Abstract
The genus Leptocybe Fisher & La Salle (Hymenoptera: Eulophidae) and its type species L. invasa were first described in 2004. Leptocybe spp. are global pests of eucalyptus plantations, and parasitoids play an important role in their control. In this review, we describe the species, distribution, biology, ecology and parasitism levels of Leptocybe spp. parasitoids and the problems associated with biological control programmes against Leptocybe spp. Additionally, prospects for the use of conservation or augmentative biological control programmes against Leptocybe spp. are discussed. Worldwide, approximately 23 species of parasitoids of Leptocybe spp. in 7 families and 10 genera have been found to date. Comparing the parasitism levels of the parasitoids showed that Quadrastichus mendeli, Selitrichodes neseri and several (approximately 4) native Megastigmus spp. could be exploited to manage Leptocybe spp. Available information on the Leptocybe spp. parasitoids is expected to improve our understanding related to ongoing studies of biological control programmes against Leptocybe spp.
Similar content being viewed by others
References
Ankita G, Poorani J (2008) New distribution and host records of Chalcidoidea (Insecta: Hymenoptera) from various parts of India. Check List 4:410–414
Anonymous (2013) One year of releasing Selitrichodes neseri: biocontrol agent for Leptocybe invasa (FABI Articles). http://www.forestry.co.za/one-year-ofreleasing-selitrichodes-neseri-biocontrol-agent-for-leptocybe-invasa/. Accessed 21 December 2017
Aytar F (2003) Natural biology, distribution and control method of Leptocybe invasa Fisher & La Salla (Hym., Eulophidae), eucalyptus gall wasp in Turkey. J DOA 9:47–66
Bush SJ, Dittrich-Schröder G, Neser S, Gevers C, Baffoe KO, Slippers B, Hurley BP (2017) First record of Quadrastichus mendeli, a parasitoid of Leptocybe invasa, in South Africa. South Forests 80:275–277
Cooper WR, Rieske LK (2007) Community associates of an exotic gall maker Dryocosmus kuriphilus (Hymenoptera: Cynipidae) in eastern North America. Ann Ent Soc 100:236–244
De Bach P, Rosen D (1991) Biological control by natural enemies. Cambridge University Press, Cambridge, p 440
De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698
Dittrich-Schröder G, Wingfield MJ, Hurley BP, Slippers B (2012) Diversity in Eucalyptus susceptibility to the gall-forming wasp Leptocybe invasa. Agric For Entomol 14:419–427
Dittrich-Schröder G, Harney M, Neser S, Joffe T, Bush S, Hurley BP, Wingfield MJ, Slippers B (2014) Biology and host preference of Selitrichodes neseri: a potential biological control agent of the eucalyptus gall wasp, Leptocybe invasa. Biol Control 78:33–41
Dittrich-Schröder G, Hoareau TB, Hurley BP, Wingfield MJ, Lawson S, Nahrung HF, Slippers B (2018) Population genetic analyses of complex global insect invasions in managed landscapes: a Leptocybe invasa (Hymenoptera) case study. Biol Invasions 20:2395–2420. https://doi.org/10.1007/s10530-018-1709-0
Doğanlar M (2015) Diagnosis of Megastigmus spp. (Hymenoptera: Torymidae) reared from galls of Leptocybe invasa Fisher & La Salle, 2004, (Hymenoptera: Eulophidae) on Eucalyptus spp. (Myrtaceae), with description of a new species from South Africa. Entomofauna 36:561–580
Doğanlar M, Hassan E (2010) Review of Australian species of Megastigmus (Hymenoptera: Torymidae) associated with Eucalyptus, with descriptions of new species. Aust J Basic Appl Sci 4:5059–5120
Doğanlar M, Zaché B, Wilcken CF (2013) A new species of Megastigmus (Hymenoptera: Torymidae: Megastigminae) from Brazil. Fla Entomol 96:196–199
Doğanlar MD, Huang ZY, Guo CH, Lu W, Yang ZD, Yang XH, Zheng XL (2017) A new species of Megastigmus (Hymenoptera:Torymidae:Megastigminae) form China. Mun Ent Zool 12:368–374
Feng MX (2016) Study on biology and ecology of Quadrastichus mendeli Kim & La Salle (Hymenoptera: Eulophidae). Master’ thesis, University of Hainan, China
Fuester RW, Swan KS, Dunning K, Taylor PB, Ramaseshiah G (2003) Malebiased sex ratios in Glyptapanteles flavicoxis (Hymenoptera: Braconidae), a parasitoid of gypsy moth (Lepidoptera: Lymantriidae). Ann Entomol Soc Am 96:553–559
