Parasitoid complex of overwintering cocoons of Neodiprion huizeensis (Hymenoptera: Diprionidae) in Guizhou, China
Complejo de parasitoides de capullos invernales de Neodiprion huizeensis (Hymenoptera: Diprionidae) en Guizhou, China
Li TaoI, II; Sheng Mao-LingI, III; Sun Shu-PingI, IV; Luo You-QingV
IGeneral Station of Forest Pest Management, State Forestry Administration, No. 58 Huanghe North Street, Shenyang 110034, P. R. China ]]>
IIPh. D. litao200105@163.com
IIIshengmaoling@163.com, corresponding author
IVMs. Sc. sfzzssp@163.com
VPh. D. Beijing Key Laboratory for Forest Pest Control, Beijing Forestry University, Beijing 100083, P. R. China. youqingluo@126.com
ABSTRACT
The conifer sawfly, Neodiprion huizeensis (Hymenoptera: Diprionidae), is an injurious leaf feeder of Pinus spp. (Pinaceae) in China. Its parasitoid complex of overwintering cocoons was investigated in Weining, Guizhou during 2012. The average parasitism rate of overwintering cocoons of N. huizeensis by the parasitoid complex was 34.6%. The parasitoid complex included Drino auricapita (Diptera: Tachinidae), ichneumonids, and Trichomalus sp. (Hymenoptera: Pteromalidae). The average parasitism rate of N. huizeensis by D. auricapita was 13.1%. The puparial period of D. auricapita averaged 16.4 ± 0.1 d. The female to male ratio was 1.1: 1. The ichneumonid complex included Aptesis grandis, A. melana, A. nigricoxa, Delomerista indica, Lamachus rufiabdominalis, L. nigrus, Bathythrix sp., Caenocryptus sp., Exyston spp., Gelis sp., Goryphus sp., and Olesicampe sp. The parasitism rate of N. huizeensis by ichneumonids was 17.1%. The parasitism rate of N. huizeensis by Trichomalus sp. was 4.5%, and the female to male ratio was 3.7: 1. The dominant species of parasitoids was D. auricapita followed by A. melana. The emergence of overwintered adults of N. huizeensis had two peaks: the first from the 17th to the 23rd of February, 2012; the second from February 29th to March 15th, 2012. The emergence of the parasitoid complexes coincided with each other and occurred from February 23rd to March 6th, 2012.
Key words: Neodiprion huizeensis. Parasitoid complex. Dominant species. Superparasitism. Sex ratio.
RESUMEN
]]> En China, la avispa de sierra de las coníferas Neodiprion huizeensis (Hymenoptera: Diprionidae) es un insecto perjudicial de las hojas de Pinus spp. (Pinaceae). Se estudió el complejo parasitoide de los capullos de hibernación (CPCH) en Weining, Guizhou, 2012. La tasa de parasitismo promedio del CPCH de N. huizeensis fue 34,6%. El complejo de parasitoide incluye Drino auricapita (Diptera: Tachinidae), ichneumónidos y Trichomalus sp. (Hypemoptera: Pteromalidae). La tasa de parasitismo promedio de D. auricapita en N. huizeensis fue 13,1%. El período promedio del pupario de D. auricapita fue 16,4 ± 0,1 d. La proporción hembra y macho fue 1,1: 1. El complejo ichneumónidos incluye Aptesis grandis, A. melana, A. nigricoxa, Delomerista indica, Lamachus rufiabdominalis, L. nigrus, Bathythrix sp., Caenocryptus sp., Exyston spp., Gelis sp., Goryphus sp. y Olesicampe sp. La tasa de parasitismo de icheumónidos en N. huizeensis fue 17,1% mientras que la de Trichomalus sp. en N. huizeensis fue 4,5%. La proporción hembra : macho fue 3,7: 1. Las especies dominantes de parasitoides fueron D. auricapita y A. melana. La emergencia de adultos hibernados de N. huizeensis tuvo dos picos, el primero del 17 al 23 de febrero de 2012 y el segundo del 29 de febrero al 15 de marzo de 2012. La aparición de los complejos de parasitoides coincidió mutuamente y se produjo del 23 de febrero al 6 de marzo.Palabras clave: Neodiprion huizeensis. Complejo de parasitoides. Especie dominante. Superparasitismo. Proporción de sexos.
