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Occurrence of Allorhogas sp. (Hymenoptera: Braconidae: Doryctinae) associated with galls on seeds of Inga vera (Fabaceae) in Brazil

The first phytophagy record of the Braconidae family was made by Macêdo and Monteiro (1989)MACÊDO, M.V. and MONTEIRO, R.F., 1989. Seed predation by a braconid wasp, sp. (Hymenoptera). AllorhogasJournal of the New York Entomological Society, vol. 97, no. 3, pp. 358-362. for Brazil, where Allorhogas dyspistus Marsh 1991 was observed feeding on immature seeds of the leguminous plant Pithecellobium tortum Martius (Fabaceae). Later new cases of phytophagy of the genus Allorhogas Gahan 1912 were described in leguminous seeds in Brazil. Marsh et al. (2000)MARSH, P.M., MACÊDO, M.V. and PIMENTAL, M.C.P., 2000. Descriptions and biological notes on two new phytophagous species of the genus from Brazil (Hymenoptera: Braconidae: Doryctinae). AllorhogasJournal of Hymenoptera Research, vol. 9, no. 2, pp. 292-297. found two species: Allorhogas brasiliensis Marsh 2000 in Balizia pedicellaris (DC.) Barnaby & J.W. Grimes (cited as Pithecellobium) and Allorhogas spermaphagus Marsh, 2000 in Stryphnodendron polyphyllum Martius. Tuller et al. (2015)TULLER, J., PAULA, E.L., MAIA, L.F. and MORAES, R.A., 2015. Seed predation food web, nutrient availability, and impact on the seed germination of . Senegalia tenuifolia (Fabaceae)Revista de Biologia Tropical, vol. 63, no. 4, pp. 1149-1159. http://dx.doi.org/10.15517/rbt.v63i4.16855.
http://dx.doi.org/10.15517/rbt.v63i4.168...
also found an unidentified species feeding on the seeds of Senegalia tenuifolia (L.) Britton & Rose in the region of Lavras, Minas Gerais.

Marsh (2002)MARSH, P.M., 2002. The Doryctinae of Costa Rica (excluding the genus Heterospilus). Madison: Memoirs of the American Entomological Institute. 319 p. reported two species associated with leguminous plants in Costa Rica: Allorhogas argentinus Marsh 2002 forming galls on the seeds of Abarema macradenia (Pittier) Barnaby & J.W. Grimes (cited as Pithecellobium), and Allorhogas hansoni Marsh 2002 associated with Inga vera Willd fruits. Allorhogas species have also been reared from galls on plants of other families such as Melastomataceae and Solanaceae (Chavarría et al., 2009CHAVARRÍA, L., HANSON, P.E., MARSH, P.M. and SHAW, S.R., 2009. A phytophagous braconid, n.sp. (Hymenoptera: Braconidae), in the fruits of . Allorhogas conostegiaConostegia xalapensis (Bonpl.) D. Don (Melastomataceae)Journal of Natural History, vol. 43, no. 43-44, pp. 2677-2689. http://dx.doi.org/10.1080/00222930903243996.
http://dx.doi.org/10.1080/00222930903243...
; Martinez et al., 2011MARTÍNEZ, J.J., ALTAMIRANO, A. and SALVO, A., 2011. New species of Allorhogas Gahan (Hymenoptera: Braconidae) reared from galls on Lycium cestroides Schltdl. (Solanaceae) in Argentina. Entomological Science, vol. 14, no. 3, pp. 304-308. http://dx.doi.org/10.1111/j.1479-8298.2011.00453.x.
http://dx.doi.org/10.1111/j.1479-8298.20...
).

