Advertisement

Biologia

pp 1–13 | Cite as

Aphids of the family Adelgidae in Lithuania: distribution, host specificity and molecular (mitochondrial COI and nuclear EF-1α) diversity

  • Jekaterina HavelkaEmail author
  • Jurij Danilov
  • Rimantas Rakauskas
Original Article
  • 8 Downloads

Abstract

Based on the original research of 2017–2018, also reference data, four aphid species and five species complexes of the family Adelgidae listed for Lithuanian fauna. Pineus (Pineus) strobi (Hartig, 1839) is a new species for the fauna of Lithuania. Summarized information on the distribution and host specificity of adelgid species in Lithuania is presented. The most common species recorded from all geographical regions of Lithuania were the ones belonging to the species complexes Adelges laricis – A. tardus, Pineus orientalis – P. pini, Sacchiphantes viridis – S. abietis and Gilletteella cooleyiG. coweni. Six species of Adelgidae inhabit host plants of the genus Picea, three live on Larix, three – on Pinus, two – on Abies, one – on Pseudotsuga. Partial sequences of mitochondrial (COI) and nuclear (EF-1α) DNA of Lithuanian samples were analysed in comparison with available data from GeneBank representing samples from Central Europe. Pairwise distances of COI and EF-1α fragments between samples belonging to species complexes Adelges laricis – A. tardus, Dreyfusia nordmannianae – D. piceae, Sacchiphantes viridis – S. abietis, Gilletteella cooleyiG. coweni and Pineus orientalisP. pini suggest each species complex being a single species.

