Evolution of life cycles of nematodes parasitizing woody plants as a result of ecological and phylogenetic co-adaptations with hosts and vectors

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

Fundamental aspects in the evolution of nematodes parasitizing woody plants are reviewed. 1) Nematode faunal lists of natural refigia are useful to predict the risks of opportunistic pathogens becoming true pathogens in the forest and park communities. 2) Nematode composition in natural refugia gives a chance to identify nematode antagonists of insect vectors of dangerous fungal and nematode infections, which can be potentially used as of the biological agents for woody plants’ protection. 3) Dauers of the ancestors of wood-inhabiting nematodes played a role as a survival stage in the detritus decomposition succession, and they later acquired the functions of dispersion and adaptations for transmission using insect vectors. 4) When inspecting wilted trees, it is necessary to use dauers for diagnostics, as sexually mature nematodes may absent in tree tissues. 5) Plant parasitic nematodes originated from members of the detritus food web and retained a detritivorous phase in the life cycle as a part of the propagative generation. 6) Vectors in the life cycles of plant parasitic nematodes are inherited from the ancestral detritivorous nematode associations, rather than inserted in the dixenic life cycle of the ‘nematode-fungus-plant’ association. 7) Despite the significant difference in the duration of the nematode-tree and nematode-vector phases of the life cycle, the actual parasitic nematode specificity is twofold: firstly to the vector and secondly to the natural host plant (as demonstrated in phytotests excluding a vector).

作者简介

A. Ryss

Зоологический институт РАН

Email: nema@zin.ru

参考

  1. Павловский Е.Н. 1964. Природная очаговость трансмиссивных болезней в связи с ландшафтной эпидемиологией зооантропонозов. М., Л., Медицина, 211 с.
  2. Pavlovsky Ye.N. 1964. Natural refugia of the transmissive diseases associated with the landscape-dependent epidemiology of zoonosis and human infections. Moscow, Leningrad, 211 pp. (In Russian).
  3. Парамонов А.А. 1962. Основы фитогельминтологии. Т. 1. Москва, Наука, 480 с.
  4. Paramonov A.A. 1962. Fundamental of plant helminthology. V. 1. Moscow, Nauka, 480 pp. (In Russian).
  5. Полянина К.С. 2023. Ксилобионтные нематоды лиственных древесных растений: фауна, жизненные циклы и паразито-хозяинные отношения. Автореф. дис. … канд. биол. наук. СПб., 24 с.
  6. Polyanina K.S. 2023. Xylobiont nematodes of deciduous woody plants: fauna, life cycles and host-parasite relations. Abstract of PHD Thesis (Biology). Saint-Petersburg, Zoological Institute RAS, 24 pp. (In Russian).
  7. Полянина К.С., Рысс А.Ю. 2019. Жизненные циклы нематод, ассоциированных с болезнями лиственных деревьев. В кн.: Галактионов К.В. (ред.). Школа по теоретической и морской паразитологии. VII Всероссийская конференция с международным участием, 9-14 сентября 2019 г., Севастополь. Тезисы докладов. Севастополь, ФИЦ ИнБЮМ, 21-22.
  8. Polyanina K.S., Ryss A.Y. 2019. Life cycles of nematodes associated with diseases of deciduous trees. In: Galaktionov K.V. (ed.). School of fundamental and marine parasitology. VII All-Russian conference with international participants, September 2019, Sevastopol. Abstracts. Sevastopol, IBSS RAS, 21-22. (In Russian).
  9. Рысс А.Ю. 2009. Пути становления паразитизма у фитонематод отрядов Tylenchida и Aphelenchida. Труды Зоологического института РАН 313: 257-272.
  10. Ryss A.Y. 2009. Ways of origin of parasitism in plant parasitic nematodes of the orders Tylenchida и Aphelenchida. Proceeding of the Zoological Institute RAS 313: 257-272. (In Russian).
  11. Рысс А.Ю., Виейра П., Мота М. 2008. История расселения видов рода Bursaphelenchus (Nematoda: Aphelenchida: Parasitaphelenchidae). Доклады Академии Наук. Общая биология 419: 138-141.
  12. Ryss A.Y., Vieira P., Mota M. 2008. History of expansion of the species of the genus Bursaphelenchus (Nematoda: Aphelenchida: Parasitaphelenchidae). Doklady Akademii Nauk. Obshchaya Biologia 419: 138-141. (In Russian).
