First occurrence of Euneura sopolis (Hymenoptera, Pteromalidae) hyperparasiting Xenostigmus bifasciatus (Hymenoptera, Braconidae) in Brazil: implications for biological control of pine aphids

S. B. Z. Cunha A. N. Ferreira M. T. Tavares C. R. Sousa-Silva About the authors

It is estimated that the planting of pinus in Brazil exceeds 2 million hectares comprising mainly two species Pinus taeda and P. elliottii. Due to the expansion of this culture and the often inappropriate cultural methods, this crop became increasingly susceptible to pest insects (Zaleski et al., 2005Zaleski, S.R.M., Lazzari, S.M.N. and Penteado, S.R.C., 2005. Danos qualitativos e quantitativos de Cinara atlantica (Wilson) (Hemiptera:Aphididae) em mudas de Pinus taeda Linnaeus (Pinaceae). Revista Brasileira de Zoologia, vol. 3, no. 22, pp. 591-596. http://dx.doi.org/10.1590/S0101-81752005000300011.
http://dx.doi.org/10.1590/S0101-81752005...
). Among these the aphids are outstanding due to their characteristics such as high fertility, presence of both wingless and winged forms, thus facilitating dispersal, parthenogenetic reproduction that coupled to the favorable Brazilian climatic conditions make them one of the most important pests of Pinus spp. plantations (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.).

Because aphids are easily dispersed, several species some of the genus Cinara occur in the regions with conifers plantations, usually of the families Pinaceae and Cupressaceae as hosts. They are observed feeding on pine branches, sprouts and even the roots (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.). In this genus there are ca. 200 species (Costa et al., 1993Costa, C.L., Eastop, V.F. and Blackmam, R.L., 1993. Brazilian Aphidoidea:II. Accounts of the Lachninae, Chaitophorinae, Greenideinae, Anoeciinae, and Hormaphidinae. Pesquisa Agropecuaria Brasileira, vol. 28, no. 3, pp. 269-280.). According to Sousa-Silva and Ilharco (1995)Sousa-Silva, C.R. and Ilharco, F.A., 1995. Afídeos do Brasil e suas plantas hospedeiras (lista preliminar). São Carlos: Edufscar. 85 p., the species Cinara atlantica, C. cupressi, C. fresai, C. maritimae, C. piniformosana, C. pinivora and C. tujafilina occur in Brazil.

Infestations of aphids on pine can cause considerable decrease on growth and morphological changes that significantly reduces the economic value of wood (Zaleski et al., 2005Zaleski, S.R.M., Lazzari, S.M.N. and Penteado, S.R.C., 2005. Danos qualitativos e quantitativos de Cinara atlantica (Wilson) (Hemiptera:Aphididae) em mudas de Pinus taeda Linnaeus (Pinaceae). Revista Brasileira de Zoologia, vol. 3, no. 22, pp. 591-596. http://dx.doi.org/10.1590/S0101-81752005000300011.
http://dx.doi.org/10.1590/S0101-81752005...
). The control of aphids is based mainly on biological methods using predators, parasitoids and entomopathogenic fungi.

Predators as the coleopterans (Coccinellidae), neuropterans (Chrysopidae) and the larvae of the dipterans (Syrphidae), are found near the colonies of aphids, which occur in abundance in the winter, when the number of predators decreases and the control of large pest populations decreases as well. Therefore, the use of parasitoids, besides being specific is also more efficient (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.). The parasitoids species belonging to the genera Pauesia and Xenostigmus (Hymenoptera: Braconidae) are the most frequently used to control aphids attacking pine plantations.

To control populations of C. atlantica and C. pinivora in pinus plantations in Paraná state, Brazil, a program was started to introduce the parasitoid Xenostigmus bifasciatus from the USA east coast. The mummified aphids were collected in North America and a quarantined was carried out in Brazil before these parasitoids were cultured and released in the field (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.). The release occurred between 2002 and 2004 in different municipalities of Paraná and Santa Catarina states. Shortly thereafter, this parasitoid was recorded in several areas attacked by the pine aphid and its dispersion was estimated at approximately 80 km per year, and so its establishment in Brazil was confirmed (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.).