Introduction
The conifer sawfly, Neodiprion huizeensis Xiao & Zhou, 1998, belongs to the genus Neodiprion of Diprionidae (Hymenoptera: Symphyta). This genus includes 51 described species (Taeger et al. 2010), of which 6 are known from China (Wei et al. 2006). Neodiprion huizeensis is a well-known pest defoliating Pinus armandii Franch. (Xiao et al. 1984, 1992) and Pinus yunnanensis Franch. (Pinaceae) (Xu et al. 1990) in Yunnan and Guizhou, South China.
Neodiprion huizeensis has two generations a year in China. Mature larvae spin cocoons in the litter under the crowns of trees and overwinter as diapausing prepupae. The research on N. huizeensis has been focused on biology, ecology and integrated management, especially chemical control (Xu et al. 1990; Xu 1998). Parasitoids of this sawfly have not as well been studied in China. One paper found that the parasitism rate of sawfly cocoons was about 10.0% (Xu et al. 1990). Four parasitoids, Aptesis melana Li & Sheng, 2013, Aptesis nigricoxa Li & Sheng, 2013, Lamachus nigrus Li, Sheng & Sun, 2012, and Lamachus rufiabdominalis Li, Sheng & Sun, 2012, (Hymenoptera: Ichneumonidae), have been reported on N. huizeensis (Li et al. 2012a, 2013).
Systematic research on the parasitoid complex will be important for biological control of N. huizeensis. The purpose of this survey was to determine the principal species of parasitoids from overwintering cocoons of N. huizeensis.
Materials and methods
]]> Field investigation and rearing conditions. Overwintering cocoons of N. huizeensis were collected in Weining County (26°54'N, 104°13'E, elevation 2,000 to 2,400 m), Guizhou Province. The three samples (N = 2225, 2040 and 1908 cocoons, respectively) were taken on 6th to 8th January 2012. The cocoons were kept at 2 °C one week under laboratory conditions, and then they were stored individually in glass tubes (100 mm long and 15 mm in diameter) with a piece of filter paper dipped in distilled water in order to prevent desiccation, plugged with absorbent cotton, and maintained at 23 ± 1 °C with 60% to 70% relative humidity and 14 hours to 10 hours light and dark photoperiod.All cocoons were checked daily for sawfly and parasitoid emergence until late July. Emerged parasitoid larvae and pupae were kept in glass tubes at the same temperature until adult emergence. After emergence of sawflies and parasitoids was complete (that is to say, there were no sawflies or parasitoids emergence), all remaining cocoons were dissected and their condition (i.e., the status of the diprionid adults and larvae, and parasitism) was recorded. Adults of N. huizeensis and its parasitoids were collected with intercept trap (Li et al. 2012b) in the field.
Identification. Tachinid parasitoids were identified by Dr. Chun-Tian Zhang (Shenyang Normal University, P. R. China), chalcid parasitoids by Dr. Stefan Schmidt (Zoologische Staatssammlung München, Germany), Delomerista indica Gupta, 1982, by Dr. Gavin R. Broad (Department of Entomology, the Natural History Museum, United Kingdom), Gelis sp. by Dr. Martin Schwarz (Eben 21, A-4202 Kirchschlag, Austria) and N. huizeensis by Dr. Mei-Cai Wei (Central South University of Forestry and Technology, P. R. China). All specimens have been deposited in the Insect Museum, General Station of Forest Pest Management, State Forestry Administration, P. R. China.
Statistical analysis. Parasitism rates data (p) were transformed by arcsin (p)1/2 in order to better fit the assumptions of normality and homogeneity of variances for ANOVA. The means were analyzed by one-way ANOVA, followed by the Ryan-Einot-Gabriel-Welsh (REGW) multiple Q test (SPSS 17.0 for Windows) at α = 0.05 (Li et al. 2012c).