  13. Рысс А.Ю., Мокроусов М.В. 2014. Анализ климатических и биологических параметров для модели оценки риска распространения стволовых нематод Bursaphelenchus spp. и Devibursaphelenchus teratospicularis (Rhabditida: Aphelenchoidea). Паразитология 48: 454-460.
  14. Ryss A.Y., Mokrousov M.V. 2014. Analysis of climate and biological parameters for pest risk modeling of the expansion of wood inhabiting nematodes Bursaphelenchus spp. and Devibursaphelenchus teratospicularis (Rhabditida: Aphelenchoidea). Parazitologiya 48: 454- 460. (In Russian).
  15. Рысс А.Ю., Полянина К.С., Скрябина М.Д. 2018. Стволовые нематоды со сложным циклом на примере двух видов паразитов лиственных деревьев. В кн.: Галактионов К.В., Медведев С.Г., Рысс А.Ю., Фролов Ф.О. (ред.). Современная паразитология - основные тренды и вызовы. Международная конференция (VI съезд Паразитологического общества). г. Санкт-Петербург, 15-19 октября 2018 г. Спб., Издательство "Лема", 211.
  16. Ryss A.Y., Polyanina K.S., Skrjabina M.D. 2018. Wood inhabiting nematodes with the polyxenic life cycle studied on example of two species of parasites of deciduous plants. In: Galaktionov K.V., Medvedev S.G., Ryss A.Y., Frolov A.O. (eds). Modern parasitology - basic trends and challenges. VI Congress of Parasitological Society. Saint-Petersburg, Russia, October 15-19, 2018. Saint Petersburg, Lema, 211. (In Russian).
  17. Рысс А.Ю., Субботин С.А. 2017. Коэволюция стволовых нематод рода Bursaphelenchus Fuchs, 1937 с насекомыми переносчиками и растениями-хозяевами. Журнал общей биологии 78: 32-61.
  18. Ryss A.Y., Subbotin S.A. 2017. Coevolution of the wood-inhabiting nematodes of the genus Bursaphelenchus Fuchs, 1937 with insect vectors and plant hosts. Zhurnal obshchei biologii 78: 32-61. (In Russian).
  19. Рысс A.Ю. 2016. Происхождение фитопаразитизма нематод и их коэволюция с хозяевами и переносчиками (на примере афеленхоидных нематод). Глава III. В кн.: Галактионов К.В. (ред.). Коэволюция паразитов и хозяев. Коллективная монография. Труды Зоологического института РАН, Т. 320. Приложение 4. Спб., Издательство ЗИН РАН, 127-159.
  20. Ryss A.Y. 2016. Origin of plant parasitism of nematodes and their co-evolution with hosts and vectors (with analysis of the aphelenchoidids). Chapter III. In: Galaktionov K.V. (ed.). Coevolution of parasites and their hosts. Monograph. Proceedings of the Zoological Institute RAS, Vol. 320, Supplement 4. Saint-Petersburg, Zoological Institute RAS, 127-159 (In Russian).
  21. Рысс A.Ю., Полянина К.С., Скрябина М.Д. 2018. Стволовые нематоды лиственных деревьев: цикл развития и специфичность к растениям-хозяевам. В кн: Мовсесян С.О. (ред.) Биоразнообразие паразитов. Доклады Международной научной конференции, посвященной 75-летию Центра паразитологии и 140-летию со дня рождения академика К.И. Скрябина, 23-25 октября 2018 г. г. Москва, Товарищество научных изданий КМК. Труды Центра Паразитологии 50: 216.
  22. Ryss A.Y., Polyanina K.S., Skrjabina M.D. 2018. Wood inhabiting nematodes of the deciduous trees: life cycles and host specificity to plants. In: Movsesyan S.O. (ed.). Bidiversity of parasites. Proceedings of international scientific conference, devoted to 140 anniversary of K.I. Skrjabin, October 23-25, 2018. Moscow, KMK Scientific Press Ltd. Trudy Centra Parazitologii 50: 2016. (In Russian).
  23. Чижов В.Н., Буторина Н.Н., Таболин С.Б., Лиманцева Л.А., Субботин С.А. 2019. Энтомопаразитические нематоды отрядов Tylenchida и Aphelenchida. Москва, Товарищество научных изданий КМК, 691 c.
  24. Chizhov V.N., Butorina N.N., Tabolin S.B., Limantseva L.A., Subbotin S.A. 2019. Entomoparasitic nematodes of the orders Tylenchida and Aphelenchida. Moscow, KMK Publishers, 691 pp. (In Russian).