In Brazil, I. vera occurs from Rio Grande do Sul to Minas Gerais states, mainly in the Atlantic rainforest (Figliolia and Kageyama, 1994FIGLIOLIA, M.B. and KAGEYAMA, P.Y., 1994. Maturação de sementes de Hook. et Arn. em floresta ripária do rio Moji-Guaçu, Município de Moji-Guaçu. Inga uruguensisRevista do Instituto Florestal, vol. 6, pp. 13-52.; Lorenzi, 2002LORENZI, H., 2002. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. 4th ed. Nova Odessa: Instituto Plantarum de Estudos da Flora. 368 p.).We collected 10 fruits of an I. vera specimen on November 22, 2013, in an area located on the BR 464 roadway margins, on the border of the municipalities of Delfinópolis and São João Batista do Glória (20° 33' 4.6”S 46° 32' 10.2”W), about 36 km from the main entrance of the Serra da Canastra National Park, in the southwest of Minas Gerais. The tree was found laterally to a bridge over the Rio Grande, whose local vegetation was composed of gallery forest and grassland. The fruits were collected using long-handle (6 meters) pruning shears and individually placed in sealed plastic bags still in the field, later being transported to the laboratory of Entomology at the Universidade do Estado de Minas Gerais, (UEMG - Unidade Passos). In the laboratory, they were individually kept in polypropylene plastic pots (750 ml), sealed with voil fabric for the emerging fauna containment, allowing air circulation and to prevent fungi proliferation. The specimens of Eurytoma Illiger 1807 sp. (Eurytomidae) of this study are found in the same laboratory, and those of Allorhogas sp. are in the Hymenoptera parasitoid studies laboratory of the Department of Ecology and Evolutionary Biology at the Universidade Federal de São Carlos, all in flasks with 70% ethanol. For the identification of specimens we use the following keys to the genera: DiGiulio (1997)DIGIULIO, J.A., 1997. Eurytomidae. In: G.A.P. GIBSON, J.T. HUBER and J.B. WOOLLEY, eds. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa: NRC Research Press, pp. 477-495. (for Eurytoma) and Marsh (1997)MARSH, P.M., 1997. Subfamily Doryctinae. In: R.A. WHARTON, P.M. MARSH and M.J. SHARKEY, eds. Manual of the New World Genera of the Family Braconidae (Hymenoptera). Washington: International Society of Hymenopterists, pp. 207-233. Special Publication, no. 1. (for Allorhogas).

We found five individuals of Allorhogas sp. forming galls on the seeds (Figure 1A), and three individuals of its parasitoid, Eurytoma sp., within the galls formed by them (Figure 1B). Among the galls only one adult of Allorhogas emerged, all other gall produced adult individuals that failed to emerge.

Figure 1
Inga vera seeds with ovoid galls: (A) Galls with Allorhogas sp.; (B) Galls with Allorhogas sp. (Left) and its parasitoid Eurytoma sp. (Right).

Through dissection of galls we observed that there was no evidence of parasitism by Allorhogas because we did not find remains of other species inside the gall chambers, suggesting that Allorhogas is the gall-inducing species. For Eurytoma, we observe that inside the galls had traces of parasitism, but the remains of the host could not be directly associated to Allorhogas. However, specimens of Eurytoma has been pointed out as ectoparasitoides of Allorhogas in works such as those of Macêdo and Monteiro (1989)MACÊDO, M.V. and MONTEIRO, R.F., 1989. Seed predation by a braconid wasp, sp. (Hymenoptera). AllorhogasJournal of the New York Entomological Society, vol. 97, no. 3, pp. 358-362., Penteado-Dias and Carvalho (2008)PENTEADO-DIAS, A.M. and CARVALHO, F.M., 2008. New species of Hymenoptera associated with galls on . Calliandra brevipes Benth. (Fabaceae, Mimosoidea) in BrazilRevista Brasileira de Entomologia, vol. 52, no. 3, pp. 305-310. http://dx.doi.org/10.1590/S0085-56262008000300001.
http://dx.doi.org/10.1590/S0085-56262008...
and Tuller et al. (2015)TULLER, J., PAULA, E.L., MAIA, L.F. and MORAES, R.A., 2015. Seed predation food web, nutrient availability, and impact on the seed germination of . Senegalia tenuifolia (Fabaceae)Revista de Biologia Tropical, vol. 63, no. 4, pp. 1149-1159. http://dx.doi.org/10.15517/rbt.v63i4.16855.
http://dx.doi.org/10.15517/rbt.v63i4.168...
. All galls presented a similar aspect as those observed by Tuller et al. (2015)TULLER, J., PAULA, E.L., MAIA, L.F. and MORAES, R.A., 2015. Seed predation food web, nutrient availability, and impact on the seed germination of . Senegalia tenuifolia (Fabaceae)Revista de Biologia Tropical, vol. 63, no. 4, pp. 1149-1159. http://dx.doi.org/10.15517/rbt.v63i4.16855.
http://dx.doi.org/10.15517/rbt.v63i4.168...
, of Allorhogas specimens feeding on S. tenuifolia seeds extremities and causing their deformation. In our studies the galls had an ovoid aspect with yellow / brown coloration, located at the extremities of the seed.

