Abstract
A new genus of Chamaemyiidae (Diptera: Lauxanioidea) is described, namely Leucotaraxis gen. nov. (type species Leucopis atrifacies Aldrich; other included species Leucotaraxis argenticollis (Zetterstedt), comb. nov., Leucotaraxis piniperda (Malloch), comb. nov., and Leucotaraxis sepiola sp. nov.). These species are predators of Adelgidae (Hemiptera) infesting Pinaceae. Leucotaraxis argenticollis is Holarctic, while the other three species are Nearctic. The phylogeny of Leucotaraxis with other representatives of Chamaemyiidae was elucidated using mitochondrial and nuclear DNA sequences and the genus was found to be monophyletic. Egg and puparial stages are discussed or described and illustrated for all species except Leucotaraxis sepiola. A key is provided to all species of Chamaemyiidae known to attack Pinaceae-infesting Sternorrhyncha, an annotated list of these taxa is provided, and a habitus photograph is provided for each genus with such species. In addition, a lectotype is designated for Leucopis olivacea Meijere, and it is synonymized under Neoleucopis obscura (Haliday), syn. nov.
References
Aldrich, J.M. (1925) A new Leucopis from San Francisco. Pan-Pacific Entomologist, 1 (4), 152.
Barriault, S., Soares, A.O., Gaimari, S.D. & Lucas, E. (2018) Leucopis glyphinivora Tanasijtshuk (Diptera: Chamaemyiidae), a new aphidophagous biocontrol agent; development, survival and comparison with Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Bulletin of Entomological Research, 109 (4), 472–478. https://doi.org/10.1017/S0007485318000767
Bertone, M.A., Courtney, G.W. & Wiegmann, B.M. (2008) Phylogenetics and temporal diversification of the earliest true flies (Insecta: Diptera) based on multiple nuclear genes. Systematic Entomology, 33, 668–687. https://doi.org/10.1111/j.1365-3113.2008.00437.x
Blanchard, E.E. (1964) Nuevos predatores de la familia Chamaemyiidae con información sobre otras especies argentinas (Dipt.). Revista de Investigaciones Agropecuarias, Serie 5, Patologia Vegetal, 1, 133–150. [in Spanish]
Cole, F.R. & Schlinger, E.I. (1969) The Flies of Western North America. University of California Press, Berkeley and Los Angeles, California, 693 pp.
Culliney, T.W., Beardsley Jr., J.W. & Drea, J.J. (1988) Population regulation of the Eurasian pine adelgid (Homoptera: Adelgidae) in Hawaii. Journal of Economic Entomology, 81, 142–147. https://doi.org/10.1093/jee/81.1.142
Cumming, J.M. & Wood, D.M. (2009) Adult Morphology and Terminology. In: Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, N.E. & Zumbado, M. (Eds.), Manual of Central American Diptera. Vol. 1. NRC Research Press, Ottawa, pp. 9–50.
Czerny, L. (1904) Cremifania nigrocellulata, eine neue Ochthiphiline. Systematische Stellung und Gattungen-Diagnose der Ochthiphilinen. Wiener entomologische Zeitung, 23, 167–170. https://doi.org/10.5962/bhl.part.27205
Czerny, L. (1936) 51. Chamaemyiidae (Ochthiphilidae). In: Lindner E. (Ed.), Die Fliegen der Palaearktischen Region. Vol. 103. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp. 1–25.
Dietschler, N.J., Bittner, T.D., Trotter III, R.T., Fahey, T.J. & Whitmore, M.C. (2021) Biological control of hemlock woolly adelgid: Implications of adult emergence patterns of two Leucopis spp. (Diptera: Chamaemyiidae) and Laricobius nigrinus (Coleoptera: Derodontidae) larval drop. Environmental Entomology, 50 (4), 803–813. https://doi.org/10.1093/ee/nvab037
Ebejer, M.J. (2016) The first record of the genus Melanochthiphila Frey (Diptera: Chamaemyiidae) from the Palaearctic, and new data on other Chamaemyiidae from Morocco. Studia dipterologica, 22 (1), 111–120.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
Eichhorn, O. (1968) Problems of the population dynamics of silver fir woolly aphids, genus Adelges (=Dreyfusia), Adelgidae. Zeitschrift für Angewandte Entomologie, 61, 157–214. https://doi.org/10.1111/j.1439-0418.1968.tb03886.x
Gaimari, S.D. (2010) Chamaemyiidae. In: Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, N.E. & Zumbado, M. (Eds.), Manual of Central American Diptera. Vol. 2. NRC Research Press, Ottawa, pp. 997–1007.