This study aimed to determine the occurrence of aphid species in a P. elliottii plantation in a Cerrado area at the São Carlos region and the possible occurrence of their natural enemies. Ten samplings were carried out from October 2013 to August 2014 in P. elliottii plantation area of approximately 4,000 square meters at the 21 ° 58'24.02 “S, 47 ° 53'7.39” W. The collected aphids were placed in bottles containing 100% alcohol and later mounted on microscope slides, according to the methodology described by Ilharco and Lemos (1981)Ilharco, F.A. and Lemos, A., 1981. Algumas notas sobre a montagem de afídeos para observação microscópica (Homoptera: Aphidoidea). Agronomia Lusitana , vol. 41, pp. 53-57.. They were subsequently identified under an optical microscope using the key of Costa et al. (1993)Costa, C.L., Eastop, V.F. and Blackmam, R.L., 1993. Brazilian Aphidoidea:II. Accounts of the Lachninae, Chaitophorinae, Greenideinae, Anoeciinae, and Hormaphidinae. Pesquisa Agropecuaria Brasileira, vol. 28, no. 3, pp. 269-280.. The mummies were placed in Eppendorf tubes and after the emergence the parasitoids were preserved in 70% ethanol and then mounted and identified.

Cinara maritimae was the aphid with the highest frequency of occurrence during the collection period. From the 63 mummies of C. maritimae collected, the parasitoid Xenostigmus bifasciatus (Ashmead) emerged from only two, whereas the hyperparasitoid Euneura sopolis (Walker) emerged from 23 mummies.

Xenostigmus bifasciatus was introduced in 2002 in Paraná state to control the species C. atlantica and C. pinivora, pests of pine, and its occurrence has also been reported in several regions of the states of Santa Catarina, Minas Gerais and São Paulo. However this is the first report of X. bifasciatus parasitizing C. maritimae.

Euneura sopolis is widely distributed in Europe, Japan and Eastern United States. Its presence in Brazil is here recorded for the first time. This species parasitizes microhymenopterans of the genera Pauesia and Xenostigmus (Garrido Torres and Nieves-Aldrey, 1999GARRIDO TORRES, A.M. and NIEVES-ALDREY, J.L., 1999. Pteromálidos de la comunidad de Madrid: faunística y catálogo (Hymenoptera, Chalcidoidea, Pteromalidae). Graellsia, vol. 55, no. 0, pp. 9-147. http://dx.doi.org/10.3989/graellsia.1999.v55.i0.322.
http://dx.doi.org/10.3989/graellsia.1999...
), parasitoids of aphids belonging to the Lachnidae family.

In the quarantine period before the introduction of X. bifasciatus in Brazil, in 2002, several hyperparasitoids emerged from mummies of C. atlantica brought from the USA: Alloxysta lachni, Anastastus sp., Asaphes suspensus, Dendrocerus sp., Diaretus sp., Syrphofagus sp., Tetrastichus sp., Euneura lachni and Euneura sopolis. These hyperparasitoids were destroyed and samples of X. bifasciatus free from parasitoids were introduced in Paraná state (Penteado et al., 2004Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.).

Acknowledgements

We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

References

  • Costa, C.L., Eastop, V.F. and Blackmam, R.L., 1993. Brazilian Aphidoidea:II. Accounts of the Lachninae, Chaitophorinae, Greenideinae, Anoeciinae, and Hormaphidinae. Pesquisa Agropecuaria Brasileira, vol. 28, no. 3, pp. 269-280.
  • GARRIDO TORRES, A.M. and NIEVES-ALDREY, J.L., 1999. Pteromálidos de la comunidad de Madrid: faunística y catálogo (Hymenoptera, Chalcidoidea, Pteromalidae). Graellsia, vol. 55, no. 0, pp. 9-147. http://dx.doi.org/10.3989/graellsia.1999.v55.i0.322
    » http://dx.doi.org/10.3989/graellsia.1999.v55.i0.322
  • Ilharco, F.A. and Lemos, A., 1981. Algumas notas sobre a montagem de afídeos para observação microscópica (Homoptera: Aphidoidea). Agronomia Lusitana , vol. 41, pp. 53-57.
  • Penteado, S.R.C., Reis-Filho, W. and Iede, E.T., 2004. Os pulgões-gigantes-do-Pinus, Cinara pinivora e Cinara atlantica, no Brasil. Circular Técnica, vol. 87, pp. 1-10.
  • Sousa-Silva, C.R. and Ilharco, F.A., 1995. Afídeos do Brasil e suas plantas hospedeiras (lista preliminar). São Carlos: Edufscar. 85 p.
  • Zaleski, S.R.M., Lazzari, S.M.N. and Penteado, S.R.C., 2005. Danos qualitativos e quantitativos de Cinara atlantica (Wilson) (Hemiptera:Aphididae) em mudas de Pinus taeda Linnaeus (Pinaceae). Revista Brasileira de Zoologia, vol. 3, no. 22, pp. 591-596. http://dx.doi.org/10.1590/S0101-81752005000300011
    » http://dx.doi.org/10.1590/S0101-81752005000300011

Publication Dates

  • Publication in this collection
    03 May 2016
  • Date of issue
    Jul-Sep 2016

History

  • Received
    11 Nov 2014
  • Accepted
    29 June 2015
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br