Keywords

Adelgidae Taxonomy Distribution Europe Mitochondrial COI Nuclear EF-1α 

Notes

Acknowledgments

This research was funded by grant No P-MIP-17-365 from the Research Council of Lithuania. Authors highly acknowledge an important methodological help of Jan Havelka (Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic) when performing the present research. Administrations of Dubrava Arboretum, Botanical gardens of Vilnius University, Vytautas Magnus University, Klaipėda University and Šiauliai University have kindly ensured aphid sampling in respective dendrological collections.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Albrecht AC (2017) Illustrated identification guide to the Nordic aphids feeding on conifers (Pinophyta) (Insecta, Hemiptera, Sternorhyncha, Aphidomorpha). Eur J Taxon 338:1–160.  https://doi.org/10.5852/ejt.2017.338 CrossRefGoogle Scholar
  2. Annand PN (1928) A contribution towards a monograph of the Adelginae (Phylloxeridae) of North America. Stanford University Press, Palo AltoGoogle Scholar
  3. Binazzi A (2000) Notes on and key to winged forms of adelgids recorded from Italy (Homoptera, Aphidoidea, Adelgidae). Redia 83:187–215Google Scholar
  4. Blackman RL (1974) Life-cycle variation of Myzus persicae (Sulz.) (Hom., Aphididae) in different parts of the world, in relation to genotype and environment. Bull Entomol Res 63:595–607.  https://doi.org/10.1017/S0007485300047830 CrossRefGoogle Scholar
  5. Blackman RL, Brown PA (1991) Morphometric variation within and between populations of Rhopalosiphum maidis with a discussion of the taxonomic treatment of permanently parthenogenetic aphids (Homoptera: Aphididae). Entomol Gen 16(2):97–113.  https://doi.org/10.1127/entom.gen/16/1991/097 CrossRefGoogle Scholar
  6. Blackman RL, Eastop VF (1984) Aphids on the World’s crops: an identification and information guide. Wiley, ChichesterGoogle Scholar
  7. Blackman RL, Eastop VF (2019) Aphids on the World’s plants: an identification and information guide. http://www.aphidsonworldsplants.info/. Accessed 14 March 2019
  8. Börner CV, Heinze K (1957) Aphidina-Aphidoidea. In: Blunck H (ed) Tierische Schädlinge an Nutzpflanzen, Homoptera, 2 Teil. Paul Parey, Berlin, pp 323–355Google Scholar
  9. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659.  https://doi.org/10.1046/j.1365-294x.2000.01020.x CrossRefPubMedGoogle Scholar
  10. Durak R, Lachowska-Cierlik D, Bartoszewski S (2014) Relationships within aphids Cinara (Cupressobium) (Hemiptera) based on mitochondrial and nuclear DNA sequences. J Appl Genet 55:89–96.  https://doi.org/10.1007/s13353-013-0184-7 CrossRefPubMedGoogle Scholar
  11. Earle CJ (2019) The Gymnosperm Database https://www.conifers.org/. Accessed 30 Nov 2018
  12. Eichhorn O (1989) Zum Generations- und Wirtswechsel der Fichtengallenläuse, Sacchiphantes spp. (Hom., Adelgidae). J Appl Entomol 108:44–53.  https://doi.org/10.1111/j.1439-0418.1989.tb00431.x CrossRefGoogle Scholar
  13. Eichhorn O, Carter CI (1978) Investigation into conifer woolly aphids (Hemiptera: Adelgidae) in Japan, with the descriptions of two new species. Z Angew Ent 86:273–289.  https://doi.org/10.1111/j.1439-0418.1978.tb01934.x CrossRefGoogle Scholar
  14. Favret C, Havill NP, Miller GL, Sano M, Victor B (2015) Catalog of the adelgids of the world (Hemiptera, Adelgidae). ZooKeys 534:35–54.  https://doi.org/10.3897/zookeys.534.6456 CrossRefGoogle Scholar
  15. Foottit RG (1997) Recognition of parthenogenetic insect species. In: Claridge MF, Dawah HA, Wilson MR (eds) Species: the units of biodiversity. Chapman and Hall, London, pp 291–307Google Scholar
  16. Foottit RG, Maw HEL, von Dohlen CD, Hebert PDN (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Mol Ecol Resour 8:1189–1201.  https://doi.org/10.1111/j.1755-0998.2008.02297.x CrossRefPubMedGoogle Scholar
  17. Foottit RG, Maw HEL, Havill NP, Ahern RG, Montgomery ME (2009) DNA barcodes to identify species and explore diversity in the Adelgidae. Mol Ecol Resour 9(Suppl. 1):188–195.  https://doi.org/10.1111/j.1755-0998.2009.02644.x CrossRefPubMedGoogle Scholar