Gaimari, S.D. (2012) A new genus and species of Chamaemyiidae (Diptera: Lauxanioidea) from South America feeding on Ceroplastes wax scales (Hemiptera: Coccidae), and status of the genus Ortalidina as a chamaemyiid. Zootaxa, 3342 (1), 39–50. https://doi.org/10.11646/zootaxa.3342.1.2
Gaimari, S.D. (2020) Two new genera of Nearctic Chamaemyiidae (Diptera: Lauxanioidea) associated with Cinara aphids (Hemiptera) on Pinus. Zootaxa, 4852 (1), 61–82. https://doi.org/10.11646/zootaxa.4852.1.3
Gaimari, S.D. (2021 in press) 76. Chamaemyiidae (Silver Flies). In: Kirk-Spriggs, A.H. & Sinclair, B.J. (Eds.), Manual of Afrotropical Diptera. Vol. 3. Brachycera: Cyclorrhapha, excluding Calyptratae. Suricata 6. African National Biodiversity Institute, Pretoria, pp. 1633–1656.
Gaimari, S.D., Milonas, P. & Souliotis, C. (2007) Notes on the taxonomy, biology and distribution of Neoleucopis kartliana (Diptera: Chamaemyiidae). Folia Heyrovskyana, Series A, 15, 7–16.
Greathead, D.J. (1995) The Leucopis spp. (Diptera: Chamaemyiidae) introduced for biological control of Pineus sp. (Homoptera: Adelgidae) in Hawaii: implications for biological control of Pineus ?boerneri in Africa. The Entomologist, 114, 83–90.
Grubin, S.M., Ross, D.W. & Wallin, K.F. (2011) Prey suitability and phenology of Leucopis spp. (Diptera: Chamaemyiidae) associated with hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environmental Entomology, 40 (6), 1410–1416. https://doi.org/10.1603/EN11127
Haliday, A.H. (1833) Catalogue of Diptera occurring about Holywood in Downshire. Entomological Magazine, 1, 147–180.
Harris, J.W.E. & Dawson, A.F. (1979) Predator release program for balsam woolly aphid Adelges piceae (Homoptera: Adelgidae) in British Columbia, Canada, 1960–1969. Journal of the Entomological Society of British Columbia, 76, 21–26.
Havill, N.P., Gaimari, S.D. & Caccone, A. (2018) Cryptic east-west divergence and molecular diagnostics for two species of silver flies (Diptera: Chamaemyiidae: Leucopis) from North America being evaluated for biological control of hemlock woolly adelgid. Biological Control, 121, 23–29. https://doi.org/10.1016/j.biocontrol.2018.02.004
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101, 14812–14817. https://doi.org/10.1073/pnas.0406166101
Humble, L.M. (1994) Recovery of additional exotic predators of balsam woolly adelgid, Adelges piceae (Ratzeburg) (Homoptera: Adelgidae), in British Columbia. The Canadian Entomologist, 126, 1101–1103. https://doi.org/10.4039/Ent1261101-4
Kohler, G.R., Stiefel, V.L., Wallin, K.F. & Ross, D.W. (2008) Predators associated with the hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environmental Entomology, 37, 494–504. https://doi.org/10.1093/ee/37.2.494
Krishnaswamy, S. & Chako, M.J. (1988) Population dynamics of Adelges knucheli and its predators in the north-western Himalayas. I. Host phase: Gallicola. Journal of Biological Control, 2, 92–96.
Malloch, J.R. (1921) Forest insects in Illinois, I. The subfamily Ochthiphilinae (Diptera, Family Agromyzidae). Bulletin of the Illinois Natural History Survey, 13, 347–361. https://doi.org/10.21900/j.inhs.v13.338
Malloch, J.R. (1933) Diptera of Patagonia and South Chile based mainly on material in the British Museum (Natural History). Part VI—Fascicle 4. Acalyptrata (Helomyzidae, Trypetidae, Sciomyzidae, Sapromyzidae, etc. British Museum (Natural History), London, pp. 171–391, 7 pls.
