National Institute of Agricultural Technology of Argentina (INTA), through project PNBIO 1131044. We thank Dr. Juan José Martínez, from Departamento de Ciencias Naturales—Facultad de Ciencias Exactas y Naturales—Universidad Nacional de la Pampa, Argentina (UNLPAM) for their kind assistance in the determination of parasitoid species, Dr. Andrea Andorno, from Instituto de Microbiología y Zoología Agrícola (IMyZA, INTA Castelar, Argentina) for providing parasitoid adult individuals of A. colemani, and Graciela Minardi for the assistance in the statistical analyses. Dr. Donald F. Haggerty, a retired academic career investigator from University of California, USA edited an earlier draft version of the manuscript.

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Francesena, N., Arneodo, J.D., Rocca, M. et al. Exploring the factors involved in the absence of parasitism of Chaetosiphon fragaefolii by generalist parasitoids in strawberry. BioControl 65, 681–692 (2020). https://doi.org/10.1007/s10526-020-10044-9

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Keywords

  • Aphidius matricariae
  • Aphidius colemani
  • Fragaria × ananassa
  • Host preference
  • Secondary symbionts