Results
The parasitoid complex of N. huizeensis included Drino auricapita Chao & Liang, 1998, (Diptera: Tachinidae), Aptesis grandis Sheng, 1998, A. melana Li & Sheng, 2013, A. nigricoxa Li & Sheng, 2013, Delomerista indica Gupta, 1982, Lamachus rufiabdominalis Li, Sheng & Sun, 2012, L. nigrus Li, Sheng & Sun, 2012, Bathythrix sp., Caenocryptus sp., Exyston spp., Gelis sp., Goryphus sp., Olesicampe sp. (Hymenoptera: Ichneumonidae), and Trichomalus sp. (Hymenoptera: Pteromalidae).
From the overwintering cocoons of N. huizeensis 1063, 964, and 1006 adult sawflies emerged and 372, 347 and 280 dead adults and larvae were discovered from dissecting cocoons (Table 1).
From the cocoons, 340, 311 and 320 adult ichneumonids emerged, and 36, 17 and 27 larvae were discovered from dissecting host cocoons. The parasitism rates of ichneumonids ranged from 16.1% to 18.2%, with an average of 17.1% (Table 1).
Drino auricapita larvae developed inside the body of N. huizeensis larvae (Fig. 1A). Most tachinid larvae made an emergence hole on the sawfly cocoons after they emerged. Five overwintering sawfly cocoons were superparasitized by D. auricapita. One cocoon included 3 larvae of D. auricapita, other four cocoons included 2 larvae of D. auricapita, respectively (Fig. 1B). 278, 288 and 189 tachinid larvae emerged from the cocoons of N. huizeensis, and 19, 26 and 11 larvae were discovered from dissected host cocoons. The parasitism rates of D. auricapita ranged from 10.5% to 15.4%, with an average of 13.1% (Table 1).
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The puparial case of D. auricapita is completed within 24 hours after the mature larva emergence from host remains. The newly pupae are cream-colored, and turn yellowish brown in several hours, and then turn bright red to dark red. The duration of pupa was studied and the results showed that the mean ranges of duration of pupa are 16.7 ± 0.1, 16.4 ± 0.1 and 16.2 ± 0.1 days, respectively. There were no significant differences of the duration of pupa among the collections (F = 6.92, df = 2, 658, P > 0.05). There were 243, 263 and 155 adults of tachinid emerged. The ratio of adult females to males was 1.1: 1 (Table 3).
Trichomalus sp. is a gregarious, primary ectoparasitoid of N. huizeensis larvae (Fig. 1C). Depending on the size of the host, 2 to 46 individuals emerged from a single cocoon, with an average of 13 individuals from a single cocoon. One cocoon was multiparasitized by Trichomalus sp. and the endoparasitic larva of D. auricapita (Fig. 1D). There were 88, 70 and 61 cocoons of N. huizeensis parasitized by this chalcid. The parasitism rates of Trichomalus sp. ranged from 3.9% to 5.3%, with an average of 4.5% (Table 1). The female to male ratio was 3.7: 1. From 49 sawflies cocoons only female chalcids emerged.
The parasitism rates of N. huizeensis by parasitoid complexes ranged from 32.6% to 35.8%, with an average of 34.6%.
The ichneumonids of N. huizeensis included Aptesis grandis, which emerged 231 adults. The female to male ratio was 1.2: 1. There were 537 adults of A. melana emerged from sawfly cocoons, and the female to male ratio was 1.7: 1. 87 adults of Delomerista indica emerged from sawfly cocoons, and the female to male ratio was 2.5: 1. 78 adults of Lamachus rufiabdominalis emerged from the cocoons of sawflies, and the female to male ratio was 2.1: 1 (Table 2). The other ichneumonids species comprised L. nigrus (8♀♀5♂♂), Goryphus sp. (3♀♀2♂♂), A. nigricoxa (2♀♀), Olesicampe sp. (1♀), Bathythrix sp. (1♀), Caenocryptus sp. (1♀1♂), and Exyston spp. (3♀♀6♂♂). Five sawfly cocoons were parasitizing by a gregarious ichneumonid, Gelis sp. (new species, unpublished). One cocoon produced 6 adults (4♀♀2♂♂) of Gelis sp. One cocoon was multiparasitized by Gelis sp. (2♀♀) and larva of D. auricapita that was within the body of sawfly larva (Fig. 1E). One cocoon was multiparasitized by Gelis sp. (3♀♀1♂) and Trichomalus sp. (Fig. 1F), and other two cocoons produced 5♀♀1♂, 6♀♀2♂♂ adults of Gelis sp., respectively.