McAlpine, J.F. (1963) Relationships of Cremifania Czerny (Diptera: Chamaemyiidae) and description of a new species. The Canadian Entomologist, 95, 239–253. https://doi.org/10.4039/Ent95239-3
McAlpine, J.F. (1965) Chamaemyiidae. In: Stone, A., Sabrosky, C.W., Wirth, W.W., Foote, R.H & Coulson, J.R. (Eds.), A catalog of the Diptera of America north of Mexico. USA Department of Agriculture, Agricultural Handbook 276. Agricultural Research Service, U.S. Dept. of Agriculture, Washington, D.C., pp. 706–709.McAlpine, J.F. (1971) A revision of the subgenus Neoleucopis (Diptera: Chamaemyiidae). The Canadian Entomologist, 103, 1851–1874. https://doi.org/10.4039/Ent1031851-12
McAlpine, J.F. (1977) A remarkable new species of Leucopis from western Canada (Diptera: Chamaemyiidae). Proceedings of the Entomological Society of Washington, 79, 14–18.
McAlpine, J.F. (1978) A new dipterous predator of balsam woolly aphid from Europe and Canada (Diptera: Chamaemyiidae). Entomologica Germanica, 4, 349–355. https://doi.org/10.1127/entom.germ/4/1978/349
McAlpine, J.F. & Tanasijtshuk, V.N. (1972) Identity of Leucopis argenticollis and description of a new species (Diptera: Chamaemyiidae). The Canadian Entomologist, 104, 1865–1875. https://doi.org/10.4039/Ent1041865-12
McLean, I.F.G. (1982) Three species of Leucopis Meigen (Diptera: Chamaemyiidae) new to Britain. Entomologist’s Record and Journal of Variation, 94, 70–72.
Meigen, J.W. (1830) Systematische Beschreibung der bekannten europäischen zweiflügeligen Insekten. Sechster Theil. Schulz, Hamm, xi + 401 + [3] pp.
Meijere, J.C.H. de (1928) Vierde supplement op de nieuwe nammlijst van nederlandsche Diptera. Tijdschrift voor Entomologie, 71, 11–83. [in Dutch]
Mills, N.J. (1990) Biological control of forest aphid pests in Africa. Bulletin of Entomological Research, 80, 31–36. https://doi.org/10.1017/S0007485300045880
Motley, K., Havill, N.P., Arsenault-Benoit, A.L., Mayfield, A.E., Ott, D.S., Ross, D., Whitmore, M.C. & Wallin, K.F. (2017) Feeding by Leucopis argenticollis and Leucopis piniperda (Diptera: Chamaemyiidae) from the western USA on Adelges tsugae (Hemiptera: Adelgidae) in the eastern USA. Bulletin of Entomological Research, 107, 699–704. https://doi.org/10.1017/S0007485317000219
Moulton, J.K. & Wiegmann, B.M. (2004) Evolution and phylogenetic utility of CAD (rudimentary) among Mesozoic-aged Eremoneuran Diptera (Insecta). Molecular Phylogenetics and Evolution, 31, 363–378. https://doi.org/10.1016/S1055-7903(03)00284-7
Neidermeier, A.N., Ross, D.W., Havill, N.P. & Wallin, K.F. (2020) Temporal asynchrony of adult emergence between Leucopis argenticollis and Leucopis piniperda (Diptera: Chamaemyiidae), predators of the hemlock woolly adelgid (Hemiptera: Adelgidae), with implications for biological control. Environmental Entomology, 49 (4), 823–828. https://doi.org/10.1093/ee/nvaa049
Nguyen, L.-T., Schmidt, H.A., Haeseler, A. von & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
Papp, L. (1979) Korhardéklegyek—Pajzstetülegyek—Lauxaniidae—Chamaemyiidae. Fauna Hungariae, 15 (4), 1–89. [in Hungarian]
Papp, L. (1994) A new Cremifania species from Hungary (Diptera, Chamaemyiidae). Annales Historico-Naturales Musei Nationalis Hungarici, 86, 105–107.
