Eur. J. Entomol. 112 (3): 440-445, 2015 | DOI: 10.14411/eje.2015.056

Influence of different species of aphid prey on the immature survival and development of four species of aphidophagous coccinellids (Coleoptera: Coccinellidae)

Dimitrios P. PAPACHRISTOS1, Ioanna KATSAROU2, Antonios MICHAELAKIS1, Nikos E. PAPANIKOLAOU1
1 Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 St. Delta Str., 145 61 Kifissia, Athens, Greece; e-mails: d.papachristos@bpi.gr; a.michaelakis@bpi.gr; nepapanikolaou@yahoo.gr
2 Department of Plant Production, Technological Educational Institute of Epirus, Kostakioi Artas, 47100 Arta, Greece; e-mail: jdkatsarou@yahoo.gr

This study was on the effect of three species of aphids (Aphis fabae, Macrosiphoniella sanborni, Brevicoryne brassicae) on the survival, growth and development of the immature stages of the aphidophagous coccinellids Coccinella septempunctata, Ceratomegilla undecimnotata, Propylea quatuordecimpunctata and Oenopia conglobata. The percentage survival was lowest, immature development most prolonged and the adults the lightest when these predators were fed on B. brassicae. In addition, C. septempunctata and C. undecimnotata performed better when fed on M. sanborni (74.1 and 72.0% total immature survival, respectively) than P. quatuordecimpunctata and O. conglobata (25.0 and 13.8% total immature survival, respectively). In addition, the host plant of A. fabae also had a significant effect on the performance of the predators. These coccinellids survived best, had shorter developmental times and were heavier as adults when fed on A. fabae reared on Vicia faba than on Phaseolus vulgaris. These results may be useful for improving the effectiveness of biological control practice and the production of coccinellids in an insectary.

Keywords: Coleoptera, Coccinellidae, Coccinella septempunctata, Ceratomegilla undecimnotata, Propylea quatuordecimpunctata, Oenopia conglobata, Aphididae, Aphis fabae, Macrosiphoniella sanborni, Brevicoryne brassicae, aphid prey, survival, development, aphid host plant

Received: June 6, 2014; Accepted: March 19, 2015; Prepublished online: May 15, 2015; Published: July 15, 2015

