Eur. J. Entomol. 112 (2): 270-280, 2015 | DOI: 10.14411/eje.2015.043

Aphis pomi and Aphis spiraecola (Hemiptera: Sternorrhyncha: Aphididae) in Europe - new information on their distribution, molecular and morphological peculiarities

Rimantas RAKAUSKAS, Jekaterina BAŠILOVA, Rasa BERNOTIENĖ
Department of Zoology, Faculty of Natural Sciences, Vilnius University, Čiurlionio str. 21/27, LT 03101 Vilnius, Lithuania; e-mails: rimantas.rakauskas@gf.vu.lt; jekaterina.basilova@gf.vu.lt; rasa.bernotiene@gf.vu.lt

Aphid species Aphis pomi (de Geer, 1773) is oligophagous on pomoideous host plants, whilst Aphis spiraecola Patch, 1914 is a polyphagous species alternating between Spiraea spp., its primary host, and a wide variety of secondary hosts, also including pomoideous species. Despite the biological distinction, these species are difficult to separate using their morphological characters. Partial sequences of mitochondrial COI and nuclear EF-1α genes were analyzed for samples from Central and Eastern Europe, Germany, Bulgaria, Italy, Turkey, China together with available data from GenBank. Interspecific pairwise sample divergences of the COI fragment ranged from 3.1 to 4.3%. One COI haplotype of A. pomi was predominant (n = 24), with a pan European distribution. The most abundant COI haplotype of A. spiraecola (n = 16) occurred in Lithuania, Latvia, Poland, Italy, Turkey and China. Interspecific pairwise sample divergences of the EF-1α fragment ranged from 0.6 to 1.2%. Analyzed partial sequences of EF-1α were identical in A. pomi. The most abundant EF-1α haplotype of A. spiraecola (n = 14) occurred in Lithuania, Poland, Italy, Turkey and China. The length of ultimate rostral segment appeared to be the most reliable morphological character for discrimination between apple and spirea aphid species. It allowed a 100% correct identification of A. pomi (n = 143) and 91.5% of A. spiraecola (n = 94) specimens in the European samples used for the molecular analysis. The existence of A. spiraecola in the Eastern Baltic region of Europe is documented for the first time.

Keywords: Hemiptera, Aphididae, Aphis pomi, Aphis spiraecola, apple aphid, spirea aphid, morphometrics, identification, mitochondrial COI, nuclear EF-1α

Received: September 22, 2014; Accepted: January 7, 2015; Prepublished online: February 16, 2015; Published: April 2, 2015

