Abstract
Gall-forming aphid species Tetraneura nigriabdominalis and T. fusiformis and its closely related species are taxonomically revised. By referring to the original descriptions, the name T. nigriabdominalis (Sasaki, 1899) is discarded as an erroneous combination, and T. akinire Sasaki, 1904 is adopted as a valid name. The T. akinire species group is defined as having long claws in the first instar nymphs of the root generation. Of the T. akinire species group distributed in Korea and Japan, T. ovaliformis sp. nov., which induces globular galls on the leaves of Ulmus davidiana var. japonica, is described, and T. akinire and T. sorini Hille Ris Lambers, 1970 are redescribed. A molecular phylogeny based on partial sequences of mitochondrial cytochrome c oxidase subunit I (COI) indicates that T. akinire is composed of two clusters, one (type A) which is distributed widely from Europe to East Asia on Ulmus spp., and the other (type B) which is found in Hokkaido, northern Japan on U. davidiana var. japonica and in tropical regions as anholocyclic lineages. Tetraneura fusiformis Matsumura, 1917, which has often been treated as a junior synonym of T. nigriabdominalis, likely corresponds to type B. The taxonomic status of T. fusiformis is discussed and this species is tentatively considered as a junior synonym of T. akinire sensu novo.
References
Akimoto, S. (1983) A revision of the genus Eriosoma and its allied genera in Japan (Homoptera: Aphidoidea). Insecta Matsumurana, new series, 27, 37–106.
Akimoto, S. (1985) Taxonomic study on gall aphids, Colopha, Paracolopha and Kaltenbachiella (Aphidoidea: Pemphigidae) in East Asia, with special reference to their origins and distributional patterns. Insecta Matsumurana, new series, 30, 1–79.
Akimoto, S. (1995) Coexistence and weak amensalism of congeneric gall-forming aphids on the Japanese elm. Researches on Population Ecology, 37, 81–89. https://doi.org/10.1007/BF02515763
Akimoto, S. & Yamaguchi, Y. (1994) Phenotypic selection on the process of gall formation of a Tetraneura aphid (Pemphigidae). Journal of Animal Ecology, 63, 727–738. https://doi.org/10.2307/5237
Akimoto, S. & Yamaguchi, Y. (1997) Gall usurpation by the gall-forming aphid, Tetraneura sorini (Insecta Homoptera). Ethology, Ecology and Evolution, 9, 159–168. https://doi.org/10.1080/08927014.1997.9522894
Abramoff, M.D., Magalhaes, P.J. & Ram, S.J. (2004) Image processing with ImageJ. Biophotonics International, 11, 36–42.
Bate-Smith, A.C. & Richens, R.H. (1973) Flavonoid chemistry and taxonomy in Ulmus. Biochemical Systematics, 1, 141–146. https://doi.org/10.1016/0305-1978(73)90004-5
Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World’s Trees. CAB International, Wallingford, 987 pp + 16 plates.
Blackman, R.L. & Eastop, V.F. (2021) Aphids on the world’s plants: an online identification and information guide. Available from http://www.aphidsonworldsplants.info/ (accessed 08 June 2021)
Chakrabarti, S. & Maity, S.P. (1982) Aphids (Homoptera: Aphididae) of North West India: new subgenus, new species and new records of root inhabiting aphids. Entomon, 3, 265–272.
Delfino, M.A. (1982) Presence of Tetraneura nigriabdominalis (Sasaki, 1899) (Homoptera: Eriosomatidae) in Argentina. Revista de la Sociedad Entomológica Argentina, 41, 111–113.
Delmotte, F., Sabater, B., Leterme, N., Latorre, A., Sunnucks, P., Rispe, C. & Simon, J-C. (2003) Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution, 57, 1291–1303. https://doi.org/10.1111/j.0014-3820.2003.tb00337.x
Eastop, V.F. (1958) A Study of the Aphididae of East Africa. Colonial Research Publication, HMSO, London, 126 pp.
Eastop, V.F. (1966) A taxonomic study of the Australian Aphidoidea (Homoptera). Australian Journal of Zoology, 14, 399–592. https://doi.org/10.1071/ZO9660399
Eastop, V.F. & Blackman, R.L. (2005) Some new synonyms in Aphididae (Hemiptera: Sternorrhyncha). Zootaxa, 1089 (1), 1–36. https://doi.org/10.11646/zootaxa.1089.1.1
Eastop, V.F. & Hille Ris Lambers, D. (1976) Survey of the World's Aphids. Dr. W. Junk. The Hague, 573 pp.
