Parasitization of the sugarcane aphid, Melanaphis sacchari, by commercially available aphid parasitoids

Abstract

Identification of natural enemies of novel pests is important for the development of effective integrated pest management. Commercially available parasitoids used for control of arthropod pests have potential for enhancing biological control of invasive pests. The sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae), is a new pest on sweet sorghum, Sorghum bicolor, in the USA. Surveys of M. sacchari have not detected any parasitoids in central Kentucky. In North America, Aphelinus abdominalis (Hymenoptera: Aphelinidae), Aphidius ervi (Hymenoptera: Braconidae), Aphidius colemani, and Aphidius matricariae are sold for aphid management. This study’s objective was to determine the host acceptance and suitability of M. sacchari for these parasitoid species. Host acceptance was assessed by counting attacks and oviposition strikes by parasitoids on M. sacchari. All parasitoid species accepted M. sacchari as a host in the parental generation (purchased adults) and the F1 generation (reared from M. sacchari). Host suitability was evaluated by transferring M. sacchari from host acceptance trials to caged sweet sorghum plants. Cages were monitored for aphid mummies and emerged adult parasitoids. Parental A. colemani produced the most mummies and adult parasitoids and reduced final M. sacchari numbers by 75%. A. ervi had a similar impact on M. sacchari populations but produced fewer mummies and adults. A. matricariae and A. abdominalis did not reduce M. sacchari populations. F1 parasitoids produced few adults and did not reduce M. sacchari populations. A. colemani demonstrated potential for field releases with the ability to use M. sacchari as a host and reduce aphid population growth.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Data availability

Data are deposited in the UKnowledge repository https://doi.org/10.13023/a4fv-f708.

References

  1. Ameri M, Rasekh A, Michaud JP, Allahyari H (2013) Morphometric indicators for quality assessment in the aphid parasitoid, Lysiphlebus fabarum (Braconidae: Aphidiinae). Eur J Entomol 110:519–525

    Google Scholar 

  2. Bai B, Mackauer M (1992) Influence of superparasitism on development rate and adult size in a solitary parasitoid wasp, Aphidius ervi. Funct Ecol 6:302–307

    Google Scholar 

  3. Bowling RD, Brewer MJ, Kerns DL, Gordy J, Seiter N, Elliott NE, Buntin GD, Way MO, Royer TA, Biles S, Maxson E (2016) Sugarcane aphid (Hemiptera: Aphididae): a new pest on sorghum in North America. J Integr Pest Manag 7:1–13

    Google Scholar 

  4. Brewer MJ, Gordy JW, Kerns DL, Woolley JB, Rooney WL, Bowling RD (2017) Sugarcane aphid population growth, plant injury, and natural enemies on selected grain sorghum hybrids in Texas and Louisiana. J Econ Entomol 110:2109–2118

    CAS  PubMed  Google Scholar 

  5. Cayetano L, Vorburger C (2015) Symbiont-conferred protection against Hymenopteran parasitoids in aphids: How general is it? Ecol Entomol 40:85–93

    Google Scholar 

  6. Cloutier C, Mackauer M (1980) The effect of superparasitism by Aphidius smithi (Hymenoptera: Aphidiidae) on the food budget of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae). Can J Zool 58:241–244

    Google Scholar 

  7. Couty A, De La Viña G, Clark SJ, Kaiser L, Pham-Delègue MH, Poppy GM (2001) Direct and indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potato-aphid parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). J Insect Physiol 47:553–561

    CAS  PubMed  Google Scholar 

  8. de Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698

    Google Scholar 

  9. de Farias AMI, Hopper KR (1999) Oviposition behavior of Aphelinus asychis (Hymenoptera: Aphelinidae) and Aphidius matricariae (Hymenoptera: Aphidiidae) and defense behavior of their host Diuraphis noxia (Homoptera: Aphididae). Environ Entomol 28:858–862

    Google Scholar 

  10. Denmark HA (1988) Sugarcane aphids in Florida (Homoptera: Aphididae). Florida Department of Agriculture & Consumer Services, Division of Plant Industry, Entomolology Circular, p 302

    Google Scholar 

  11. García-González F, Ramírez-Delgado M, Cortez-Madrigal H, de Ramirez-Ahuja ML (2018) New reports of parasitoids and hyperparasitoids of Melanaphis sacchari (Zehntner) in Mexico. Southwest Entomol 43:787–790

    Google Scholar 

  12. Gardner J, Hoffmann MP, Pitcher SA, Harper JK (2011) Integrating insecticides and Trichogramma ostriniae to control European corn borer in sweet corn: economic analysis. Biol Control 56:9–16

