Research Article |
Corresponding author: Zhong Qi Yang ( yangzhqi@126.com ) Academic editor: Jose Fernandez-Triana
© 2019 Liang Ming Cao, Yan Long Zhang, Cornelis van Achterberg, Zhi Yong Wang, Xiao Yi Wang, Wen Xia Zhao, Zhong Qi Yang.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Cao LM, Zhang YL, van Achterberg C, Wang ZY, Wang XY, Zhao WX, Yang ZQ (2019) Notes on braconid wasps (Hymenoptera, Braconidae) parasitising on Agrilus mali Matsumura (Coleoptera, Buprestidae) in China. ZooKeys 867: 97-121. https://doi.org/10.3897/zookeys.867.36170
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Braconid parasitoids reared from Malus sieversii and Malus domestica trees in NW China infested by Agrilus mali Matsumura (Coleoptera, Buprestidae) are illustrated and discussed. Six species were found parasitising Agrilus mali in NW China, namely, Atanycolus ivanowi (Kokujev) (Braconinae), Doryctes undulatus (Ratzeburg), Pareucorystes varinervis Tobias, Polystenus rugosus Foerster, Spathius sinicus Chao, and Spathius brevicaudis Ratzeburg (Doryctinae). All listed species are newly recorded parasitoids of Agrilus mali. Pareucorystes varinervis and Spathius brevicaudis are new records for the Chinese fauna, but Spathius brevicaudis has been recorded from Taiwan before. Both sexes of Spathius brevicaudis are redescribed here to allow inclusion in the recent revision of the Chinese Spathius species. An identification key to the six braconid parasitoids of Agrilus mali in NW China is provided.
Agrilus mali, Braconidae, China, new record, parasitoid wasps, Malus sieversii
The apple buprestid, Agrilus mali (Coleoptera: Buprestidae), is considered to be a dangerous pest in China of apple trees. Recently, a large area of wild Malus sieversii has been killed by Valsa mali Miyabe et Yamada and Cytospora mandshurica Miura, after infection by A. mali (Figure
Adult, egg and larval stages of Agrilus mali are shown in Figure
Using organic insecticides has allowed the control of A. mali in orchards, but in the wild this is ineffective as the trees are scattered over a vast area. The damage of A. mali is erratic, wide-spread, and frequent spraying of chemicals will be another threat to the vulnerable local ecosystem. Therefore, biological control is considered as the best countermeasure and a survey about the natural enemies of A. mali has been carried out in recent years.
This study is based on specimens retained in the Entomological Museum of Chinese Academy of Forestry (Beijing, China) and the Naturalis Biodiversity Center (Leiden, the Netherlands). Natural enemy surveys of A. mali were conducted in Xinjiang, Shaanxi and Qinghai Provinces from 2011 to 2018. Trunk bark of stressed trees was peeled off to search for A. mali larvae and associated parasitoids. The larvae and possible parasitoid cocoons were placed singly in vials (12 mm in diameter and 75 mm in length), each containing a piece of filter paper dipped in distilled water for moisture. The vials were plugged tightly with sterilised cotton and maintained at 22–25 ℃ in the rearing room. Parasitoid cocoons were successively reared to adults. Specimens were examined with a Nikon SZH 1500 stereomicroscope. Photographs were taken with an Olympus CX31 microscope with the UV–C Optical Totally Focuses System developed by Beijing United Vision Technology Co., Ltd. Terminology and measurements follow
Vipio (Atanycolus) ivanowi Kokujev, 1898: 364.
Bracon (Vipio) sculpturatus
Thomson, 1892: 1800;
Atanycolus signatus Szépligeti,1901, 33: 176. Syn. by Papp, 1960.
4♀, 20♂, China, Xinjiang Province, Gongliu City, Mohuer County, 25.VI.2006, 1325 m altitude, 43°15'27"N, 82°47'56"E, Yang ZhongQi leg. The collected cocoons were adhered to mature dead larvae of A. mali. 86♀, 78♂, same locality and biological data, but collected 25.VI.–24.VII.2015 by Wang ZhiYong.
Larva of Agrilus mali (new record) (Buprestidae). Arhopalus syriacus Reitter, Leptura rubra Linnaeus, Monochamus galloprovincialis Olivier Osphranteria inaurata Holzschuh, Tetropium fuscum Fabricius, T. gabrieli Weise (Cerambycidae); Anthaxia aurulenta Fabricius, Chrysobothris solieri Gory et Laporte, Lampra mirifica Mulsant, Melanophila decastigma Fabricius, M. picta Pallas, Sphenoptera tappesi Marseul (Buprestidae).
China (Xinjiang); Armenia; Austria; Azerbaijan; Croatia; Czech Republic; Finland; France; Germany; Greece; Hungary; Italy; Japan; Kazakhstan; Russia; Slovakia; Switzerland; Tajikistan; Turkey; Turkmenistan; Ukraine; Uzbekistan.