Elias, T.S. (1970) The genera of Ulmaceae in the southeastern United States. Journal of the Arnold Arboretum, 51, 18–40. https://doi.org/10.5962/bhl.part.7037
Van Emden, H.V. (1972) Aphid Technology. With Special Reference to the Study of Aphids in the Field. Academic Press, London, 344pp.
Favret, C. (2021) Aphid species file, version 5.0/5.0. available from http://AphidSpeciesFile.org (accessed 8 June 2021)
Foottit, R.G., Halbert, S.E., Miller, G.L., Maw, E. & Russell, L.M. (2006) Adventive aphids (Hemiptera: Aphididae) of America north of Mexico. Proceedings of the Entomological Society of Washington, 108, 583–610.
Foottit, R.G. & Richard, W.R. (1993) The Genera of the Aphids of Canada (Homoptera: Aphidoidea and Phylloxeroidea) (The Insects and Arachnids of Canada Part 22). Research Branch, Agriculture Canada, 766 pp.
Foottit, R.G., Maw, H.E.L., Pike, K.S. & Messing, R.H. (2012) The aphids (Hemiptera: Aphididae and Adelgidae) of Hawaii, annotated list and key to species of an adventive fauna. Pacific Science, 66, 1–30. https://doi.org/10.2984/66.1.1
Heie, O.E. (1967) Aphids from the Philippines and the Bismarck Islands, with description of a new species of Greenideoida. Entomologiske Meddelelser, 35, 333–340.
Heie, O.E. (1980) The Aphodoidea (Hemiptera) of Fennoscandia and Denmark. I. (Fauna Entomologica Scandinavica Vol. 9). Scandinavian Scientific Press Ltd, Klampenborg, Denmark, 236 pp.
Hille Ris Lambers, D. (1970) A study of Tetraneura Hartig, 1841 (Homoptera, Aphididae), with descriptions of a new subgenus and new species. Bollettino di Zoologia agrarian e di Bachicoltura, Serie Ⅱ, ⅴ.9, 1968–69, 21–101.
Kearney, M. (2005) Hybridization, glaciation and geographical parthenogenesis. Trends in Ecology & Evolution, 20, 495–502. https://doi.org/10.1016/j.tree.2005.06.005
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi.org/10.1093/molbev/msy096
Lee, W. & Akimoto, S. (2015) Development of new barcoding loci in gall-forming aphids (Eriosomatinae: Eriosomatini): Comparing three mitochondrial genes, ATP6, ATP8, and COI. Journal of Asia-Pacific Entomology, 18, 267–275. https://doi.org/10.1016/j.aspen.2015.03.003
Lee, W., Otsuki, A. & Akimoto, S. (2012) Rapid diagnostic method for discriminating two types of COI sequences in the gall-forming aphid Tetraneura nigriabdominalis (Hemiptera: Aphididae) by multiplex polymerase chain reaction. Entomological Science, 16, 243–247. https://doi.org/10.1111/j.1479-8298.2012.00557.x
Matsumura, S. (1917) Synopsis of the Pemphigidae of Japan. In: A Collection of Essays for Mr Yasushi Nawa, Gifu, pp. 39–94.
Matsumura, S. (1917a) Applied Entomology part 1. Keiseisha Publishing. 731 pp. [in Japanese]
Mifsud, D., Pérez Hidalgo, N. & Barbagallo, S. (2009) Aphids (Hemiptera: Aphidoidea) associated with native trees in Malta (Central Mediterranean). Bulletin of the Entomological Society of Malta, 2, 81–93.
Mille, C., Jourdan, H., Cazères, S., Maw, E. & Foottit, R. (2020) New data on the aphid (Hemiptera, Aphididae) fauna of New Caledonia: some new biosecurity threats in a biodiversity hotspot. ZooKeys, 943, 53–89. https://doi.org/10.3897/zookeys.943.47785
Mordvilko, A.K. (1935) Die Blattläuse mit unvollständigem Generationszyklus und ihre Entstehung. Ergebnisse und Fortschritte der Zoologie, 8, 36–328.
Muramatsu, K. & Akimoto, S. (2014) Drastic changes in host preference in a gall-parasitic flea weevil, Orchestes hustachei, during the last decade. Ecological Entomology 39, 531–538. https://doi.org/10.1111/een.12132
Muramatsu, K. & Akimoto, S. (2016) Spatiotemporal fluctuations in natural selection acting on the gall-parasitic aphid Tetraneura sorini. Journal of Evolutionary Biology, 29, 1423–1436. https://doi.org/10.1111/jeb.12881
Pal, P.K. & Raychaudhuri, D.N. (1978) A note on the aphids (Homoptera: Aphididae) infesting subaerial parts of grasses and sedges in north east India. Science and Culture, 44, 275–276.