  25. Bedding R.A. 1993. Biological control of Sirex nostilio using the nematode Deladenus siricidicola In: Bedding R., Akhurst R,. Kaya H. (eds). Nematodes and the biological control agents East Melbourne, CSIRO publication, 11-20.
  26. Bedding R.A., Akhurst R.J. 1974. Use of the nematode Deladenus siricidicola in the biological control of Sirex noctilio in Australia. Journal of Australian entomological society 13: 129-135.
  27. Bhuiyan N.H., Selvaraj G., Wei Y., King J. 2009. Role of lignification in plant defense. Plant Signaling & Behavior 4: 158-159. https://doi.org/10.4161/psb.4.2.7688
  28. Bongers T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14-19.
  29. Calin M., Vieira P., Costache C., Braasch H., Gu J., Wang J., Mota M. 2013. Survey of the genus Bursaphelenchus Fuchs, 1937 (Nematoda: Aphelenchoididae) in Romania. EPPO Bulletin 43: 144-151.
  30. Cheng H.R., Lin M.S. Qian R.J. 1986. A study on morphological diagnosis and pathogenicity of the pine wood nematode. Journal of Nanjing Agricultural University 2: 55-59.
  31. Donald P., Stamps W., Linit M. 2003. Plant disease lessons. Pine wilt. The Plant Health Instructor. The American Phytopathological Society (APS), 1-4. https://doi.org/10.1094/PHI-I-2003-0130-01
  32. Ferris H. 2010. Contribution of nematodes to the structure and function of the soil food web. Journal of Nematology 42: 63-67.
  33. Ferris H., Bongers T., De Goede R.G.M. 2001. A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept. Applied Soil Ecology 18: 13-29. https://doi.org/10.1016/S0929-1393(01)00152-4
  34. Fuchs A.G. 1930. Neue an Borken- und Russelkäfer gebundene Nematoden, halbparasitische und Wohnungseinmeiter. Freilebende Nematoden aus Moos und Walderde in Borken und Rüsselkäfergängen. Zoologische Jahrbücher, Abteilung für Systematik Oekologie und Geographie der Tiere für Systematik Oekologie und Geographie der Tiere, Jena 59: 505-646.
  35. Fuchs A.G. 1937. Neue parasitische und halbparasitische Nematoden bei Borkenkäfern und einige andere Nematoden. I. Teil die Parasiten der Waldgartner Myelophilus piniperda L. und minor Hartig und die Genera Rhabditis Dujardin, 1845 und Aphelenchus Bastian, 1865. Zoologische Jahrbücher, Abteilung für Systematik Oekologie und Geographie der Tiere, Jena 70: 291-380.
  36. Futai K. 2008. Pine wilt in Japan, from first incidence to the present. In: Zhao B. G., Futai K., Sutherland J. R., Takeuchi Y. (eds). Pine Wilt Disease. Tokyo, Berlin, Heidelberg, New York, Springer, 5-12. https://doi.org/10.1007/978-4-431-75655-2_2
  37. Hasegawa K., Miwa J. 2008. Embryology and Cytology of Bursaphelenchus xylophilus. In: Pine Wilt Disease. Zhao B. G., Futai K., Sutherland J. R., Takeuchi Y. (eds). Tokyo, Berlin, Heidelberg, New York, Springer, 81-104.
  38. Jones J.T., Haegeman A., Danchin E.G., Gaur H.S., Helder J., Jones M.G., Kikuchi T., Manzanilla-López R., Palomares-Rius J.E., Wesemael W.M. 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular plant pathology 14: 946-961. https://doi.org/10.1111/mpp.12057
  39. Kirino H., Maehara N., Shinya R. 2023. How did Bursaphelenchus nematodes acquire a specific relationship with their beetle vectors, Monochamus? Frontiers in Physiology 14. https://doi.org/10.3389/fphys.2023.1209695
  40. Kiyohara T., Tokushige, Y. 1971. Inoculation experiments of a nematode, Bursaphelenchus sp. onto pine trees. Journal of the Japanese Forestry Society 53: 210-218. (In Japanese, English abstract.). https://doi.org/10.11519/jjfs1953.53.7_210
  41. Kuroda K. 2008. Physiological Incidences Related to Symptom Development and Wilting Mechanism. In: Zhao B.G., Futai K., Sutherland J.R., Takeuchi Y. (eds). Pine Wilt Disease. Tokyo, Berlin, Heidelberg, New York, Springer, 204-222. https://doi.org/10.1007/978-4-431-75655-2_21
  42. Li M., Li H., Ding X., Wang L., Wang X., Fengmao C. 2022. The detection of Pine Wilt Disease: a literature review. International Journal of Molecular Sciences 23(18): 10797. https://doi.org/10.3390/ijms231810797
  43. Maehara N., Futai K. 1996. Factors affecting both the numbers of the pinewood nematode, Bursaphelenchus xylophilus (Nematoda:Aphelenchoididae), carried by the Japanese pine sawyer, Monochamus alternatus (Coleoptera, Cerambycidae), and the nematode life history. Applied Entomology and Zoology 31: 443-452.