Atanycolus ivanowi is clearly characterised by the sculpture of the first to fourth metasomal tergites (Fig.
Genus Atanycolus are ectoparasitoids of wood borers, and are usually solitary (Figure
We found two generations per year of A. ivanowi in our experimental fields. The first generation lasts ca. 40 days from late March to May, and many adults can be seen during May to July. The larvae of the overwintering generation can be seen before August and later only cocoons can be found. Obviously, this parasitoid overwinters in the cocoon stage.
In total, we collected 86 females and 78 males of A. ivanowi in 2015 from one site (Xinjiang Province, Gongliu City, Mohuer County), which shows that the approximate ratio of female and male is 11/10. The natural parasitisation rate is approximately 26.7% and according to our investigations, A. ivanowi has the maximum population on A. mali. Obviously, A. ivanowi should be protected in order to increase the biodiversity of the forests, in which Malus sieversii is the main component.
Bracon undulatus Rarzeburg, 1852: 35.
Doryctes undulatus: Reinhard, 1865: 256; Marshall, 1888: 237; Shenefelt et Marsh, 1976: 1294; Belokobylskij, 1998: 63; Belokobylskij et Maeto, 2009: 128;
Doryctes brachyurus: Marshall, 1888: 238; Shenefelt et Marsh, 1976: 1279; Papp, 1984: 175.
2♀, China, Xinjiang Province, Gongliu City, Mohuer County, 8.VIII.2008, 1325 m altitude, 43°13'25"N, 82°45'16"E, Yang ZhongQi leg. 1♀, China, Xinjiang Province, Xinyuan County, Halabula, 16.VI.2011, 46°12'16"N, 82°59'20"E, Yang ZhongQi leg., 25.VI.2011, hatched out from a mature larvae of A. mali. 3♀, China, Xinjiang Province, Xinyuan County, Halabula, 16.VI.2011, 46°12'16"N, 82°59'20"E, Yang ZhongQi leg., 10.VII.2011, hatched out from a mature larvae of A. mali. 1♂, China, Xinjiang Province, Xinyuan County, Halabula, 16.VI.2011, 46°12'16"N, 82°59'20"E, Yang ZhongQi leg., 25.VII.2011, hatched out from a mature larvae of A. mali. 1♂, China, Xinjiang Province, Gongliu City, Mohuer County, 15.VI.2011, 1325 m altitude, 43°13'25"N, 82°45'16"E, Tang YanLong, Wang ZhiYong & Yang ZhongQi leg., 8.VII.2011, hatched out from a mature larvae of A. mali.
Larva of Agrilus mali (new record) (Buprestidae). Axinopalpis gracilis Krynicki, Grammoptera ruficornis Fabricius, Molorchus kiesenwetteri Mulsant et Rey, M. umbellatarum Schreber, Pogonocherus decoratus Germar, P. fasciculatus DeGeer, P. hispidulus Piller, P. hispidus (Linnaeus), Tetrops praeustus (Linnaeus) (Cerambycidae); Agrilus convexicollis Redtenbacher, A. cuprescens Menetries, A. mendax Mannerheim A. viridis (Linnaeus) Anthaxia tuerki Scopoli (Buprestidae); Magdalis armigera Geoffroy, M. ruficornis (Linnaeus), Pityogenes bidentatus (Herbst) (Curculionidae).
China (Xinjiang, Heilongjiang, Jilin, Gansu); Bulgaria; France; Germany; Hungary; Italy; Japan; Kazakhstan; Korea; Lithuania; Moldova; Mongolia; Poland; Russia; Slovakia; Sweden; Switzerland; United Kingdom.
According to the detailed redescription of Japanese specimens (Belokobylskij et Maeto, 2009) and the key to this genus for China (
Pareucorystes varinervis Tobias, 1961: 529.
Pareucorystes depressus Fischer, 1966: 323.
10♀, 1♂, China, Qinghai Province, Hualong County, 17.VI.2008, 36°05'42"N, 102°15'43"E, Yang ZhongQi leg.
Larva of Agrilus mali (new record) (Buprestidae). Agrilus angustulus Illiger, A. auricollis Kiesenwetter, A. convexicollis Redtenbacher, A. laticornis Illiger, A. sulcicollis Lacordaire, A. viridis (Linnaeus) (Buprestidae); Tetrops praeustus (Linnaeus) (Cerambycidae).
China (Qinghai); Azerbaijan; Bulgaria; Canary Islands; Czechoslovakia; France; Hungary; Italy; Kazakhstan; Russia; Slovakia; Ukraine.
This species is mainly specialised on Agrilus species; if the population density could be enlarged, it would be a potential biological control agent. The species is also a new to the Chinese fauna, and a new parasitoid of A. mali.