Roberti, D. (1972) Contributi alla conoscenza degli afidi d’Italia. VIII. La Tetraneura (Tetraneurella) akinire Sasaki. Estratto da Entomologica, VIII, 141–205.
Sano, M. & Akimoto, S. (2011) Morphological phylogeny of gall-forming aphids of the tribe Eriosomatini (Aphididae: Eriosomatinae). Systematic Entomology, 36, 607–627. https://doi.org/10.1111/j.1365-3113.2011.00589.x
Sasaki, C. (1899) Manual of Insect Pests of Crops in Japan. Keigyosha, Tokyo. 439 pp. [in Japanese]
Sasaki, C. (1904) A gall-forming aphid on Ulmus parvifolia. Zoological Magazine, 193, 403–405. [in Japanese]
Simbaqueba-Cortés, R., Serna, F., Vergara-Navarro, E.V. & Quiroz-Gamboa, J.A. (2015) New record and re-description of a gall-forming aphid (Hemiptera: Aphididae), commonly confused in the north of South America, associated with an ant (Hymenoptera: Formicidae). Agronomía Colombiana, 33, 113–117. https://doi.org/10.15446/agron.colomb.v33n1.49368
Simon, J.C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology & Evolution, 17, 34–39. https://doi.org/10.1016/S0169-5347(01)02331-X
Singh, G. & Singh, R. (2017) Updated check-list of Indian Eriosomatinae (Aphidinae: Aphididae: Hemiptera) and their food plants. Journal of Entomology and Zoology studies, 5, 921–936.
Tanaka, T. (1957) Taxonomy and distribution of some subterranean aphids injurious to the upland. Scientific Pest Control, Kyoto University, 22, 168–176.
Tanaka, T. (1961) The rice root aphid, their ecology and control. Special Bulletin of the College of Agriculture Utsunomiya University, 10, 1–83. [in Japanese with English summary]
Tomisawa, R. & Akimoto, S. (2004). Host range and host preference of a flea weevil, Orchestes hustachei, parasitizing aphid galls. Entomologocal Science, 7, 21–30. https://doi.org/10.1111/j.1479-8298.2003.00038.x
Tong, X. & Akimoto, S. (2019) Female-female competition leads to female-biased sex allocation and dimorphism in brood sex composition in a gall-forming aphid. Functional Ecology, 33, 457–466. https://doi.org/10.1111/1365-2435.13248
Vadivelu, S., Mohanasundaram, M. & Rao, P.V.S. (1975) Record of parasites and predators on some South Indian crop pests. Indian Journal of Entomology, 37, 100–101.
Villalobos Muller, W., Pérez Hidalgo, N., Mier Durante, M.P. & Nieto Nafría, J.M. (2010) Aphididae (Hemiptera: Sternorrhyncha) from Costa Rica, with new records for Central America. Boletín de la Asociación Española de Entomología, 34, 145–182.
Walczak, U., Borowiak-Sobkowiak, B. & Wilkaniec, B. (2017) Tetraneura (Tetraneurella) nigriabdominalis (Hemiptera: Aphidoidea) – a species extending its range in Europe, and morphological comparison with Tetraneura (Tetraneura) ulmi. Entomologica Fennica, 28, 21–26. https://doi.org/10.33338/ef.84672
Wiegrefe, S.J., Sytsma, K.J. & Guries, R.P. (1994) Phylogeny of elms (Ulmus, Ulmaceae): molecular evidence for a sectional classification. Systematic Botany, 19, 590–612. https://doi.org/10.2307/2419779
Zhang, G. & Qiao, G. (1997) Three new species and two new subspecies of Eriosomatinae (Homoptera: Aphidoidea: Pemphigidae) from China. Acta Entomologica Sinica, 40, 393–401.
Zhang, G.X., Zhang, W.Y. & Zhong, T.S. (1991) Studies on the genus Tetraneura Hartig, 1841 from China (Homoptera: Pemphigidae) with descriptions of new species and subspecies. Sinozoologia, 8, 205–236.
Zhang, H-C., Zhang, D. & Qiao, G.X. (2008) Association of aphid life stages using DNA sequences: A case study of tribe Eriosomatini (Hemiptera: Aphididae: Pemphiginae). Insect Science, 15, 545–551. https://doi.org/10.1111/j.1744-7917.2008.00244.x