  18. Frey W, Lösch R (2010) Geobotanik: Pflanzen und Vegetation in Raum und Zeit, 3rd edn. Spektrum, HeidelbergCrossRefGoogle Scholar
  19. Havelka J, Danilov J, Havelka J, Starý P, Rakauskas R (2019) Aphid species of the family Adelgidae (Hemiptera: Adelgoidea) in Lithuania: an overview.  Monographs of the Upper Silesian Museum 10:73-88Google Scholar
  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  21. Havill NP, Foottit RG (2007) Biology and evolution of Adelgidae. Annu Rev Entomol 52:325–349.  https://doi.org/10.1146/annurev.ento.52.110405.091303 CrossRefPubMedGoogle Scholar
  22. Havill NP, Foottit RG, von Dohlen CD (2007) Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics. Mol Phylogenet Evol 44:357–370.  https://doi.org/10.1016/j.ympev.2006.11.008 CrossRefPubMedGoogle Scholar
  23. Holman J (2009) Host plant catalog of aphids: Palaearctic region. Springer, DordrechtCrossRefGoogle Scholar
  24. Holman J, Pintera A (1977) Aphidodea. Acta Faunistica Entomol Mus Nat Pragae 4:101–116Google Scholar
  25. Juronis V (2003) Aphids – dangerous pests of firs (Abies spp.) in Lithuania. Aphids and other Hemipterous Insects 9:63–67Google Scholar
  26. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  27. Lampel G, Meier W (2003) Hemiptera: Sternorrhyncha – Aphidina. Teil 1: non-Aphididae. In: Burckhardt D (ed) Fauna Helvetica 2. Olivier Attinger, Chaumont, pp 250–266Google Scholar
  28. Lee W, Kim H, Lim J, Choi HR, Kim Y, Kim YS, Kim YS, Ji JY, Foottit RG, Lee S (2011) Barcoding aphids (Hemiptera: Aphididae) of the Korean Peninsula: updating the global data set. Mol Ecol Resour 11:32–37.  https://doi.org/10.1111/j.1755-0998.2010.02877.x CrossRefPubMedGoogle Scholar
  29. Meusel H, Jäger EJ (eds) (1992) Vergleichende Chorologie der Zentraleuropäischen Flora, III. Gustav Fischer Verlag, JenaGoogle Scholar
  30. Nieto Nafría JM, Andreev AV, Binazzi A, Mier Durante MP, Pérez Hidalgo NJ, Rakauskas R, Stekolshchikov AV (2013) Fauna Europaea: Aphidoidea. Fauna Europaea version 2018 https://fauna-eu.org. Accessed 14 Feb 2019
  31. Osiadacz B, Halaj R (2009) The aphids (Hemiptera: Sternorrhyncha: Aphidinea) of Poland. A distributional checklist. Pol Entomol Monogr 6:1–96Google Scholar
  32. Osiadacz B, Halaj R (2010) Systematic review of aphids (Hemiptera: Sternorrhyncha: Aphidomorpha) of Poland with host plant index. A Monographic Survey. Silesian Natural History Monographs. Vol. 1. Tarnowskie Góry Institute and Museum, PolandGoogle Scholar
  33. Ozolinčius R, Navasaitis M, Balevičienė J, Smaliukas D (2003) Dendroflora of Lithuania. Lututė, Kaunas. [in Lithuanian]Google Scholar
  34. Rakauskas R (2007) Aphis holoenotherae sp. n. an European sibling of the Nearctic Aphis oenotherae Oestlund. Aphids and other Hemipterous Insects 13:15–33Google Scholar
  35. Rakauskas R, Rupais A, Juronis V (1992) The check-list of Lithuanian Aphidodea. In: New and rare for Lithuania insect species. Records and descriptions of 1992. Vol. 2, Lith Entomol Soc, Inst Ecol, Vilnius Univ, Vilnius, pp 83–100Google Scholar
  36. Rakauskas R, Havelka J, Bašilova J (2008) Contribution to the knowledge of the aphid (Hemiptera, Sternorrhyncha: Phylloxeroidea, Aphidoidea) fauna of the Curonian Spit, Lithuania. Acta Zool Lituanica 18(2):90–107.  https://doi.org/10.2478/v10043-008-0013-0 CrossRefGoogle Scholar
  37. Rakauskas R, Turčinavičienė J, Bašilova J (2011) How many species are there in the subgenus Bursaphis (Hemiptera: Sternorrhyncha: Aphididae)? COI evidence. Eur J Entomol 108:469–479.  https://doi.org/10.14411/eje.2011.060 CrossRefGoogle Scholar
  38. Redlich S, Clemens J, Martin KF, Bader MKF, Pendrigh D, Perret-Gentil A, Godsoe W, Teulon DAJ, Brockerhoff EG (2019) Identifying new associations between invasive aphids and Pinaceae trees using plant sentinels in botanic gardens. Biol Invasions 21:217–228.  https://doi.org/10.1007/s10530-018-1817-x CrossRefGoogle Scholar