Gibbs M, Schönrogge K, Alma A, Melika G, Quacchia A, Stone G, Aebi A (2011) Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe. Biocontrol 56:527–538. https://doi.org/10.1007/s10526-011-9364-8
Gualtieri L, Nugnes F, Nappo AG, Gebiola M, Bernardo U (2017) Life inside a gall: closeness does not favour horizontal transmission of Rickettsia between a gall wasp and its parasitoid. FEMS Microbiol Ecol 93(7):1–11. https://doi.org/10.1093/femsec/fx087
Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJW (2016) Exotic biological control agents: a solution or contribution to arthropod invasions? Biol Invasions 18:953–969
Hernández CM, Aquino DA, Cuello EM, Andorno AV, Botto EN (2015) First record of Megastigmus zebrinus Grissell from Argentina (Hymenoptera: Torymidae) associated with galls of Leptocybe invasa (Hymenoptera: Eulophidae). Rev Soc Entomol Argent 74:75–77
Hurley B (2012) First discovery of Selitrichodes neseri in the field [EB/OL]. http://www.forestry.co.za/first-discovery-of-selitrichodes-neseri-in-the-field/. (accessed 3 January 2018)
Hurley BP, Gevers C, Dittrich-Schröder G, Slippers B (2017a) Investigating the complex gall community of Leptocybe invasa. (Conference: Proceedings of the 5th International Symposium on Biological Control of Arthropods, Langkawi, Malaysia. September 11–15)
Hurley BP, Slippers B, Wingfield MJ (2017b) Biological control of insects in plantation forests: optimising an old approach for diverse and changing environments. (Conference: 7th Forest Science Symposium Fems)
Jacob JP, Senthil K, Sivakumar V, Seenivasan R, Chezhian P, Kumar NK (2015) Gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) management in eucalypts. J Biol Control 29:20–24
Javaregowda J, Prabhu ST, Patil RS (2010) Evaluation of botanicals and synthetic insecticides against eucalyptus gall wasp, Leptocybe invasa (Eulophidae: Hymenoptera). Karnataka J Agric Sci 23:200–202
Kelly J, La Salle J, Harney M (2012) Selitrichodes neseri n. sp., a new parasitoid of the eucalyptus gall wasp Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa 3333:50–57
Kenis M (1996) Factors affecting sex ratio in rearing of Coeloides sordidator (Hymenoptera: Braconidae). Entomophaga 41:217–224
Kim IK, Mendel Z, Protasov A (2008) Taxonomy, biology, and efficacy of two Australian parasitoids of the eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa 1910:1–20
Kulkarni H (2010) Distribution, seasonal incidence and management of eucalyptus gall wasp with special reference to native parasitoids. Master’s thesis, University of Agricultural Sciences, Bangalore, India
Kulkarni H, Kumari NK, Vastrad AS (2010) Release and recovery of parasitoids in eucalyptus against gall wasp, Leptocybe invasa (Hymenoptera: Eulophidae) under green house. Karnataka J Agri Sci 23:91–92
Kumari NK (2009) Bioecology and management of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). Master’s thesis, University of Agricultural Sciences, Bangalore, India
Lawson S (2012) Biological control of eucalypt pests overseas and in Australia. Australian Centre for International Agricultural Research (ACIAR), Canberra. Publication FR2012-26
Lawson S, Douangboupha B, Phongoudome C, Ol US, Wiwatwitaya D, Thu PQ, Bartlett T (2014) Biological control of galling pests in eucalypt plantations in the Mekong region. http://aciar.gov.au/project/fst/2012/091. (accessed 3 January 2018)
Lawson SA, Nahrung HF, Griffiths M, Healey MA (2017) BiCEP: Progress in a global collaboration for the biological control of Australian-origin eucalypt pests. (Conference: Proceedings of the 5th International Symposium on Biological Control of Arthropods, Langkawi, Malaysia)
Li DW, Wu YJ, Jiang XJ, Chang MS, Huang HY, Qin YL (2010) Aprostocetus sp. a parasitoid on the Leptocybe invasa. Chin For Sci Technol 24:52–54 (in Chinese with English summary)
Liang YP, Zheng LF, Li YZ, Wen XJ, Li JY (2010) Investigations of natural enemies in China of Leptocybe invasa Fisher & La Salle and observations on predating of the predatory natural enemy. Guangdong Forest Sci Technol 26:1–5 (in Chinese with English summary)