  44. Mallez S., Castagnone C., Espada M., Vieira P., Eisenback J., Harrell M., Mota M., Aikawa T., Akiba M., Kosaka H. 2014. Worldwide invasion routes of the pinewood nematode: What can we infer from population genetics analyses? Biological Invasions 17: 1199-1213. https://doi.org/10.1007/s10530-014-0788-9
  45. Mamiya Y. 1975. The life history of the pinewood nematode, Bursaphelenchus lignicolus. Japanese Journal of Nematology 5: 16-25.
  46. Mamiya Y. 2008. Histopathological Observations of Bursaphelenchus xylophilus in Symptomatic Tissues of Pinewood. In: Mota M.M., Vieira P. (eds). Pine Wilt Disease: A Worldwide Threat to Forest Ecosystems. New York, Springer, 321-334. https://doi.org/10.1007/978-1-4020-8455-3_27
  47. Mamiya Y., Enda N. 1972. Transmission of Bursaphelenchus lignicolus (Nematoda: Aphelenchoididae) by Monochamus alternatus (Coleoptera: Cerambycidae). Nematologica 18: 159-162. https://doi.org/10.1163/187529272X00395
  48. Massey C.L. 1964. The nematode parasites and associates of the fir engraver beetle, Scotytus ventralis Le Conte, in New Mexico. Journal of Insect Pathology 6: 133-155.
  49. Massey C.L. 1971. Nematode associates of several species of Pissodes (Coleoptera: Curculionidae) in the United States. Annals of the Entomological Society of America 64: 162-169.
  50. Massey C.L. 1974. Biology and taxonomy of nematode parasites and associates of bark beetles in the Unites States. Forest Service, U. S. Department of Agriculture, 233 pp.
  51. Miraeiz E., Heydari R., Aliramaji F., Pourjam E., Pedram M., Atighi M.R. 2016. New morphometric ranges for Bursaphelenchus willibaldi Schönfeld et al. 2006 (Nematoda: Parasitaphelenchidae) from Iran. Forest Pathology 46: 29-34. https://doi.org/10.1111/efp.12210
  52. Mota M., Braasch H., Bravo M.A., Penas A.C., Burgermeister W., Metge K., Sousa E. 1999. First report of Bursaphelenchus xylophilus in Portugal and in Europe. Nematology 1: 727-734. https://doi.org/10.1163/156854199508757
  53. Mota M.M., Vieira P., (eds) 2008. Pine Wilt Disease: A worldwide threat to forest ecosystems. New York, Springer, 405 pp.
  54. Neher D.A., Darby B.J. 2009. General community indices that can be used for analysis of nematode assemblages. In: Wilson M.J., Kakouli-Duarte T. (eds). Nematodes as environmental indicators. Wallingford, CAB International, 107-123. https://doi.org/10.1079/9781845933852.0107
  55. Nickle W.R. 1970. A taxonomic review of the genera of the Aphelenchoidea (Fuchs, 1937) Thorne, 1949 (Nematoda: Tylenchida). Journal of Nematology 2: 375-392.
  56. Odum E.P. 1983. Basic Ecology: Fundamentals of Ecology, Saunders College Pub.: Philadelphia. 325 p.
  57. Pickup J., Rothery P. 1991.Water-loss and anhydrobiotic survival in nematodes of Antarctic fellfields. Oikos 61: 379. https://doi.org/10.2307/3545245
  58. Polyanina K.S., Popovichev B.G., Ryss A.Y. 2016. Elm wood nematodes as a threat to the urban woody plantations in the Russian North-West: the laboratory tests of woody plant host range and pathogenicity. In: Musolin D.L., Selikhovkin A.V. (eds). The Kataev Memorial Readings - IX. Dendrobiotic Invertebrates and Fungi and their Role in Forest Ecosystems / Proceedings of the International Conference. Saint Petersburg (Russia), November, 23-25, 2016. Saint Petersburg, Russia, Saint Petersburg State Forest Technical University, 90-93.