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References

  1. Baker A.C. & Turner W.F. 1916: Morphology and biology of the green apple aphis. - J. Agr. Res. 5: 955-994
  2. Barbagallo S., Cravedi P., Pasqualini E., Patti I. & Stroyan H.L.G. 1997: Aphids of the Principal Fruit-Bearing Crops. Grafiche Leardini, Verona, 123 pp
  3. Blackman R.L. & Eastop V.F. 2000: Aphids on the World's Crops: An Identification and Information Guide. John Wiley and Sons, Chichester, 414 pp
  4. Brown M.W. 2011: Importance of early arrival of adult Harmonia axyridis for control of Aphis spiraecola on apple. - Biocontrol 56: 65-69 Go to original source...
  5. Brown M.W., Hogmire H.W. & Schmitt J.J. 1995: Competitive displacement of apple aphid by spirea aphid (Homoptera: Aphididae) on apple as mediated by human activities. - Environ. Entomol. 24: 1581-1591 Go to original source...
  6. Brown M.W. & Mathews C.R. 2008: Conservation biological control of spirea aphid, Aphis spiraecola (Hemiptera: Aphididae) on apple by providing natural alternative food resources. - Eur. J. Entomol. 105: 537-540 Go to original source...
  7. Caglayan K., Serce C.U., Gazel M., Kaya K., Cengiz F.C., Vidal E. & Cambra M. 2013: Evaluation of the susceptibility of different Prunus rootstocks to natural infection of Plum pox virus-T. - J. Plant Pathol. 95: 579-586
  8. Cao J., Li J., Niu J., Liu X. & Zhang Q. 2012: Population structure of Aphis spiraecola (Hemiptera: Aphididae) on pear trees in China identified using microsatellites. - J. Econ. Entomol. 105: 583-591 Go to original source...
  9. Clement M., Posada D. & Crandall K.A. 2000: TCS: a computer program to estimate gene genealogies. - Mol. Ecol. 9: 1657-1659 Go to original source...
  10. Davletshina A.G. 1963: Aphids of the Genus Aphis L. of the Uzbekistan Fauna. Nauka, Tashkent, 135 pp. [in Russian]
  11. Foottit R.G., Halbert S.E., Miller G.L., Maw H.E.L. & Russell L.M. 2006: Adventive aphids (Hemiptera: Aphididae) of America north of Mexico. - Proc. Entomol. Soc. Wash. 108: 583-610
  12. Foottit R.G., Lowery D.T., Maw H.E.L., Smirle M.J. & Lushai G. 2009: Identification, distribution, and molecular characterization of the apple aphids Aphis pomi and Aphis spiraecola (Hemiptera: Aphididae: Aphidinae). - Can. Entomol. 141: 478-495 Go to original source...
  13. Frechette B., Cormier D., Chouinard G., Vanoosthuyse F. & Lucas E. 2008: Apple aphid, Aphis spp. (Hemiptera: Aphididae), and predator populations in an apple orchard at the non-bearing stage: The impact of ground cover and cultivar. - Eur. J. Entomol. 105: 521-529 Go to original source...
  14. Grasswitz T.R. & Burts E.C. 1995: Effect of native natural enemies and augmentative releases of Chrysoperla rufilabris Burmeister and Aphidoletes aphidimyza (Rondani) on the population dynamics of the green apple aphid, Aphis pomi De Geer. - Int. J. Pest Manag. 41: 176-183 Go to original source...
  15. Halbert S.E. & Voegtlin D.J.1992: Morphological differentiation between Aphis spiraecola and Aphis pomi (Homoptera, Aphididae). - Great Lakes Entomol. 25: 1-8
  16. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. - Nucl. Acid. Symp. 41: 95-98
  17. Heie O.E. 1986: The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. III. Family Aphididae: Subfamily Pterocommatinae and Tribe Aphidini of Subfamily Aphidinae. Fauna Entomologica Scandinavica 17. E.J. Brill / Scandinavian Science Press, Leiden, Copenhagen, 316 pp
  18. Hogmire H.W., Brown M.W., Schmitt J.J. & Winfield T.M. 1992: Population development and insecticide susceptibility of apple aphid and spirea aphid (Homoptera, Aphididae) on apple. - J. Entomol. Sci. 27: 113-119 Go to original source...
  19. Holman J. 2009: Host Plant Catalog of Aphids: Palaearctic Region. Springer, New York, 1140 pp
  20. Jaskiewicz B. & Kot I. 2007: The population dynamics of Aphis pomi De Geer on Cotoneaster divaricatus Rehd. et Wils. - Aphids and other Homopterous Insects 13: 121-127
  21. Kaakeh W., Pfeiffer D.G. & Marini R.P. 1993: Effect of Aphis spiraecola and A. pomi (Homoptera, Aphididae) on the growth of young apple trees. - Crop Prot. 12: 141-147 Go to original source...
  22. Kanbe T. & Akimoto S.I. 2009: Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations. - Mol. Ecol. 18: 801-816 Go to original source...
  23. Karczewska M. 1965: Badania nad biologia mszyc (Aphididae) wystepujacych na jabloni. [Studies on the biology of aphids (Aphididae) occurring on apple trees]. - Pol. Pis. Entomol. (B) 16: 245-296
  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 EF1alpha genes. - Syst. Entomol. 33: 711-721 Go to original source...
  25. Komazaki S. 1990: Variation in the hatch timing of the overwintering egg among populations of Aphis spiraecola Patch (Homoptera, Aphididae) collected from different host plants and localities in Japan. - Appl. Entomol. Zool. 25: 27-34 Go to original source...
  26. Labanowski G. 2008: Aphids (Hemiptera, Aphidoidea) on garden perennial plants. - Aphids and other Homopterous Insects 14: 21-37