Louda SM, Pemborton RW, Johnson MT, Follet PA (2003) Nontarget effects—the Achillis’ heel of biological control? Retrospective analyses to reduce risk associate with biocontrol introductions. Annu Rev Entomol 43:101–113
Maatouf N, Lumaret JP (2012) Eco-ethology of new invasive pest species on eucalyptus plantation of Morocco. Ann Entomol Soc Am 48:289–297
Masson MV, Tavares WDS, Lopes FDA, Souza ARD, Ferreira-Filho PJ, Barbosa LR, Wilcken CF, Zanuncio JC (2017) Selitrichodes neseri (Hymenoptera: Eulophidae) recovered from Leptocybe invasa (Hymenoptera: Eulophidae) galls after initial release on eucalyptus (Myrtaceae) in Brazil, and data on its biology. Fla Entomol 100:589–593
Mendel Z, Protasov A, Fisher N, La Salle J (2004) Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on eucalyptus. Aust J Entomol 43:101–113
Mendel Z, Protasov A, La Salle J (2017) Classical biological control of two eucalyptus gall wasps; main outcome and conclusions. Biol Control 105:66–78
Moriya S, Shinga M, Adachi I (2003) Classical biological control of the chestnut gall wasp in Japan. In: Van Driesche R (ed) Proc 1st Internat Symp, Biological Control of Arthropods. US Dept Agr For Serv, Honolulu, pp 407–415
Narendran TC, Kumar PG, Vastrad AS (2010) Two new species of Megastigmus dalman (Hymenoptera: Torymidae) from India, with a revised key to Indian species. Rec Zool Surv India 110:1–6
Nicholls JA, Fuentes-Utrilla P, Hayward A, Melika G, Csoka G, Nieves-Aldrey JL, Pujade-Villar J, Tavakoli M, Schonrogge K, Stone GN (2010) Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts. Evol Biol 10:1–12
Nugnes F, Gebiola M, Monti M, Gualtieri L, Giorgini M, Wang J, Bernardo U (2015) Genetic diversity of the invasive gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) and of its rickettsia endosymbiont, and associated sex-ratio differences. PLoS One 10(5):e0124660. https://doi.org/10.1371/journal.pone.0124660
Nugnes F, Gebiola M, Gualtieri L (2016) When exotic biocontrol agents travel without passport: first record of Quadrastichus mendeli, parasitoid of the blue-gum chalcid Leptocybe invasa, in Italy. B Insectol 69:85–91
Odhiambo KO, Wanjala FME, Khaemba BN (2013) Ecological dynamics and cultural control of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle. Afr J Educ Sci Technol 1:75–83
Protasov A, La Salle J, Blumberg D (2007) Biology, revised taxonomy and impact on host plants of Ophelimus maskelli, an invasive gall inducer on Eucalyptus spp. in the Mediterranean area. Phytoparasitica 35:50–76
Protasov A, Doğanlar M, La Salle J, Mendel Z (2008) Occurrence of two local Megastigmus species parasitic on the eucalyptus gall wasp Leptocybe invasa in Israel and Turkey. Phytoparasitica 36:449–459
Ramanagouda SH (2012) Studies on biological control, host plant resistance and genetic diversity of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). Master’s thesis, University of Agricultural Sciences, Dharwad, Bangalore, India
Ramanagouda SH, Vastrad A (2015) Biological control of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) by its native parasitoids. Entomon 40:85–96
Ramanagouda SH, Vastrad AS, Narendran TC, Basavanagoud K, Shashidhar V (2011) Current status of eucalyptus gall wasp and its native parasitoids in Karnataka. J Biol Control 25:193–197
Rizzo MC, Verde GL, Rizzo R, Caleca V (2015) Risk assessment of non-target effects of Closterocerus chamaeleon (Girault) parasitoid of the eucalypt gall maker Ophelimus maskelli (Ashmead) (Hymenoptera, Eulophidae). Phytoparasitica 43:407–415
Sangtongpraow B, Charernsom K (2012) Longevity and developmental time of Aprostocetus sp. (Hymenoptera: Eulophidae), the local parasitoid of Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). (Conference: International Symposium of BioPesticides and Ecotoxicological Network, 2nd IS - BioPEN, September 24–25, At Maruay Garden Hotel, Bangkok, Thailand)
Sangtongpraow B, Charernsom K (2013) Evaluation of parasitism capacity of Megastigmus thitipornae Doğanlar & Hassan (Hymenoptera: Torymidae), the local parasitoid of eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). Kasetsart J (Nat Sci) 47:191–204
Shafiee S, Hesami S, Madjdzadeh SM, Gheibi M (2014) New records of six species of Eulophidae (Hymenoptera: Chalcidoidea) from Iran. In: Proceedings of the 21st Iranian Plant Protection Congress, Urmia University, Iran. 723 p