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References

  1. Aslan M.M. & Uygun N. 2005: The aphidophagous coccinellid (Coleoptera: Coccinellidae) species in Kahramanmaraš, Turkey. - Turk. J. Zool. 29: 1-8.
  2. Beninger C.W., Abou-Zaid M.M., Kistner A.L.E., Hallett R.H., Iqbal M.J., Grodzinski B. & Hall J.C. 2004: A flavanone and two phenolic acids from Chrysanthemum morifolium with phytotoxic and insect growth regulating activity. - J. Chem. Ecol. 30: 589-606. Go to original source...
  3. Blackman R.L. & Eastop V.F. 2000: Aphids on the World's Crops. An Identification and Information Guide. 2nd ed. John Wiley & Sons, Chichester, 476 pp.
  4. Bridges M., Jones A.M.E, Bones A.M., Hodgson C., Cole R., Bartlet E., Wallsgrove R., Karapapa V.K., Watts N. & Rossiter J.T. 2002: Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. - Proc. R. Soc. Lond. (B) 269: 187-191. Go to original source...
  5. Cabral S., Soares A.O., Moura R. & Garcia P. 2006: Suitability of Aphis fabae, Myzus persicae (Homoptera: Aphididae) and Aleyrodes proletella (Homoptera: Aleyrodidae) as prey forCoccinella undecimpunctata (Coleoptera: Coccinellidae). - Biol. Contr. 39: 434-440. Go to original source...
  6. Carter M.C., Sutherland D. & Dixon A.F.G. 1984: Plant structure and the searching efficiency of coccinellid larvae. - Oecologia (Berlin) 63: 394-397. Go to original source...
  7. Chaplin-Kramer R., Kliebenstein D.J., Chiem A., Morrill E., Mills N. & Kremen C. 2011: Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators. - J. Appl. Ecol. 48: 880-887. Go to original source...
  8. Clark T.L. & Messina F.J. 1998: Plant architecture and the foraging success of ladybird beetles attacking the Russian wheat aphids. - Entomol. Exp. Appl. 86: 153-161. Go to original source...
  9. Dmitriew C. & Rowe L. 2011: The effects of larval nutrition on reproductive performance in a food-limited adult environment. - PLoS ONE 6: e17399. Go to original source...
  10. Francis F., Haubruge E., Hastir M.P. & Gaspar C. 2001a: Effects of aphid host plant on development and reproduction of the third trophic level, the predator Adalia bipunctata (Coleoptera: Coccinellidae). - Environ. Entomol. 30: 947-952. Go to original source...
  11. Francis F., Lognay G., Wathelet J.P. & Haubruge E. 2001b: Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. - J. Chem. Ecol. 27: 243-256. Go to original source...
  12. Francis F., Lognay G., Wathelet J.P. & Haubruge E. 2002: Characterisation of aphid myrosinase and degradation studies of glucosinolates. - Arch. Insect Biochem. Physiol. 50: 173-182. Go to original source...
  13. Freier B., Triltsch H., Mowes M. & Moll E. 2007: The potential of predators in natural control of aphids in wheat: Results of a ten-year field study in two German landscapes. - BioControl 52: 775-788. Go to original source...
  14. Giles K.L., Madden R.D., Stockaland R., Payton M.E. & Dillwith J.W. 2002: Host plants affect predator fitness via the nutritional value of herbivore prey: investigation of a plant-aphid-ladybeetle system. - BioControl 47: 1-12. Go to original source...
  15. Hauge M.S., Nielsen F.H. & Toft S. 1998: The influence of three cereal aphid species and mixed diet on larval survival, development and adult weight of Coccinella septempunctata. - Entomol. Exp. Appl. 89: 319-322. Go to original source...
  16. Hodek I. 1993: Habitat and food specificity in aphidophagous predators. - Biocontr. Sci. Technol. 3: 91-100. Go to original source...
  17. Hodek I. & Evans E.W. 2012: Food relationships. In Hodek I., van Emden H.F. & Honėk A. (eds): Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Wiley-Blackwell, Chichester, pp. 141-274.
  18. Hodek I. & Honėk A. 1996: Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, 464 pp.
  19. Hodek I. & Michaud J.P. 2008: Why is Coccinella septempunctata so successful? (A point-of-view). - Eur. J. Entomol. 105: 1-12. Go to original source...
  20. Honėk A. 1985: Habitat preferences of aphidophagous coccinellids (Coleoptera). - Entomophaga 30: 253-264. Go to original source...