  27. Lagos D.M., Voegtlin D.J., Coeur d'acier A. & Giordano R. 2014: Aphis (Hemiptera: Aphididae) species groups found in the Midwestern United States and their contribution to the phylogenetic knowledge of the genus. - Insect Sci. 21: 374-391 Go to original source...
  28. Lowery D.T., Smirle M.J., Foottit R.G. & Beers E.H. 2006: Susceptibilities of apple aphid and spirea aphid collected from apple in the Pacific Northwest to selected insecticides. - J. Econ. Entomol. 99: 1369-1374 Go to original source...
  29. Lushai G., Foottit R., Maw E. & Barette R. 2004: Genetic variation in the green apple aphid, Aphis pomi De Geer (Aphididae, Homoptera) detected using microsatellite DNA flanking sequences. In Simon J.C., Dedryver C.A., Rispe C. & Hulle M. (eds): Aphids in a New Millennium. INRA, Paris, pp. 245-251
  30. Naaum A.M., Foottit R.G., Maw H.E.L. & Hanner R. 2012: Differentiation between Aphis pomi and Aphis spiraecola using multiplex real-time PCR based on DNA barcode sequences. - J. Appl. Entomol. 136: 704-710 Go to original source...
  31. Nieto Nafria J.M., Andreev A.V., Binazzi A., Mier Durante M.P., Perez Hidalgo N., Rakauskas R. & Stekolshchikov A.V. 2010: Aphidoidea. Fauna Europaea. Version 2.2. http://www.faunaeur.org
  32. Palmer M.A. 1952: Aphids of the Rocky Mountain Region. Hirschfeld Press, Denver, 452 pp
  33. Patch E.M. 1923: The summer food plants of the green apple aphid. - Maine AES Bull. 313: 45-68
  34. Patch E.M. 1929: The apple aphid and the citrus aphid: Aphis pomi DeGeer and A. spiraecola Patch. - J. Econ. Entomol. 22: 698 Go to original source...
  35. Posada D. 2008: jModelTest: Phylogenetic model averaging. - Mol. Biol. Evol. 25: 1253-1256 Go to original source...
  36. Rakauskas R. & Buga S. 2010: Contribution to the knowledge of the aphid (Hemiptera, Sternorrhyncha: Aphidoidea) fauna of the Gorodok Highland, Belarus. - Acta Zool. Lituan. 20: 205-224 Go to original source...
  37. Rakauskas R.P. & Rupais A.A. 1983: Biology of the green apple aphid in Lithuania. - Acta Entomol. Lituan. 6: 20-30 [in Russian]
  38. Rakauskas R., Turcinaviciene J. & Basilova J. 2011: How many species are there in the subgenus Bursaphis (Hemiptera: Sternorrhyncha: Aphididae)? COI evidence. - Eur. J. Entomol. 108: 469-479 Go to original source...
  39. Ronquist F. & Huelsenbeck J.P. 2003: MRBAYES 3: Bayesian phylogenetic inference under mixed models. - Bioinformatics 19: 1572-1574 Go to original source...
  40. Singh R.S. & Rhomberg L. 1984: Allozyme variation, population structure, and sibling species in Aphis pomi. - Can. J. Genet. Cytol. 26: 364-373 Go to original source...
  41. Smirle M.J., Zurowski C.L., Lowery D.T. & Foottit R.G. 2010: Relationship of insecticide tolerance to esterase enzyme activity in Aphis pomi and Aphis spiraecola (Hemiptera: Aphididae). - J. Econ. Entomol. 103: 374-378 Go to original source...
  42. Stoeckli S., Mody K. & Dorn S. 2008: Aphis pomi (Hemiptera: Aphididae) population development, shoot characteristics, and antibiosis resistance in different apple genotypes. - J. Econ. Entomol. 101: 1341-1348 Go to original source...
  43. Stroyan H.L.G. 1985: Aphids - Aphidinae (Macrosiphini). In: Handbooks for the Identification of British Insects. Royal Entomological Society, London, 414 pp
  44. Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739 Go to original source...
  45. Tsai J.H. & Wang J.J. 2001: Effects of host plants on biology and life table parameters of Aphis spiraecola (Homoptera: Aphididae). - Environ. Entomol. 30: 44-50 Go to original source...
  46. Turcinaviciene J., Pedersen B.V. & Rakauskas R. 2006: Phylogenetic relationships in the "grossulariae" species group of the genus Aphis (Hemiptera: Sternorrhyncha: Aphididae): Molecular evidence. - Eur. J. Entomol. 103: 597-604 Go to original source...
  47. von Dohlen C.D. & Teulon D.A.J. 2003: Phylogeny and historical biogeography of New Zealand indigenous Aphidini aphids (Hemiptera, Aphididae): An hypothesis. - Ann. Entomol. Soc. Am. 96: 107-116 Go to original source...
  48. von Dohlen C.D., Rowe C.A. & Heie O.E. 2006: A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. - Mol. Phylogenet. Evol. 38: 316-329 Go to original source...
  49. Wang J.F., Jiang L.Y. & Qiao G.X. 2011: Use of a mitochondrial COI sequence to identify species of the subtribe Aphidina (Hemiptera, Aphididae). - ZooKeys 122: 1-17 Go to original source...
  50. Westigard P.H. & Madsen H.F. 1964: Oviposition and egg dispersion of apple aphid. - J. Econ. Entomol. 57: 597-600 Go to original source...
  51. Wieczorek K., Bartosz J., Plachno B.J. & Swiatek P. 2011: Comparative morphology of the male genitalia of Aphididae (Insecta, Hemiptera). Part 1. - Zoomorphology 130: 289-303 Go to original source...
  52. Yovkova M., Petrovic-Obradovic O., Tasheva-Terzieva E. & Pencheva A. 2013: Aphids (Hemiptera, Aphididae) on ornamental plants in greenhouses in Bulgaria. - ZooKeys 319: 347-361 Go to original source...