Quadrastichus mendeli (Hymenoptera: Eulophidae): parasitism on Leptocybe invasa (Hymenoptera: Eulophidae) and first record in Brazil

The eucalyptus gall wasp Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae), of the subfamily Tetrastichinae, from Australia, is an important exotic pest in eucalypts plantations in the world. The first report of L. invasa in Brazil was in 2007 damaging plants of Eucalyptus camaldulensis x Eucalyptus grandis hybrid clones in nursery and plantations in the Bahia state (Costa et al., 2008).

Damage by this insect reduces the growth and wood production of Eucalyptus spp. This insect lays eggs in the region of the central rib of the leaves, petiole, apex and new branches where its larvae make galls, affecting the sap flow and may cause plant death (Kavitha-Kumari et al., 2010; Costa et al., 2008).

Biological control and genetic selection of plants are promising to manage L. invasa, since the efficiency of chemical insecticides against larvae of this pest in their galls is reduced (Masson, 2015). The specific parasitoid of L. invasa, Selitrichodes neseri Kelly & La Salle (Hymenoptera: Eulophidae: Tetrastichinae), was imported from South Africa to Brazil in 2015. This natural enemy has adapted to laboratory rearing, released and established in the field with adequate efficiency (Masson et al., 2017). Quadrastichus mendeli Kim & La Salle (Hymenoptera: Eulophidae: Tetrastichinae), from Australia, is another promising and effective parasitoid of L. invasa (Kim et al., 2008).

The parasitoid Q. mendeli is distributed in South Africa, Argentina, China, India, Israel, Italy and Thailand with adequate parasitism levels (Kim et al., 2008; Shylesha, 2008; Nugnes et al.; 2016; Zheng et al., 2016; Mendel et al., 2017; Aquino et al., 2018; Bush et al., 2018; Sangtongpraow & Charernsom, 2019) and efficiently controlled L. invasa in Thailand (Sangtongpraow & Charernsom, 2019).

Quadrastichus mendeli parasitized young and mature Leptocybe sp. larvae (Huang et al., 2018a) and its well-developed ovipositor is adapted to access its host inside the galls (Huang et al., 2019). In addition, the high number and variety of chemosensory antennal sensilla on the Q. mendeli indicate that olfactory cues are important for this natural enemy host pests (Huang et al., 2018b). Volatiles released by galls induced by L. invasa attract Q. mendeli (Huang et al., 2021, 2022).

Branches of a Eucalyptus grandis clone with developed L. invasa galls were collected in a forest plantation in the municipality of Luís Antônio (-21.49583, -47.93254), São Paulo state, Brazil in 2018. These branches were transferred to the Laboratory of Biological Control of Forest Pests (LCBPF) of the FCA/UNESP, Campus of Botucatu, São Paulo state, Brazil, caged in plastic pots with water in acrylic vial at 25 ± 2 °C and 60 ± 2% relative humidity until insect emergence. The insects emerged were identified as L. invasa females, except for 30 individuals of other species (Figure 1). The latter were sent to Dr. II-Kwon Kim (School of Botany and Zoology, Australian National University) for identification confirming Quadrastichus mendeli Kim and La Salle (Hymenoptera: Eulophidae: Tetrastichinae).

Figure 1
Quadrastichus mendeli (Hymenoptera: Eulophidae: Tetrastichinae) females (A) emerged from Leptocybe invasa (Hymenoptera: Eulophidae) galls and parasitizing L. invasa larvae into its galls (B).

The DNA, which identified the insect as Q. mendeli was extracted and analyzed, in triplicate, with 80 μL of 10% Chelex100® resin solution [Bio-Rad Laboratories, USA] and 8 μlL of proteinase K (20 mg/ml). The 28S gene of Q. mendeli was amplified in a thermocycler [Infinigen, TC-96CG, USA] with the primers 28SF3633 (5'-TACCGTGAGGGAAAGTTGAAA −3′) and 28SR4076 (5′-AGACTCCT TGGTCCGTGTTT −3′) (Tiawsirisup et al., 2008) following the PCR denaturation cycle with initial denaturation step at 94 °C for 2 min; 38 cycles of 94 °C for 30 s, annealing at 58 °C for 50 s, 72 °C for 1 min 30 s; and extension at 72 °C for 10 min, submitted to 1% agarose gel electrophoresis and analyzed with UV light. The DNA sequence obtained showed high identity with Q. mendeli 28s gene and it was deposited in the GenBank as accession nº. MT645225.