  21. Hu L. & Chen Z. 1997: Sesquiterpenoid alcohols from Chrysanthemum morifolium. - Phytochemistry 44: 1287-1290. Go to original source...
  22. Iperti G. 1999: Biodiversity of predaceous coccinellidae in relation to bioindication and economic importance. - Agr. Ecosyst. Environ. 74: 323-342. Go to original source...
  23. Jones A.M.E, Bridges M., Bones A.M., Cole R. & Rossiter J.T. 2001: Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.). - Ins. Biochem. Mol. Biol. 31: 1-5. Go to original source...
  24. Kalushkov P. & Hodek I. 2004: The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. - BioControl 49: 21-32. Go to original source...
  25. Kamo T., Tokuoka Y. & Miyazaki M. 2010: Influence of aphid-host plant pairs on the survivorship and development of themulticolored Asian ladybird beetle: implications for the management of vegetation in rural landscapes. - Ecol. Res. 25: 1141-1149. Go to original source...
  26. Katsoyannos P., Kontodimas D. & Stathas G. 2005: Summer diapause and winter quiescence of Hippodamia (Semiadalia)undecimnotata (Coleoptera: Coccinellidae) in central Greece. - Eur. J. Entomol. 102: 453-457. Go to original source...
  27. Kavallieratos N.G., Athanassiou C.G., Tomanovic Z., Papadopoulos G.D. & Vayias B.J. 2004: Seasonal abundance and effects of predators (Coleoptera, Coccinellidae) and parasitoids (Hymenoptera: Braconidae, Aphidiinae) on Myzus persicae (Hemiptera, Aphidoidea) densities on tobacco: a two-year study from central Greece. - Biologia (Bratislava) 59: 613-619.
  28. Kazana E., Pope T.W., Tibbles L., Bridges M., Pickett J.A., Bones A.M., Powell G. & Rossiter J.T. 2007: The cabbage aphid: a walking mustard oil bomb. - Proc. R. Soc. Lond. (B) 274: 2271-2277. Go to original source...
  29. Khan I., Din S., Khalil S.K. & Rafi M.A. 2007: Survey of predatory coccinellids (Coleoptera: Coccinellidae) in the Chitral district, Pakistan. - J. Insect Sci. 7(7): 1-6. Go to original source...
  30. Kil B.-S. & Lee S.Y. 1987: Allelopathic effects of Chrysanthemum morifolium on germination and growth of several herbaceous plants. - J. Chem. Ecol. 13: 299-308. Go to original source...
  31. Kontodimas D.C., Milonas P.G., Stathas G.J., Papanikolaou N.E., Skourti A. & Matsinos Y.G. 2008: Life table parameters of the aphid predators Coccinella septempunctata, Ceratomegilla undecimnotata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). - Eur. J. Entomol. 105: 427-430. Go to original source...
  32. Kos M., Houshyani B., Achhami B.B., Wietsma R., Gols R., Weldegergis B.T., Kabouw P., Bouwmeester H.J., Vet L.E.M., Dicke M. & Loon J.J.A. 2012: Herbivore-mediated effects of glucosinolates on different natural enemies of a specialist aphid. - J. Chem. Ecol. 38: 100-115. Go to original source...
  33. Kos M., Kabouw P., Noordam R., Hendriks K., Vet L.E.M., Van Loon J.J.A. & Dicke M. 2011: Prey-mediated effects of glucosinolates on aphid predators. - Ecol. Entomol. 36: 377-388. Go to original source...
  34. Legrand A. & Barbosa P. 2003: Plant morphological complexity impacts foraging efficiency of adult Coccinella septempunctata L. (Coleoptera: Coccinellidae). - Environ. Entomol. 32: 1219-1226. Go to original source...
  35. Leiss K.A., Maltese F., Choi Y.H., Verpoorte R. & Klinkhamer P.G.L. 2009: Identification of chlorogenic acid as a resistance factor for thrips in Chrysanthemum. - Plant Physiol. 150: 1567-1575. Go to original source...
  36. Madzdzadeh S.M. & Mehrparvar M. 2009: Morphological discrimination of geographical populations of Macrosiphoniella sanborni (Gillette, 1908) (Hem.: Aphididae) in Iran. - North-West. J. Zool. 5: 338-348.
  37. Nedvėd O. & Honėk A. 2012: Life history and development. In Hodek I., van Emden H.F. & Honėk A. (eds): Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Wiley-Blackwell, Chichester, pp. 54-109.
  38. Obrycki J.J. & Kring T.J. 1998: Predaceous coccinellidae in biological control. - Annu. Rev. Entomol. 43: 295-321. Go to original source...