Polystenus rugosus
Foerster, 1863: 237; Shenefelt et Marsh, 1976: 1361; Papp, 1984: 182; Belokobylskij et Tobias, 1986: 34; Belokobylskij, 1998: 74; Belokobylskij et Maeto, 2009: 409;
Corystes aciculatus Reinhard, 1865: 259.
Eucorystes aciculatus Marshall, 1888: 204.
Eucorystoides aciculatus Ashmead, 1900: 368; Shenefelt et Marsh, 1976: 1354; Papp, 1984: 182.
1♀, China, Shaanxi Province, Yijun County, 29.VII.2006, 35°23'56"N, 109°06'41"E, Yang ZhongQi leg, 28.VII.2006, hatched out from a mature larva of A. mali. 1♂, China, Xinjiang Province, Gongliu City, Mohuer County, 26.VI.2006, 1325 m altitude, 43°13'25"N, 82°45'16"E, Yang ZhongQi leg, 13.VII.2006, hatched out from a mature larvae of A. mali.
Larva of Agrilus mali (new record) (Buprestidae). Agrilus angustulus Illiger, A. auricollis Kiesenwetter, A. sulcicollis Lacordaire, A. viridis (Linnaeus), Anthaxia manca Linnaeus, Coraebus bifasciatus Olivier (Buprestidae); Sinoxylon sexdentatum Olivier (Bostrichidae).
China (Xinjiang, Shaanxi, Henan, Zhejiang, Taiwan?), Austria; Czech Republic; Germany; Hungary; Italy; Japan; Kazakhstan; Korea; Liechtenstein; Poland; Russia; Slovakia; Switzerland; Tajikistan; Ukraine.
This species is newly reported for Xinjiang and Shaanxi and A. mali is a new host record.
Spathius sinicus
Chao, 1957: 3; 1977: 209; Chen & Shi, 2004: 162;
6♀, China, Xinjiang Province, Gongliu City, Mohuer County, 15.VI.2011, 1325 m altitude, 43°13'25"N, 82°45'16"E, Zhang YanLong, Wang ZhiYong & Yang ZhongQi leg, 8.VII.2011, hatched out from mature larvae of A. mali.
Larva of A. mali (new record) (Buprestidae).
China (Xinjiang, Fujian, Heilongjiang, Hunan, Shanghai, Jilin, Tianjin, Zhejiang); Japan.
This species is widely distributed in China and A. mali is the first reported of a host. It is peculiar that during several years of investigation, only 6 individuals have been found on A. mali at one tree, which indicates that it is an occasional parasitism.
Spathius brevicaudis Ratzeburg, 1844: 49; Nixon, 1943: 202; Belokobylskij, 1996: 188.
1♀, 1♂, China, Xinjiang Province, Gongliu City, Mohuer County, 26.VI.2006, 1325 m altitude, 43°13'25"N, 82°45'16"E, Zhang YanLong, Wang ZhiYong & Yang ZhongQi leg., 12.VII.2006, hatched out from mature larvae of A. mali.
Body length, ♀/♂ = 2.9/2.8 mm; forewing length, ♀/♂ = 2.34/2.25 mm.
Head dark brown, basal half of antenna yellow, its apical half brown; mesoscutal lobes, scutellum dark brown, pronotum brown; metasoma dark brown except first and second metasomal segments, basal portion of third metasomal segment yellow; fore wing partly weakly darkened; legs yellow (Fig.
Median length 0.7 times of its width in dorsal view; vertex broad, surface rough, with low (fine) sculptures and rare white setae (Fig.
Length of mesosoma 1.9 × its width and 1.6 × its height in lateral view (Fig.
Fore femur 0.8 times as long as fore tibia and 3.75 times as long as its width, fore tibia 8.0 times of its width, outside with a row of spines and apex with comb of spines, ratio of fore tarsal segments I–V = 1.4:0.7:0.5:0.3:0.6; mid femur 0.8 times of mid tibia, ratio of mid tarsal segments I–V = 7:5:4:5:7; hind femur 2.7 times of its width, 0.8 times as long as hind tibia, ratio of hind tarsal segments I–V =1.5:0.8:0.5:0.4:0.8 (Fig.
Fore wing with faintly brown along veins in basal half, apical half of fore wing largely subhyaline, its length 3.2 times of width; pterostigma 4.0 times as long as its maximum width; vein 1-R1 1.3 times of pterostigma, vein r originates at middle of pterostigma; vein SR1 8.5 times as long as vein r and straight; vein r nearly 1/4 of vein 2-SR, vein cu-a perpendicular to vein CU1, vein m-cu enters second submarginal cell; meeting point of veins 2-SR, 2-M and 2-SR+M finely sclerotised, veins reduced; vein 1-SR+M straight, vein 1-SR 1/3 length of vein 1-M; vein r-m weakly sclerotised, nearly invisible; veins 3-M and CU1a extending to wing margin (Fig.