Leptocybe invasa galls were offered to Q. mendeli females after the identification of this natural enemy, to evaluate parasitism. Quadrastichus mendeli parasitized L. invasa larvae (Figure 1), completed its cycle inside this pest galls and its adults emerged after 40 days of parasitism. The parasitism of L. invasa larvae into galls by Q. mendeli supports the potential of this parasitoid as a biological control agent in the integrated management of L. invasa in Brazil.

This manuscript is an original contribution with the first report of the occurrence of Q. mendeli in Brazil and its record parasitizing L. invasa larvae into its galls, as a good contribution for biological control programs of this pest.

Acknowledgements

To the Brazilian institutions “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES- Finance Code 001), “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)” for financial support.

References

• AQUINO, D.A., ANDORNO, A.V., PATHAUER, P.S., BOTTO, E.N. and LÓPEZ, S.N., 2018. Primera cita de Quadrastichus mendeli (Hymenoptera: Eulophidae: Tetrastichinae) de Argentina, asociado a agallas de Leptocybe invasa (Hymenoptera: Eulophidae: Tetrastichinae). Acta Zoológica Lilloana, vol. 68, no. 1, pp. 50-52.
• BUSH, S.J., DITTRICH-SCHRÖDER, G., NESER, S., GEVERS, C., BAFFOE, K.O., SLIPPERS, B. and HURLEY, B.P., 2018. First record of Quadrastichus mendeli, a parasitoid of Leptocybe invasa, in South Africa. Southern Forests, vol. 80, no. 3, pp. 275-277. http://dx.doi.org/10.2989/20702620.2017.1318347
  » http://dx.doi.org/10.2989/20702620.2017.1318347
• COSTA, V.A., BERTI FILHO, E., WILCKEN, C.F., STAPE, J.L., LASALLE, J. and DE DIANA 0TEIXEIRA, L., 2008. Eucalyptus gall-wasp Leptocybe invasa Fisher & La Salle (Eulophidae, Hymenoptera), in Brasil: new forest pest reaches the new word. Revista de Agricultura, vol. 83, no. 2, pp. 136-139. http://dx.doi.org/10.37856/bja.v83i2.1479
  » http://dx.doi.org/10.37856/bja.v83i2.1479
• HUANG, Z.Y., LI, J., LU, W., ZHENG, X.L. and YANG, Z.D., 2018a. Parasitoids of the eucalyptus gall wasp Leptocybe spp.: a global review. Environmental Science and Pollution Research International, vol. 25, no. 30, pp. 29983-29995. http://dx.doi.org/10.1007/s11356-018-3073-0 PMid:30178405.
  » http://dx.doi.org/10.1007/s11356-018-3073-0
• HUANG, Z.Y., LI, S.Y., LU, W. and ZHENG, X.L., 2019. Structure and sense organs of ovipositors of an endoparasitoid Aprostocetus causalis and an ectoparasitoid Quadrastichus mendeli in Leptocybe spp. Microscopy and Microanalysis, vol. 25, no. 1, pp. 250-256. http://dx.doi.org/10.1017/S1431927618015647 PMid:30712524.
  » http://dx.doi.org/10.1017/S1431927618015647
• HUANG, Z.Y., LIU, Z.J., WANG, X.Y., ZHANG, Z.L., LU, W. and ZHENG, X.L., 2022. Electroantennographic and olfactory responses of Quadrastichus mendeli to eucalyptus volatiles induced by the gall-forming insect Leptocybe invasa. Pest Management Science, vol. 78, no. 6, pp. 2405-2416. http://dx.doi.org/10.1002/ps.6869 PMid:35289069.
  » http://dx.doi.org/10.1002/ps.6869
• HUANG, Z.Y., WANG, X.Y., LU, W. and ZHENG, X.L., 2021. Sensory gene identification in the transcriptome of the ectoparasitoid Quadrastichus mendeli. Scientific Reports, vol. 11, no. 1, pp. 9726. http://dx.doi.org/10.1038/s41598-021-89253-w PMid:33958688.
  » http://dx.doi.org/10.1038/s41598-021-89253-w
• HUANG, Z.Y., ZHANG, Y.J., LIU, J.Y., YANG, Z.D., LU, W. and ZHENG, X.L., 2018b. Ultrastructure of female antennal sensilla of an endoparasitoid wasp, Quadrastichus mendeli Kim & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Microscopy and Microanalysis, vol. 24, no. 4, pp. 431-441. http://dx.doi.org/10.1017/S1431927618012424 PMid:30175705.