]]> The main parasitoids of N. huizeensis included D. auricapita, A. melana, A. grandis, D. indica, L. rufiabdominalis, and Trichomalus sp. The parasitism rates of N. huizeensis by these parasitoids were 13.1%, 8.7%, 3.8%, 1.4%, 1.3% and 4.5%, respectively. There were significant differences in the parasitism rates among these six species of parasitoids (F = 51.38, df = 5, 12, P < 0.001) (Fig. 2). There were significant differences of parasitism rates between D. auricapita and other five species (P < 0.001). There were significant differences of parasitism rates between A. melana and other 4 species (P < 0.001). There were no significant differences of parasitism rates between Trichomalus sp. and A. grandis (P > 0.05), but those parasitism rates of Trichomalus sp. being significantly higher than those of both D. indica and L. rufiabdominalis (P < 0.001), and no significant differences of parasitism rates among A. grandis, D. indica and L. rufiabdominalis (P > 0.05). The dominant parasitoid species of N. huizeensis were D. auricapita followed by A. melana.
The adult emergence of N. huizeensis had two peaks and does not consider the male and female. The first peak occurred from 17th to 23rd February with 179 sawflies emerging on 20th February. The second peak was from 29th February to 15th March with 174 sawflies emerging on 3rd March. The number of sawflies emerging dropped gradually from 15th March and ended on 5th April 2012 (Fig. 3).
]]> The mature larvae emergence periods of D. auricapita out from the sawfly cocoons were from 8th February to 24th March. There had one peak occurred from 8th to 20th February, with 140 final instar larvae emerging on 11th February. The numbers of larvae emerging dropped gradually from 14th February. The adult emergence periods of D. auricapita were from 20th February to 2nd April, had one peak occurred from 23rd February to 6th March, with 75 flies on 29th February. The adult emergence periods of D. auricapita had 43 days (Fig. 3).
The adult emergence periods of A. grandis were from 20th February to 9th March, with 24 adults on 29th February. The adult emergence periods of A. melana were from 17th February to 12th March, with 63 adults on 20th February. The adult emergence periods of D. indica were from 17th February to 3rd March, with 10 adults on 23rd February. The adult emergence periods of L. rufiabdominalis were from 3rd to 30th March, with 5 adults on 18th March (Fig. 3).
The emergence periods of ectoparasitoid Trichomalus sp. were from 17th February to 12th March, had one peak occurred from 23rd February to 3rd March, with 26 sawflies cocoons were parasitized by this chalcid on 26th February (Fig. 3).
The adults emergence of parasitoids were coincide with each other and occurring from 23rd February to 6th March, which was between the emergence peak of N. huizeensis.
Discussion
The average parasitism rate of N. huizeensis by parasitoids was 34.6%. These parasitoids play an important role to control N. huizeensis populations in nature. The emergence of overwintering adults of N. huizeensis were from middle March to late April (Xu et al. 1990, Ying and Luo 2002). Under the experimental conditions, these periods of N. huizeensis were from late February to early April.
The genus Drino comprises 38 described species in China (O'Hara et al. 2009). Most species of this genus parasitize on either sawfly or lepidopteran larvae (Shima 1999). Drino auricapita parasitizing on Neodiprion sertifer (Geoffroy, 1785), Diprion jingyuanensis Xiao & Zhang, 1994, in Sichuan and Shanxi Province (Chao et al. 1998). Drino auricapita was the dominant species, attacking 13.1% of the N. huizeensis cocoons. Tachinids are playing an important role in control sawflies.