This study reports for the first time the occurrence of Allorhogas sp. forming galls on Inga vera seeds in Brazil. The detailed biology of most Allorhogas species is still little studied (Chavarría et al., 2009CHAVARRÍA, L., HANSON, P.E., MARSH, P.M. and SHAW, S.R., 2009. A phytophagous braconid, n.sp. (Hymenoptera: Braconidae), in the fruits of . Allorhogas conostegiaConostegia xalapensis (Bonpl.) D. Don (Melastomataceae)Journal of Natural History, vol. 43, no. 43-44, pp. 2677-2689. http://dx.doi.org/10.1080/00222930903243996.
http://dx.doi.org/10.1080/00222930903243...
). Such record may contribute, to both the hymenopteran fauna survey in the Cerrado area, located in the southwest Minas Gerais, and to the advancement of knowledge on Allohogas biology in Brazil.

Acknowledgements

We thank the Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides da Região Sudeste Brasileira (INCT- HYMPAR Sudeste) for the partnership and logistical support. The Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the scholarship provided to T. Morales-Silva. We also thank Domício P. Costa-Júnior for help in the field and Juliano F. Nunes for confirmation of identification of the insects.

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References

  • CHAVARRÍA, L., HANSON, P.E., MARSH, P.M. and SHAW, S.R., 2009. A phytophagous braconid, n.sp. (Hymenoptera: Braconidae), in the fruits of . Allorhogas conostegiaConostegia xalapensis (Bonpl.) D. Don (Melastomataceae)Journal of Natural History, vol. 43, no. 43-44, pp. 2677-2689. http://dx.doi.org/10.1080/00222930903243996
    » http://dx.doi.org/10.1080/00222930903243996
  • DIGIULIO, J.A., 1997. Eurytomidae. In: G.A.P. GIBSON, J.T. HUBER and J.B. WOOLLEY, eds. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa: NRC Research Press, pp. 477-495.
  • FIGLIOLIA, M.B. and KAGEYAMA, P.Y., 1994. Maturação de sementes de Hook. et Arn. em floresta ripária do rio Moji-Guaçu, Município de Moji-Guaçu. Inga uruguensisRevista do Instituto Florestal, vol. 6, pp. 13-52.
  • LORENZI, H., 2002. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. 4th ed. Nova Odessa: Instituto Plantarum de Estudos da Flora. 368 p.
  • MACÊDO, M.V. and MONTEIRO, R.F., 1989. Seed predation by a braconid wasp, sp. (Hymenoptera). AllorhogasJournal of the New York Entomological Society, vol. 97, no. 3, pp. 358-362.
  • MARSH, P.M., 1997. Subfamily Doryctinae. In: R.A. WHARTON, P.M. MARSH and M.J. SHARKEY, eds. Manual of the New World Genera of the Family Braconidae (Hymenoptera). Washington: International Society of Hymenopterists, pp. 207-233. Special Publication, no. 1.
  • MARSH, P.M., 2002. The Doryctinae of Costa Rica (excluding the genus Heterospilus). Madison: Memoirs of the American Entomological Institute. 319 p.
  • MARSH, P.M., MACÊDO, M.V. and PIMENTAL, M.C.P., 2000. Descriptions and biological notes on two new phytophagous species of the genus from Brazil (Hymenoptera: Braconidae: Doryctinae). AllorhogasJournal of Hymenoptera Research, vol. 9, no. 2, pp. 292-297.
  • MARTÍNEZ, J.J., ALTAMIRANO, A. and SALVO, A., 2011. New species of Allorhogas Gahan (Hymenoptera: Braconidae) reared from galls on Lycium cestroides Schltdl. (Solanaceae) in Argentina. Entomological Science, vol. 14, no. 3, pp. 304-308. http://dx.doi.org/10.1111/j.1479-8298.2011.00453.x
    » http://dx.doi.org/10.1111/j.1479-8298.2011.00453.x
  • PENTEADO-DIAS, A.M. and CARVALHO, F.M., 2008. New species of Hymenoptera associated with galls on . Calliandra brevipes Benth. (Fabaceae, Mimosoidea) in BrazilRevista Brasileira de Entomologia, vol. 52, no. 3, pp. 305-310. http://dx.doi.org/10.1590/S0085-56262008000300001
    » http://dx.doi.org/10.1590/S0085-56262008000300001
  • TULLER, J., PAULA, E.L., MAIA, L.F. and MORAES, R.A., 2015. Seed predation food web, nutrient availability, and impact on the seed germination of . Senegalia tenuifolia (Fabaceae)Revista de Biologia Tropical, vol. 63, no. 4, pp. 1149-1159. http://dx.doi.org/10.15517/rbt.v63i4.16855
    » http://dx.doi.org/10.15517/rbt.v63i4.16855

Publication Dates

  • Publication in this collection
    25 May 2017
  • Date of issue
    Feb 2018

History

  • Received
    09 July 2016
  • Accepted
    25 July 2016
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