First tergite length 1.55 × its maximum apical width in dorsal view, apical 2/3 with regular longitudinal striae, basal 1/3 rugulose; in lateral view first tergite very robust, spiracular tubercles located at basal 1/4, laterally with erect white long setae, apical 1/3 of laterotergites visible; second tergite largely rugulose and with several large round yellow spots; basal 2/3 of third tergite striate-rugulose, apical 1/3 smooth; fourth tergite basally 1/4 with longitudinal rugulosity; fifth and sixth tergites smooth. Length of setose part of the ovipositor sheath 0.7 × length of metasoma, 0.38 × length of fore wing, and 0.3 × length of body (Figs
Body length 2.8 mm, otherwise similar to female (Figs
China (Xinjiang, Taiwan); Austria; Azerbaijan; Bulgaria; Czech Republic; Denmark; France; Georgia; Germany; Hungary; Italy; Japan; Kazakhstan; Korea; Moldova; Mongolia; Poland; Romania; Russia; Slovakia; Sweden; Switzerland.
Larva of Agrilus mali (new record), Agrilus viridis (Linnaeus), Anthaxia manca Linnaeus, A. quadripunctata (Linnaeus), Bostrichus bidens Fabricius (Buprestidae); Acanthocinus griseus (Fabricius), Arhopalus coreanus Sharp, Exocentrus lusitanus (Linnaeus) (Cerambycidae); Blastophagus minor (Hartig), B. piniperda (Linnaeus), Carphoborus minimus (Fabricius), Ceutorhynchus quadridens (Panzer), Dryocoetes autographus (Ratzeburg), Hylesinus fraxini Panzer, Ips acuminatus (Gyllenhal), I. typographus (Linnaeus), Lixus bidens Fabricius, Magdalis frontalis Gyllenhal, M. violacea (Linnaeus), Niphades variegatus Roelofs, Onthotomicus angulatus Eichhoff, Phloeotribus rhododactylus (Marsham), Pissodes notatus Fabricius, P. obscurus Roelofs, Pityogenes bidentatus (Herbst), P. chalcographus (Linnaeus), Pityophthorus micrographus (Linnaeus), Polygraphus subopacus Thomson, Rynchaenus fagi (Linnaeus), R. pilosus Fabricius, R. quercus (Linnaeus) R. salicis (Linnaeus), R. testaceus Muller, Scolytus intricatus (Ratzeburg), S. koenigi Schewyrew, S. laevis Chapuis, S. mali (Bechstein), S. multistriatus (Marsham), S. rugulosus (Muller), Shirahoshizo insidiosus Roelefs, Sh. pini Morimoto, Sh. rufescens Roelofs (Curculionoidea); Xiphydria longicollis (Geoffroy) (Xiphydriidae).
Among all the parasitoids of A. mali we found in the past years, only two specimens of S. brevicaudis were recorded, which indicates that it is an occasional parasitoid of this host. This species is here recorded as new for continental China, after
1 | Occipital and prepectal carinae absent (Fig. |
Atanycolus ivanowi (Kokujev) |
– | Occipital and prepectal carinae present (Figs |
2 |
2 | Forewing with two submarginal cells, because vein r-m of fore wing is completely absent (except sometimes in Pareucorystes) (Figs |
3 |
– | Forewing with three submarginal cells, because vein r-m is weakly developed (Figs |
4 |
3 | Metasomal tergites 2+3 with V-shaped pale area and without posteriorly curved transverse groove (Fig. |
Polystenus rugosus Foerster |
– | Metasomal tergites 2+3 without V-shaped pale area and with posteriorly curved transverse groove (Fig. |
Pareucorystes varinervis Tobias |
4 | Vein m-cu of fore wing entering first submarginal cell (antefurcal: Fig. |
Doryctes undulatus (Ratzeburg) |
– | Vein m-cu of fore wing entering second submarginal cell (postfurcal: Figs |
5 |
5 | Forewing partly strongly infuscated (Fig. |
Spathius sinicus Chao |
– | Forewing weakly infuscated, subhyaline (Fig. |
Spathius brevicaudis Ratzeburg |
We sincerely thank Dr. Jose Fernandez-Triana (Canadian National Collection of Insects, Ottawa, Canada) and Dr. Sergey Belokobylskij (Zoological Institute, Russian Academy of Sciences, St Petersburg, Russia) for their critical reading of and helpful comments on the manuscript. This research is financially supported by the Special Fund for Forest Scientific Research in the Public Welfare (Grant No. 201404403) and the National Key R&D Program of China (2016YFC0501503-1-1).