Superparasitism in the parasitic Diptera appears to be both widely distributed among species and common within populations (Feener and Brown 1997). This phenomenon was observed frequently with D. gilva for the common pine sawfly (Herz and Heitland 1999). Superparasitism of the gypsy moth, Lymantria dispar (Linnaeus, 1758) by Parasetigena silvestris (Robineau-Desvoidy, 1863) to be up to 83% and that to be as high as 77% by Blepharipa schineri (Mesnil, 1939) (Maier 1990). The superparasitism can be advantageous when the number of unparasitized hosts is low in the field (van Alphen and Visser 1990). Drino auricapita is a solitary endoparasitoid of N. huizeensis larvae and has been observed to superparasitize N. huizeensis infrequently. The biology, ecology of D. auricapita and relationship with its host need more investigation.
Ichneumonid complexes of N. huizeensis were including more than 12 species, of which 6 are identified as species. The unidentified species need more investigation. Delomerista indica is distributed in India, and no host record known (Gupta 1982). Lamachus gilpiniae Uchida, 1955, parasitizing on Diprion jingyuanensis and Gilpinia tohi Takeuchi, 1940, distributed in China and Japan (Uchida 1955; Li et al. 2012d). In our investigation, L. rufiabdominalis and L. nigrus reared from N. huizeensis in South China (Li et al. 2012a).
]]> The parasitism rates of N. huizeensis by the genus Aptesis were about 12.5%, including 8.7% by A. melana which is a dominant species for N. huizeensis follows Drino auricapita. However, only two females of A. nigricoxa reared from the overwintering cocoons of N. huizeensis (Li et al. 2012a). Gelis sp. which parasitizing on N. huizeensis is a gregarious parasitoid, and a multiparasitoid with Drino auricapita or Trichomalus sp. One N. huizeensis cocoon was parasitized by an endoparasitoid D. auricapita and emerged two females of gregarious Gelis sp. Another sawfly cocoon mulitparasitized by Gelis sp. and Trichomalus sp., they all emerged from the cocoon. Gelis sp. parasitic characteristics and relationships with its host need more investigation.
Acknowledgements
We are gratefully indebted to Dr. Gavin R. Broad (Department of Life Sciences, the Natural History Museum, United Kingdom) and anonymous reviewers for reviewing the manuscript and providing helpful comments. We would also like to thank Dr. Stefan Schmidt (Zoologische Staatssammlung München, Germany), Dr. Gavin R. Broad, Dr. Martin Schwarz (Eben 21, A-4202 Kirchschlag, Austria), Dr. Chun-Tian Zhang (Shenyang Normal University, P. R. China) for identifying the parasitoids and Dr. Mei-Cai Wei (Central South University of Forestry and Technology, P. R. China) for identifying the sawfly. This research was supported by the National Natural Science Foundation of China (NSFC, No. 30872035, No. 31110103062).