  39. Obrycki J.J., Orr D.B., Orr C.J., Wallendorf M. & Flanders R.V. 1993: Comparative developmental and reproductive biology of three populations of Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). - Biol. Contr. 3: 27-33. Go to original source...
  40. Omkar & Pervez A. 2005: Ecology of two-spotted aphidophagous ladybird, Adalia bipunctata: a review. - J. Appl. Entomol. 129: 465-474. Go to original source...
  41. Papanikolaou N.E., Milonas P.G., Kontodimas D.C., Demiris N. & Matsinos Y.G. 2013: Temperature-dependent development, survival, longevity, and fecundity of Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). - Ann. Entomol. Soc. Am. 106: 228-234. Go to original source...
  42. Pervez A. & Omkar 2006: Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: a review. - Biocontr. Sci. Technol. 16: 112-128. Go to original source...
  43. Pervez A. & Omkar 2011: Ecology of aphidophagous ladybird Propylea species: A review. - J. Asia-Pac. Entomol. 14: 357-365.
  44. Pratt C. 2008: Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two coccinellid species. - J. Chem. Ecol. 34: 323-329. Go to original source...
  45. Price P.W., Bouton C.E., Gross P., McPheron B.A., Thompson J.N. & Weis A.E. 1980: Interaction among three trophic levels: influence of plant on interaction between insect herbivores and natural enemies. - Annu. Rev. Ecol. Evol. Syst. 11: 41-65. Go to original source...
  46. Putman W.L. 1955: Bionomics of Stethorus punctillum Weise in Ontario. - Can. Entomol. 87: 9-33. Go to original source...
  47. Shah M.A. 1982: The influence of plant surfaces on the searching behaviour of Coccinellid larvae. - Entomol. Exp. Appl. 31: 377-380. Go to original source...
  48. Shannag H.K. & Obeidat W.M. 2006: Voracity and conversion efficiency by larvae of Coccinella septempunctata L. (Coleoptera: Coccinellidae) on Aphis fabae Scop. (Homoptera: Aphididae) reared on two faba bean cultivars with different levels of resistance. - Appl. Entomol. Zool. 41: 521-527. Go to original source...
  49. Shannag H.K. & Obeidat W.M. 2008: Interaction between plant resistance and predation of Aphis fabae (Homoptera: Aphididae) by Coccinella septempunctata (Coleoptera: Coccinellidae). - Ann. Appl. Biol. 152: 331-337. Go to original source...
  50. SPSS 2004: SPSS 14 for Windows User's Guide. SPSS, Chicago, IL, USA.
  51. Theunissen N. 1989: Integrated control of aphids on field-grown vegetables. In Minks A.K. & Harrewijn P. (eds): Aphids, their Biology, Natural Enemies and Control. Vol. C. Elsevier, Amsterdam, pp. 285-289.
  52. Traugott M.S. & Stamp N.E. 1997: Effects of chlorogenic acid-and tomatinefed caterpillars on performance of an insect predator. - Oecologia 109: 265-272. Go to original source...
  53. Tsaganou F.C., Hodgson C.J., Athanassiou C.G., Kavallieratos N.G. & Tomanovic Z. 2004: Effect of Aphis gossypii Glover, Brevicoryne brassicae (L.), and Megoura viciae Buckton (Hemiptera: Aphidoidea) on the development of the predator Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). - Biol. Contr. 31: 138-144. Go to original source...
  54. Vanhaelen N., Gaspar C. & Francis F. 2002: Influence of prey host plant on a generalist aphidophagous predator: Episyrphus balteatus (Diptera: Syrphidae). - Eur. J. Entomol. 99: 561-564. Go to original source...
  55. Wheeler A.G.J. 1990: Propylea quatuordecimpunctata: Additional U.S. records of an adventive lady beetle (Coleoptera: Coccinellidae). - Entomol. News 101: 164-165.
  56. Yašar B. & Özger S. 2005: Functional response of Oenopia conglobata (L.) (Coleoptera: Coccinellidae) on Hyalopterus pruni (Geoffroy) (Homoptera: Aphididae) in three different size arenas. - Turk. J. Entomol. 29: 91-99.
  57. Xia J.Y., van der Werf W. & Rabbinge R. 1999: Temperature and prey density on bionomics of Coccinella septempunctata (Coleoptera: Coccinellidae) feeding on Aphis gossypii (Homoptera: Aphididae) on cotton. - Environ. Entomol. 28: 307-314. Go to original source...