  59. Polyanina K.S., Ryss A.Y. 2019. Life cycles of xylobiont nematodes with special reference to three species parasitising deciduous trees. Abstracts of the Thirteenth International Symposium of the Russian Society of Nematologists (Russia, Republic of Karelia, 29 July-4 August, 2019). Russian Journal of Nematology 27: 153.
  60. Polyanina K.S., Ryss A.Y. 2021. Parameters of ontogeny and population dynamics modeling of Panagrolaimus detritophagus (Nematoda: Rhabditida) in vitro. Proceedings of the Zoological Institute RAS 325: 91-98. https://doi.org/10.31610/trudyzin/2021.325.1.91
  61. Rühm W. 1956. Die Nematoden der Ipiden. Parasitologische Schriftenreihe 6: 1-435.
  62. Ryss A., Vieira P., Mota M., Kulinich O. 2005. A synopsis of the genus Bursaphelenchus Fuchs, 1937 (Aphelenchida: Parasitaphelenchidae) with keys to species Nematology 7: 393-458.
  63. Ryss A., Polyanina K. 2022a. Life cycle and population dynamics of Bursaphelenchus willibaldi (Nematoda: Rhabditida: Aphelenchoididae) in vitro. Nematology 24: 1105-1119. https://doi.org/10.1163/15685411-bja10194
  64. Ryss A.Y., Polyanina K.S. 2022b. Life cycle and population dynamics of the Rhabditolaimus ulmi (Nematoda: Rhabditida: Diplogastridae) in vitro. Russian Journal of Nematology 30: 21-30. https://doi.org/10.24412/0869-6918-2022-1-21-30
  65. Ryss A.Y., Polyanina K.S. 2022c. The development and population dynamics of Aphelenchoides sp. from Quercus robur (Nematoda: Rhabditida: Aphelenchoididae) in vitro. Russian Journal of Nematology 31: 1-15. https://doi.org/10.24412/0869-6918-2023-1-1-15
  66. Ryss A., Polyanina K.S., Popovichev B.G., Subbotin S.A. 2015. Description of Bursaphelenchus ulmophilus sp. n. (Nematoda: Parasitaphelenchinae) associated with Dutch elm disease of Ulmus glabra Huds. in the Russian North West. Nematology 17: 685-703. https://doi.org/10.1163/15685411-00002902
  67. Ryss A.Y., Polyanina K.S., Petrov A.V., Sazonov A.A., Mandelshtam M.Yu., Subbotin S.A. 2019. Report of Bursaphelenchus crenati Rühm, 1956 (Nematoda: Parasitaphelenchinae) from Belarus and Russia with a diagnostic key and phylogeny of the Sexdentati group. Forest Pathology 49: e12534. https://doi.org/10.1111/efp.12534
  68. Ryss A.Y., Polyanina K.S., Popovichev B.G., Krivets S.A., Kerchev I.A. 2018. Plant host range specificity of Bursaphelenchus mucronatus Mamiya et Enda, 1979 tested in the laboratory experiments. Паразитология 52: 32-40.
  69. Ryss A.Y., Polyanina K.S., Álvarez-Ortega S., Subbotin S.A. 2021. Morphology, development stages and phylogeny of the Rhabditolaimus ulmi (Nematoda: Diplogastridae), a phoront of the bark beetle Scolytus multistriatus from the elm Ulmus glabra Huds. in Northwest Russia. Journal of Nematology 53: e2021-2025. https://doi.org/10.21307/jofnem-2021-025
  70. Ryss A.Y., Subbotin S.A. 2023. New Records of Wood- and Bark-Inhabiting Nematodes from Woody Plants with a Description of Bursaphelenchus zvyagintsevi sp. n. (Aphelenchoididae: Parasitaphelenchinae) from Russia. Plants 12. https://doi.org/10.3390/plants12020382
  71. Salehian S., Braeckman B., Beladjal L., Bert W., Clegg J., Mertens J. 2011. The importance of feeding status and desiccation rate in successful anhydrobiosis of Panagrolaimus detritophagus. Nematology 13: 185-191. https://doi.org/10.1163/138855410X512656
  72. Sandhove J., Spann N., Ristau K. 2016.The anhydrobiotic potential of the terrestrial nematodes Plectus parietinus and Plectus velox. Journal of experimental zoology, Part A: Ecological genetics and physiology: 325. https://doi.org/10.1002/jez.2028
  73. Schönfeld U., Braasch H., Burgermeister W. 2006. Bursaphelenchus spp. (Nematoda: Parasitaphelenchidae) in wood chips from sawmills in Brandenburg and description of Bursaphelenchus willibaldi sp. n. Russian Journal of Nematology 14: 119-126.