  » http://dx.doi.org/10.1017/S1431927618012424
• KAVITHA-KUMARI, N., KULKARNI, H., VASTRAD, A.S. and GOUD, K.B., 2010. Biology of eucalyptus gall wasp, Leptocybe invasa Fisher and La Salle (Hymenoptera: eulophidae). Karnataka Journal of Agricultural Sciences, vol. 23, pp. 211-212.
• KIM, I.K., MENDEL, Z., PROTASOV, A., BLUMBERG, D. and LA SALLE, J., 2008. Taxonomy, biology and efficacy of two Australian parasitoids of the eucalyptus gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae: Tetrastichinae). Zootaxa, vol. 1910, no. 1, pp. 1-20. http://dx.doi.org/10.11646/zootaxa.1910.1.1
  » http://dx.doi.org/10.11646/zootaxa.1910.1.1
• MASSON, V.M., 2015. Dinâmica populacional e manejo de Leptocybe invasa (Hymenoptera: Eulophidae) em plantações de eucalipto. São Paulo: Faculdade de Ciências Agronômicas, Universidade Estadual Paulista, 86 p. Tese de Doutorado em Ciência Florestal.
• MASSON, V.M., TAVARES, W.S., LOPES, F.A., SOUZA, A.R., FERREIRA-FILHO, P.J., BARBOSA, L.R., WILCKEN, C.F. and ZANUNCIO, J.C., 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. The Florida Entomologist, vol. 100, no. 3, pp. 589-593. http://dx.doi.org/10.1653/024.100.0316
  » http://dx.doi.org/10.1653/024.100.0316
• MENDEL, Z., PROTASOV, A., LA SALLE, J., BLUMBERG, D., BRAND, D. and BRANCO, M., 2017. Classical biological control of two Eucalyptus gall wasps, main outcome and conclusions. Biological Control, vol. 105, pp. 66-78. http://dx.doi.org/10.1016/j.biocontrol.2016.11.010
  » http://dx.doi.org/10.1016/j.biocontrol.2016.11.010
• NUGNES, F., GEBIOLA, M., GUALTIERI, L., RUSSO, E., SASSO, R. and BERNARDO, U., 2016. When exotic biocontrol agents travel without passport: first record of Quadrastichus mendeli, parasitoid of the blue-gum chalcid Leptocybe invasa, in Italy. Bulletin of Insectology, vol. 69, no. 1, pp. 85-91.
• SANGTONGPRAOW, B. and CHARERNSOM, K., 2019. Biological traits of Quadrastichus mendeli (Hymenoptera, Eulophidae), parasitoid of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera, Eulophidae) in Thailand. Parasite, vol. 26, pp. 8. http://dx.doi.org/10.1051/parasite/2019008 PMid:30794147.
  » http://dx.doi.org/10.1051/parasite/2019008
• SHYLESHA, A.N., 2008. Classical biological control of Eucalyptus gall wasp Leptocybe invasa Fisher & La Salle: final project report on the management of emerging pests Eucalyptus. Bangalore: National Bureau of Agriculturally Important Insects. Available from: http://www.dcpulppaper.org/gifs/ report63.pdf
  » http://www.dcpulppaper.org/gifs/
• TIAWSIRISUP, S., SRIPATRANUSORN, S., ORAVEERAKUL, K. and NUCHPRAYOON, S., 2008. Distribution of mosquito (Diptera: Culicidae) species and Wolbachia (Rickettsiales: Rickettsiaceae) infections during the bird immigration season in Pathumthani province, central Thailand. Parasitology Research, vol. 102, no. 4, pp. 731-735. http://dx.doi.org/10.1007/s00436-007-0825-z PMid:18066693.
  » http://dx.doi.org/10.1007/s00436-007-0825-z
• ZHENG, X.L., HUANG, Z.Y., DONG, D., GUO, C.H., LI, L., YANG, Y., YANG, X.H. and LU, W., 2016. Parasitoids of the eucalyptus gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) in China. Parasite, vol. 23, no. 1, pp. 58-65. http://dx.doi.org/10.1051/parasite/2016071 PMid:28000590.
  » http://dx.doi.org/10.1051/parasite/2016071

Publication Dates

• Publication in this collection
  29 July 2022
• Date of issue
  2022

History

• Received
  07 June 2022
• Accepted
  19 July 2022