    CAS  Google Scholar 

  13. Gariepy V, Boivin G, Brodeur J (2015) Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions. Biol Control 80:1–7

    Google Scholar 

  14. He XZ, Wang Q (2006) Asymmetric size effect of sexes on reproductive fitness in an aphid parasitoid Aphidius ervi (Hymenoptera: Aphidiidae). Biol Control 36:293–298

    Google Scholar 

  15. Henry LM, Roitberg BD, Gillespie DR (2008) Host-range evolution in Aphidius parasitoids: fidelity, virulence and fitness trade-offs on an ancestral host. Evolution 62:689–699

    PubMed  Google Scholar 

  16. Hinson PO (2017) Effect of temperature on the development of sugarcane aphid, Melanaphis sacchari, on sorghum. A&M University, West Texas

    Google Scholar 

  17. Höller C, Haardt H (1993) Low field performance of an aphid parasitoid, Aphelinus abdominalis, efficient in the laboratory [Hym., Aphelinidae]. Entomophaga 38:115–124

    Google Scholar 

  18. Holt JR, Styer A, White JA, Armstrong JS, Nibouche S, Costet L, Malacrinò A, Antwi JB, Wulff J, Peterson G, McLaren N, Medina RF (2020) Differences in microbiota between two multilocus lineages of the sugarcane aphid (Melanaphis sacchari) in the continental United States. Ann Entomol Soc Am 113:257–265

    CAS  Google Scholar 

  19. Ingerslew KS, Finke DL (2017) Mechanisms underlying the nonconsumptive effects of parasitoid wasps on aphids. Environ Entomol 46:75–83

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Japoshvili G, Abrantes I (2006) Aphelinus species (Hymenoptera: Aphelinidae) from the Iberian Peninsula, with the description of one new species from Portugal. J Nat Hist 40:855–862

    Google Scholar 

  21. Jones TS, Bilton AR, Mak L, Sait SM (2015) Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecol Evol 5:459–465

    PubMed  PubMed Central  Google Scholar 

  22. Kaiser MC, Heimpel GE (2016) Parasitoid-induced transgenerational fecundity compensation in an aphid. Entomol Exp Appl 159:197–206

    Google Scholar 

  23. Kavallieratos NG, Tomanović Ž, Starý P, Athanassiou CG, Sarlis GP, Petrović O, Niketić M, Veroniki MA (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Appl Entomol Zool 39:527–563

    Google Scholar 

  24. Kim H, Lee S (2008) A molecular phylogeny of the tribe Aphidini (Insecta: Hemiptera: Aphididae) based on the mitochondrial tRNA/COII, 12S/16S and the nuclear EF1α genes. Syst Entomol 33:711–721

    Google Scholar 

  25. La-Spina M, Jandricic SE, Buitenhuis R (2019) Short-term increases in aphid dispersal from defensive dropping do not necessarily affect long-term biological control by parasitoids. J Econ Entomol 112:1552–1559

    PubMed  Google Scholar 

  26. Larocca A, Fanti P, Romano VA, Marsicovetere E, Isidoro 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 

  27. Lenhart PA, White JA (2017) A defensive endosymbiont fails to protect aphids against the parasitoid community present in the field. Ecol Entomol 42:680–684

    Google Scholar 

  28. Maxson EL, Brewer MJ, Rooney WL, Woolley JB (2019) Species composition and abundance of the natural enemies of sugarcane aphid, Melanaphis sacchari (Zehnter) (Hemiptera: Aphididae), on sorghum in Texas. Proc Entomol Soc Washingt 121:657–680

    Google Scholar 

  29. McLean AHC, Godfray HCJ (2015) Evidence for specificity in symbiont conferred protection against parasitoids. Proc R Soc B Biol Sci 282:20150977

    Google Scholar 

  30. Messing RH, Rabasse JM (1995) Oviposition behaviour of the polyphagous aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Agric Ecosyst Environ 52:13–17

    Google Scholar 

  31. Montoya P, Liedo P, Benrey B, Cancino J, Barrera JF, Sivinski J, Aluja M (2000) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 18:216–224

    Google Scholar 

  32. Nibouche S, Costet L, Holt JR, Jacobson A, Pekarcik A, Sadeyen J, Scott AJ, Peterson GC, McLaren N, Medina RF (2018) Invasion of sorghum in the Americas by a new sugarcane aphid (Melanaphis sacchari) superclone. PLoS ONE 13(4):e0196124