  39. Roversi PF, Binazzi A (1996) Life cycle of the Douglas-fir woolly aphid Gillettiella coweni (Gillette) in Central Italy (Homoptera Adelgidae). Redia 79:241–245Google Scholar
  40. Rupais A (1989) The aphids (Aphidoidea) of Latvia. Zinatne, Rīga. [in Russian]Google Scholar
  41. Rupais A, Juronis V (1983) Aphids found in Kaunas and its environs in 1963-1980 (1. Families Adelgidae, Phylloxeridae, Pemphigidae, Lachnidae, Mindaridae, Anoeciidae, Thelaxidae, Callaphididae, Chaitophoridae). Proc Acad Sci Lithuanian SSR, Series C 2(82):63–69Google Scholar
  42. Sanchis A, Michelena JM, Latorre A, Quicke DLJ, Gardenfors U, Belshaw R (2001) The phylogenetic analysis of variable-length sequence data: elongation factor–1a introns in European populations of the parasitoid wasp genus Pauesia (Hymenoptera: Braconidae: Aphidiinae). Mol Biol Evol 18(6):1117–1131CrossRefGoogle Scholar
  43. Sano M, Tabuchi K, Ozaki K (2008) A holocyclic life cycle in a gall-forming adelgid, Adelges japonicus (Homoptera: Adelgidae). J Appl Entomol 132:557–565.  https://doi.org/10.1111/j.1439-0418.2008.01299.x CrossRefGoogle Scholar
  44. Sano M, Havill NP, Ozaki K (2011) Taxonomic identity of a galling adelgid (Hemiptera: Adelgidae) from three spruce species in Central Japan. Entomol Sci 14:94–99.  https://doi.org/10.1111/j.1479-8298.2010.00417.x CrossRefGoogle Scholar
  45. Sano M, Ozaki K (2012) Variation and evolution of the complex life cycle in Adelgidae (Hemiptera). Entomol Sci 15:13–22.  https://doi.org/10.1111/j.1479-8298.2011.00483.x CrossRefGoogle Scholar
  46. Steffan AW (1964) Problems of evolution and speciation in Adelgidae (Homoptera: Aphidoidea). Can Entomol 96:155–157.  https://doi.org/10.4039/Ent96155-1 CrossRefGoogle Scholar
  47. Steffan AW (1970) Die eidonomischen und zytologischen Grundlagen bei der Enstehung anholozyklisch-parthenogenetischer Adelgidae-Species (Homoptera: Aphidina). J Appl Entomol 65:444–452.  https://doi.org/10.1111/j.1439-0418.1970.tb04008.x CrossRefGoogle Scholar
  48. Toenshoff ER, Gruber D, Horn M (2012a) Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol 14(5):1284–1295.  https://doi.org/10.1111/j.1462-2920.2012.02712.x CrossRefPubMedGoogle Scholar
  49. Toenshoff ER, Penz T, Narzt T, Collingro A, Schmitz-Esser S, Pfeiffer S, Klepa W, Wagner M, Weinmaier T, Rattei T, Horn M (2012b) Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 6:384–396.  https://doi.org/10.1038/ismej.2011.102 CrossRefPubMedGoogle Scholar
  50. Toenshoff ER, Szabó G, Gruber D, Horn M (2014) The pine bark adelgid, Pineus strobi, contains two novel bacteriocyte-associated gammaproteobacterial symbionts. Appl Environ Microbiol 80(3):878–885.  https://doi.org/10.1128/AEM.03310-13 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Tzvelev N (2000) Opredelitel sosudistych rastenij severo-zapadnoj Rossii [Manual of the vascular plants of North -West Russia]. Spb State CHF Academy Press, Sankt Peterburg. [in Russian]Google Scholar
  52. Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968.  https://doi.org/10.1111/j.1471-8286.2007.01821.x CrossRefGoogle Scholar
  53. Wojciechowski W, Depa L, Kanturski M, Wegierek P, Wieczorek K (2015) An annotated checklist of the aphids (Hemiptera: Aphidomorpha) of Poland. Pol J Entomol 84:383–420.  https://doi.org/10.1515/pjen-2015-0033 CrossRefGoogle Scholar
  54. Wojciechowski W, Depa L, Halgoš J, Matečny JL, Kanturski M (2016) Aphids of Slovakia. KO & KA, BratislavaGoogle Scholar
  55. Žurovcová M, Havelka J, Starý P, Věchtová P, Chundelová D, Jarošová A, Kučerová L (2010) “DNA barcoding” is of limited value for identifying adelgids (Hemiptera: Adelgidae) but supports traditional morphological taxonomy. Eur J Entomol 107:147–156.  https://doi.org/10.14411/eje.2010.020 CrossRefGoogle Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2019

Authors and Affiliations

  1. 1.Institute of BiosciencesVilnius UniversityVilniusLithuania

Personalised recommendations