  74. Schiffer P., Danchin E., Burnell A.M., Schiffer A.-M., Creevey C., Wong S., Dix I., O'Mahony G., Culleton B., Rancurel C., Stier G., Martínez-Salazar E., Marconi A., Trivedi U., Kroiher M., Thorne M., Schierenberg E., Wiehe T., Blaxter M. 2017. Signatures of the evolution of parthenogenesis and cryptobiosis in panagrolaimid nematodes. iScience 21: 587-602. https://doi.org/10.1016/j.isci.2019.10.039
  75. Shatilovich A., Gade V.R., Pippel M., Hoffmeyer T., Tchesunov A., Stevens L., Winkler S., Hughes G., Traikov S., Hiller M. 2023. A novel nematode species from the Siberian permafrost shares adaptive mechanisms for cryptobiotic survival with C. elegans dauer larva. PLoS genetics 19: e1010798. https://doi.org/10.1371/journal.pgen.1010798
  76. Shin Sang-Chul 2008. Pine wilt disease in Korea. In: Zhao B.G., Futai K., Sutherland J.R., Takeuchi Y. (eds). Pine Wilt Disease. Tokyo, Berlin, Heidelberg, New York, Springer, 26-32. https://doi.org/10.1007/978-4-431-75655-2_5
  77. Steiner G., Buhrer E.M. (1934). Aphelenchoides xylophilus n. sp., a nematode associated with blue-stain and other fungi in timber. Journal of Agricultural Research 48: 949-951.
  78. Tanaka S.E., Aikawa T., Takeuchi-Kaneko Y., Fukuda K., Kanzaki N. 2017. Artificial induction of third-stage dispersal juveniles of Bursaphelenchus xylophilus using newly established inbred lines. Plos One 12: e0187127. https://doi.org/10.1371/journal.pone.0187127
  79. Togashi K., Kasuga H., Kasuga S., Matsunaga K., Jikumaru S. 2023. Pathogenicity and boarding ability of hybrid-derived populations between Bursaphelenchus xylophilus and B. mucronatus (Nematoda: Aphelenchoididae). Nematology: 1-13 (published online ahead of print 2023). https://doi.org/10.1163/15685411-bja10286
  80. Tokushige Y., Kiyohara T. 1969. Bursaphelenchus sp. in the wood of dead pine trees. Journal of the Japanese Forestry Society 51 (7): 193-195. (In Japanese). https://doi.org/10.11519/jjfs1953.51.7_193
  81. Tomalak M., Filipiak A. 2019. Bursaphelenchus michalskii sp. n. (Nematoda: Aphelenchoididae), a nematode associate of the large elm bark beetle, Scolytus scolytus Fabr. (Coleoptera: Curculionidae), in Dutch elm disease-affected elm, Ulmus laevis Pall. Nematology 21: 301-318. https://doi.org/10.1163/15685411-00003215
  82. van Megen H.H.B., van den Elsen S.J.J., Holterman M.H.M., Karssen G., Mooyman P.J.W., Bongers A.M.T., Holovachov O.V., Bakker J., Helder J. 2009. A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11: 927-950. https://doi.org/10.1163/156854109x456862
  83. Yeates G.W., Bongers T., Goede De R.G.M., Freckman D.W., Georgieva S.S. 1993. Feeding habits in soil nematode families and genera - an outline for soil ecologists. Journal of nematology 25: 315-331. PMID: 19279775; PMCID: PMC2619405
  84. Zhao B.G. 2008. Pine wilt disease in China. In: Zhao B.G., Futai K., Sutherland J.R., Takeuchi Y. (eds). Pine Wilt Disease. Tokyo, Berlin, Heidelberg, New York, Springer, 18-25. https://doi.org/10.1007/978-4-431-75655-2_4
  85. Zhao B.G., Futai K., Sutherland J.R., Takeuchi Y. (eds) 2008. Pine Wilt Disease. Tokyo, Berlin, Heidelberg, New York, Springer, 459 pp.

版权所有 © Russian Academy of Sciences, 2023
##common.cookie##