Literature cited
CHAO, C. M.; LIANG, E. Y.; SHI, Y. S.; ZHOU, S. X.; SUN, X. K.; CHEN, R. J. 1998. Tachinidae. pp. 1833-1835. In: Xue, W. Q.; Chao, C. M. (Eds.). Flies of China. Volume II. Liaoning Science and Technology Press, Shenyang. China. 2425 p. [ Links ]
FEENER, D. F. Jr.; BROWN, B. V. 1997. Diptera as parasitoids. Annual Review of Entomology 42: 73-97. [ Links ]
]]>GUPTA, V. K. 1982. A revision of the genus Delomerista (Hymenoptera: Ichneumonidae). Contributions to the American Entomological Institute 19 (1): 1-42. [ Links ]
HERZ, A.; HEITLAND, W. 1999. Larval parasitism of a forest pest, the common pine sawfly Diprion pini (L.) (Hym., Diprionidae), during an endemic density phase. Journal of Applied Entomology 123 (3): 129-137. [ Links ]
LI, T.; SHENG, M. L.; SUN, S. P. 2012a. Species of the genus Lamachus Förster (Hymenoptera, Ichneumonidae) parasitizing diprionid sawflies (Hymenoptera, Diprionidae) with descriptions of two new species and a key to Chinese species. Zookeys 249: 37-49. [ Links ]
LI, T.; SHENG, M. L.; SUN, S. P.; CHEN, G. F.; GUO, Z. H. 2012b. Effect of the trap color on the capture of ichneumonids wasps (Hymenoptera). Revista Colombiana de Entomología 38 (2): 338-342. [ Links ]
LI, T.; SHENG, M. L.; SUN, S. P.; LUO, Y. Q. 2012c. Parasitoids of the sawfly, Arge pullata, in the Shennongjia National Nature Reserve. Journal of Insect Science 12: 97. Available online: http://www.insectscience.org/12.97. [ Links ]
]]>LI, T.; SHENG, M. L.; ZOU, Q. C. 2012d. A new Chinese record species of Ichneumonidae (Hymenoptera) parasitizing Diprion jingyuanensis. Acta Zootaxonomica Sinica 37 (2): 463-465. [ Links ]
LI, T.; SHENG, M. L.; SUN, S. P. 2013. Chinese species of the genus Aptesis Förster (Hymenoptera, Ichneumonidae) parasitizing sawflies, with descriptions of three new species and a key to species. Zookeys 290: 55-73. [ Links ]
MAIER, K. 1990. Contribution to the biology of primary and secondary parasitoids of Lymantria dispar L. (Lep., Lymantriidae). Journal of Applied Entomology 110: 167-182. [ Links ]
O'HARA, J. E.; SHIMA, H.; ZHANG, C. T. 2009. Annotated catalogue of the Tachinidae (Insecta: Diptera) of China. Zootaxa 2190: 1-236. [ Links ]
SHIMA, H. 1999. Host-parasite catalog of Japanese Tachinidae (Diptera). Makunagi/Acta Dipterologica Supplement 1: 1-108. [ Links ]
]]>TAEGER, S.; BLANK, S. M.; LISTON, A. D. 2010. World catalog of Symphyta (Hymenoptera). Zootaxa 2580: 1-1064. [ Links ]
UCHIDA, T. 1955. Neue oder wenig bekannte Schmarotzer der Nadelholz-Blattwespen nebst einem neuen sekundären Schmarotzer. Insecta Matsumurana 19 (1-2): 1-8. [ Links ]
VAN ALPHEN, J. J. M.; VISSER, M. 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35: 59-79. [ Links ]
WEI, M.; NIE, H. Y.; TAEGER, A. 2006. Sawflies (Hymenoptera: Symphyta) of China- Checklist and Review of Research, pp. 505-574. In: Blank, S. M.; Schmidt, S.; Taeger, A. (Eds.). Recent Sawfly esearch - Synthesis and Prospects. Goecke & Evers, Keltern. 704 p. [ Links ]
XIAO, G. R.; ZHOU, S. Z.; HUANG, X. Y. 1984. Seven new species of sawflies from Yunnan Province (Hymenoptera: Symphyta: Diprionidae). Entomotaxonomia 6 (2-3): 141-146. [ Links ]
]]>XIAO, G. R.; HUANG, X. Y.; ZHOU, S. Z.; WU, J.; ZHANG, P. Y. 1992. Economic sawfly Fauna of China (Hymenoptera: Symphyta) (I). Tianze Eldonejo. Yangling. China. 220 p. [ Links ]
XU, Z. H.; XU, Z. Q.; WU, Y. 1990. A biological observation on Neodiprion huizeensis. Journal of Southwest Forestry College 10 (2): 203-209. [ Links ]
XU, Z. H. 1998. A classification of larvae of Diprionidae in Yunnan Province - Genus Neodiprion Rohwer (Hymenoptera: Symphyta). Journal of Southwest Forestry College 18 (4): 254-259. [ Links ]
YING, H. T.; LUO, Z. F. 2002. Biological characteristics and control of Neodiprion huizeensis. Yunnan Forestry Science and Technology 1: 65-67. [ Links ]
]]> Received: 12-Nov-2014