Shivaraju C (2012) Bio-intensive management of invasive eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Eulophidae: Hymenoptera). Master’s thesis, University of Agricultural Sciences, Dharwad, Bangalore, India
Shylesha AN (2008) Classical biological control of eucalyptus gall wasp Leptocybe invasa Fisher & La Salle. Final project report on the management of emerging pests Eucalyptus, URL: http://www.dcpulppaper.org/gifs/report63.pdf
Silva IMMS, Van Meer MMM, Roskam MM, Hoogenboom A, Gort G, Stouthamer R (2000) Biological control potential of Wolbachia-infected versus uninfected wasps: laboratory and greenhouse evaluation of Trichogramma cordubensis and T. deion strains. Biocontrol Sci Tech 10:223–238
Udagedara UKSK, Warusapperuma KAIP (2014) Biology, damage and parasitoids of the eucalyptus gall wasp, Leptocybe invasa (Hymenoptera: Eulophidae), infesting Eucalyptus camaldulensis (Myrtaceae) in Maragamuwa plantation, Sri Lanka. Int J Tropical Insect Sci 34:179–189
Vargo EL, Husseneder C, Woodson D, Waldvogel MG, Grace JK (2006) Genetic analysis of colony and population structure of three introduced populations of the formosan subterranean termite (Isoptera: Rhinotermitidae) in the continental United States. Environ Entomol 35:151–166
Vastrad AS, Basavanagoud K, Kumari NK (2010) Native parasitoids of eucalyptus gall wasp. Entomon 34:197–200
Verghese A, Bakthavatsalam N, Shylesha AN, Jacob JP, Ravindra KV (2013) Management of eucalyptus gall wasp, Leptocybe invasa through classical biological control and Semiochemicals. (Conference: National Workshop on eucalyptus Gall Wasp - Present Status and Future Strategies, At IFGTB, Coimbatore India, Volume: 1)
Viggiani G, Laudonia S, Bernardo U (2000) The increase of insect pests in Eucalyptus. Informatore Agrario 58:86–87
Xu JX, Ren H, Zhao DY, Lin MS, Qiu HX, Zhong TK, Chen MR, Huang MY, Chen RP (2008) Study on the population regularity and spatial distribution pattern of Leptocybe invasa at Eucalyptus. Guangdong Forest Sci Technol 24:50–57 (in Chinese with English summary)
Yang MM, Lin YC, Wu YJ, Fisher N (2014) Two new Aprostocetus species (Hymenoptera: Eulophidae: Tetrastichinae), fortuitous parasitoids of invasive eulophid gall inducers (Tetrastichinae) on Eucalyptus and Erythrina. Zootaxa 3846:261–272
Yousuf M, Singh S, Ikram M, Singh RB (2014) Biological control of Leptocybe invasa “eucalyptus gall wasp” in Punjab. (Conference: 13th Silviculture Conference, Management of Insect Pests/ diseases, At Forest Research Institute, Dehra Dun, India)
Yousuf M, Singh S, Ikram M, Singh RB (2017) Release of larval parasitoids for biological control of eucalyptus gall wasp Leptocybe invasa in Punjab and their impact. FRI Dehradun, India, XIX Commonwealth Forestry conference, Forest Research Institute DOI:https://doi.org/10.13140/RG.2.2.15600.66561
Zheng XL, Li J, Yang ZD, Xian ZH, Wei JG, Lei CL, Wang XP, Lu W (2014) A review of invasive biology, prevalence and management of Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Afr Entomol 22:68–79
Zheng XL, Huang ZY, Dong D, Guo CH, Li J, Yang ZD, Yang XH, Lu W (2016) Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China. Parasite 23:58. https://doi.org/10.1051/parasite/2016071
Acknowledgements
We are grateful to Prof. & Dr. Mikdat Doğanlar (Biological Control Research Station, Adana, Turkey) for providing very useful information and thank Dr. Brett P. Hurley (University of Pretoria, Pretoria, South Africa) for providing references and publications. We also thank the anonymous reviewers for their valuable comments on an earlier version.
Funding
This work was supported by the National Natural Science Foundation of China [grant number: 31870634 and 31560212] and the Natural Science Foundation of Guangxi [grant number: 2018GXNSFAA138099].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Huang, ZY., Li, J., Lu, W. et al. Parasitoids of the eucalyptus gall wasp Leptocybe spp.: a global review. Environ Sci Pollut Res 25, 29983–29995 (2018). https://doi.org/10.1007/s11356-018-3073-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-3073-0