Papp, L. (2010) A new Cremifania species from Bulgaria (Diptera, Cremifaniidae), with a proposal for wing venation terms in higher Diptera. Annales Historico-Naturales Musei Nationalis Hungarici, 102, 193–204.
Rao, V.P. (1965) Final technical report covering the period May 2, 1960 to May 1, 1965. U.S. PL–480 Project: Survey for natural enemies of Adelges spp. attacking silver fir and spruce in the Himalayas. Commonwealth Institute of Biological Control, India Station, Bangalore, 85 pp.
Rao, V.P. & Ghani, M.A. (1972) Studies on predators of Adelges spp. in the Himalayas. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, England. Miscellaneous Publication, 3, 1–116.
Raspi, A. (2008) Order Diptera, family Chamaemyiidae. Arthropod Fauna of the UAE, 1, 662–665.
Ratzeburg, J.T.C. (1844) Die Forst-Insecten oder Abbildung und Beschreibung der in den Wäldern Preussens und der Nachbarstaaten als schädlich oder nützlich bekannt gewordenen Insecten; in systematischer Folge und mit besonderer Rücksicht auf die Vertilgung der Schädlichen. Vol. 3. Die Ader-, Zwei-, Halb-, Netz- und Geradflügler. Nicolai, Berlin, vii + 314 pp., 16 pls.
Rondani С. (1848) Osservazioni sopra parecchie specie di esapodi afidicidi e sui loro nemici [part]. Nuovi Annali delle Scienze Naturali e Rendiconto delle Sessioni della Società Agraria e dell’Accademia delle Scienze dell’Instituto di Bologna, Serie 2, 8 [1847], 337–351, 432–448.
Ross, D.W., Gaimari, S.D., Kohler, G.R., Wallin, K.F. & Grubin, S.M. (2011) Chamaemyiid predators of the hemlock woolly adelgid from the Pacific Northwest. In: Reardon, R. & Onken, B. (Eds.), Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. U.S. Forest Service, Publication FHTET-2011-04. U.S. Forest Service, Morgantown, West Virginia, pp 97–106
Sano, M., Tabuchi, K. & Ozaki, K. (2008) A holocyclic life cycle in a gall-forming adelgid, Adelges japonicus (Homoptera: Adelgidae). Journal of Applied Entomology, 132, 557–565. https://doi.org/10.1111/j.1439-0418.2008.01299.x
Sluss, T.P. & Foote, B.A. (1973) Biology and immature stages of Leucopis pinicola and Chamaemyia polystigma (Diptera: Chamaemyiidae). The Canadian Entomologist, 105, 1443–1452. https://doi.org/10.4039/Ent1051443-11
Talavera, G., Lukhtanov, V., Pierce, N.E. & Vila, R. (2021) DNA barcodes combined with multilocus data of representative taxa can generate reliable higher-level phylogenies. Systematic Biology, syab038. [published online] https://doi.org/10.1093/sysbio/syab038
Tanasijtshuk, V.N. (1958) New species of the genus Leucopis (Diptera, Chamaemyiidae) from Leningrad region. Trudy Zoologicheskogo Instituta, 24, 89–98. [in Russian]
Tanasijtshuk, V.N. (1962) New and little-known species of the genus Leucopis (Diptera, Chamaemyiidae) from the European part of the USSR. Entomologicheskoye Obozreniye, 41, 220–229. [in Russian; English translation: (1962) Entomological Review, 41, 132–138]
Tanasijtshuk, V.N. (1966) New species of the genus Leucopis (Diptera, Chamaemyiidae) from south-western Kazakhstan. Trudy Zoologicheskogo Instituta Akademii Nauk SSSR, 37, 233–236. [in Russian]
Tanasijtshuk, V.N. (1968) Species of Leucopis (Diptera, Chamaemyiidae) from India. Bulletin of Entomology, Madras, 9, 6–12.
Tanasijtshuk, V.N. (1986) [Silver-flies (Chamaemyiidae)]. Fauna of the USSR. New Series 134. Dipterans. Vol. 14. Zoological Institute of the Russian Academy of Sciences, Nauka Publishers, St Petersburg, 335 pp. [in Russian]
Tanasijtshuk, V.N. (1997) A new Holarctic genus of Chamaemyiidae (Diptera). International Journal of Dipterological Research, 8 (2), 113–116.