    PubMed  PubMed Central  Google Scholar 

  33. Oliver KM, Russell JA, Morant NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Pennacchio F, Digilio MC, Tremblay E, Tranfaglia A (1994) Host recognition and acceptance behaviour in two aphid parasitoid species Aphidius ervi and Aphidius microlophii (Hymenoptera: Braconidae). Bull Entomol Res 84:57–64

    Google Scholar 

  35. R Core Team (2016) R: a language and environment for statistical computing, R versions 333 R Foundation for Statistical Computing. Austria, Vienna. http://www.r-project.org

  36. Salas-Araiza MD, Lopez-Gutierrez DR, Martinez-Jaime OA, Guzman-Mendoza R (2017) Parasitoids of sugarcane aphid, Melanaphis sacchari, at Irapuato, Guanajuato, Mexico. Southwest Entomol 42:1091–1094

    Google Scholar 

  37. SAS Institute Inc (2014) Base SAS® 9.4 procedures guide. SAS Institute Inc., Cary, NC

    Google Scholar 

  38. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    CAS  Google Scholar 

  39. Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. Proc R Soc B Biol Sci 270:1905–1909

    Google Scholar 

  40. Silava RJ, Cidanes FJ, Pedroso EC, Sala SRD (2011) Host quality of different aphid species for rearing Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). Neotrop Entomol 40:477–482

    Google Scholar 

  41. Singh BU, Padmaja PG, Seetharama N (2004) Biology and management of the sugarcane aphid, Melanaphis sacchari (Zehntner) (Homoptera: Aphididae), in sorghum: a review. Crop Prot 23:739–755

    Google Scholar 

  42. Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107

    Google Scholar 

  43. Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716

    Google Scholar 

  44. Stary P, Gerding M, Norambuena H, Remaudiere G (1993) Environmental research on aphid parasitoid biocontrol agents in Chile (Hym., Aphidiidae; Hom., Aphidoidae). J Appl Entomol 115:292–306

    Google Scholar 

  45. Tomanović Ž, Kavallieratos NG, Starý P, Stanisavljević LŽ, Ćetković A, Stamenković S, Jovanović S, Athanassiou CG (2009) Regional tritrophic relationship patterns of five aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) in agroecosystem-dominated landscapes of Southeastern Europe. J Econ Entomol 102:836–854

    PubMed  Google Scholar 

  46. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634

    PubMed  Google Scholar 

  47. Vasquez GMV, Orr DB, Baker JR (2006) Efficacy assessment of Aphidius colemani (Hymenoptera: Braconidae) for suppression of Aphis gossypii (Homoptera: Aphididae) in greenhouse-grown chrysanthemum. J Econ Entomol 99:1104–1111

    PubMed  Google Scholar 

  48. Velasco-Hernández MC, Desneux N, Ramírez-Martínez MM, Cicero L, Ramirez-Romero R (2017) Host species suitability and instar preference of Aphidius ervi and Aphelinus abdominalis. Entomol Gen 36:347–367

    Google Scholar 

  49. Villanueva RT (2016) The sugarcane aphid arrived to Kentucky a month earlier in 2016 than in 2015. In: Kentucky pest news. https://kentuckypestnews.wordpress.com/2016/07/19/the-sugarcane-aphid-arrived-to-kentucky-a-month-earlier-in-2016-than-in-2015/. Accessed 20 July 2016

  50. Vinson SB (1976) Host selection by insect parasitoids. Annu Rev Entomol 21:109–133

    Google Scholar 

  51. Vinson SB, Iwantsch GF (1980) Host suitability for insect parasitoids. Annu Rev Entomol 25:397–419

    Google Scholar 

  52. Visser ME (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J Anim Ecol 63:963–978

    Google Scholar 

  53. Wharton RA (1983) The status of Aphelinus varipes (Foster) and Aphelinus nigritus Howard (Hymenoptera: Aphelinidae). Proc Entomol Soc Washingt 85:626–627

    Google Scholar 

Download references

Acknowledgements

This work is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch project accession numbers 1008480.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nathan H. Mercer.

Ethics declarations

Conflict of interests

The authors have no conflicts of interest with this work.

Additional information

Handling Editor: Stefano Colazza.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mercer, N.H., Bessin, R.T. & Obrycki, J.J. Parasitization of the sugarcane aphid, Melanaphis sacchari, by commercially available aphid parasitoids. BioControl 66, 181–191 (2021). https://doi.org/10.1007/s10526-020-10051-w

Download citation

Keywords

  • Parasitoid wasp
  • Host acceptance
  • Host suitability
  • Hemiptera
  • Aphididae
  • Hymenoptera