Tanasijtshuk, V.N. (2001) On two sister species of the genus Anchioleucopis Tanasijtshuk, 1997 (Diptera, Chamaemyiidae) from the Holarctic region. Entomologicheskoye Obozreniye, 80 (4), 901–907. [in Russian; English translation: (2001) Entomological Review, 81 (5), 542–547]
Tanasijtshuk, V.N. (2002) Studies on Nearctic species of Leucopis (Diptera: Chamaemyiidae). I. The redescription of Nearctic Leucopis published before 1965. Zoosystematica Rossica, 11, 193–207.
Tanasijtshuk, V.N. (2003) Studies on Nearctic species of Leucopis (Diptera: Chamaemyiidae). II. New species. Zoosystematica Rossica, 11, 375–396.
Tanasijtshuk, V.N. (2005) Studies on Nearctic species of Leucopis (Diptera: Chamaemyiidae). III. L. annulipes Zetterstedt and a new sibling species from the Nearctic. Zoosystematica Rossica, 13 (2), 233–238.
Tanasijtshuk, V.N. (2006) Studies on Nearctic species of Leucopis (Diptera: Chamaemyiidae). IV. New species. Zoosystematica Rossica, 14 (2), 281–288. https://doi.org/10.31610/zsr/2005.14.2.281
Thunes, K.H., Skartveit, J., Gjerde, I., Stary, J., Solhoy, T., Fjellberg, A., Kobro, S., Nakahara, S., zur Strassen, R., Vierbergen, G., Szadziewski, R., Hagan, D.V., Grogan Jr., W.L., Jonassen, T., Aakra, K., Anonby, J., Greve, L., Aukema, B., Heller, K., Michelsen, V., Haenni, J.-P., Emeljanov, A.F., Douwes, P., Berggren, K., Franzen, J., Disney, R.H.L., Prescher, S., Johanson, K.A., Mamaev, B., Podenas, S., Andersen, S., Gaimari, S.D., Nartshuk, E., Søli, G.E.E., Papp, L., Midtgaard, F., Andersen, A., Tschirnhaus, M. von, Bächli, G., Olsen, K.M., Olsvik, H., Foldvari, M., Raastad, J.E., Hansen, L.O. & Djursvoll, P. (2004) The arthropod community of Scots pine (Pinus sylvestris L.) canopies in Norway. Entomologica Fennica, 15, 65–90.
Viggiani, G. & Mustica, L. (2008) Some notes on the biological control of insect pests in the island of Ischia. Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri, 62, 79–82.
Wantuch, H.A., Havill, N.P., Hoebeke, E.R., Kuhar, T.P. & Salom, S.M. (2019) Predators associated with the pine bark adelgid (Hemiptera: Adelgidae), a native insect in Appalachian forests, United States of America, in its southern range. The Canadian Entomologist, 151 (1), 73–84. https://doi.org/10.4039/tce.2018.53
Wilson, F. (1938) Notes on the insect enemies of chermes with particular reference to Pineus pini, Koch, and P. strobi, Hartig. Bulletin of Entomological Research, 29, 373–389. https://doi.org/10.1017/S0007485300026286
Zetterstedt, J.W. (1848) Diptera Scandinaviae disposita et descripta. Tomus septimus. Officina Lundbergiana, Lundae [=Lund], pp. 2581–2934.
Zetterstedt, J.W. (1855) Diptera Scandinaviae disposita et descripta. Tomus duodecimus seu supplementum tertium, continens addenda, corrigenda & emedanda tomis undecim prioribus. Officina Lundbergiana, Lundae [=Lund], pp. i–xx + 4547–4942.
Zondag, R. & Nuttall, M.J. (1989) Pineus laevis (Maskell), pine twig chermes or pine woolly aphid (Homoptera: Adelgidae). In: Cameron, P.J., Hill, R.L., Bain, J. & Thomas, W.P. (Eds.), Review of Biological Control of Invertebrate Pests and Weeds in New Zealand 1874 to 1987. CAB International Institute of Biological Control, Wallingford, Oxon, pp. 295–297.