pdf (Español (España))
FLIP
How to Cite
Albano Araújo, V. ., Bacca, T. ., & Gomes Dias, . L. . (2020). Histological structure of the treehopper male reproductive system Aethalium reticulatum (Hemipteara: Aethalionidae). Boletín Científico. Centro De Museos, 24(2), 127–137. https://doi.org/10.17151/bccm.2020.24.2.9
More Citation Formats
Authors
Vinícius Albano Araújo
Perfil Google Scholar
Tito Bacca
Lucimar Gomes Dias
Abstract
To expand knowledge about the reproductive biology of the Auchenorrhyncha hemiptera group, this paper describes the histology of the male reproductive system of Aethalio reticulatum. Scope. The treehoppers of the Aethalionidae family are terrestrial insects and predominantly phytophagous, which are configured as agricultural pests when they are in high population densities. Knowledge of the reproductive biology of these insects generates characters that can provide key information for future work related to evolution, behavior and pest control strategies. Methodology. Insect samples were collected from the Trema micrantha bush and optical microscopy techniques were used to study the reproductive anatomy of A. reticulatum. Main results. The anatomy of the internal reproductive system in males is composed of a pair of testicles, each of which contains four follicles, seminal vesicles, vas deferens, accessory glands and an ejaculatory duct. Testicular follicles have cells at different stages of development. The sperm leave the testicles in packages and break down when they reach the seminal vesicles. On each cyst on average 649 sperm were found. The accessory glands secrete different types of secretion granules. The ejaculatory duct has a cuticle that shows its ectodermal origin. Conclusion. The histology of the reproductive system of the Aethalionidae family is described for the first time, generating information that increases knowledge about its biology and that can be used in the Auchenorrhyncha system and in future control strategies for this important agricultural pest.
Keywords:
References
Adams, T.S. (2000). Morphology of the internal reproductive system of the male and female two-spotted stink bug, Perillus bioculatus (F.) (Heteroptera: Pentatomidae) and the transfer of products during mating. Invertebrate Reprod.Dev., 39: 45-53.
Araújo, V.A., Zama, U., N.,eves, C.A., Dolder, H. y Lino-Neto, J. (2005). Ultrastructural, histological and histochemical characteristics of the epithelial wall of the seminal vesicle of mature Scaptotrigona xanthotricha Moure males (Hymenoptera, Apidae, Meliponini). Braz. J.Morphol.Sci., 22: 129-137.
Araújo, V.A., Moreira, J. y Lino-Neto, J. (2009). Structure and ultrastructure of the spermatozoa of Trypoxylon (Trypargilum) albitarse Fabricius 1804 (Hymenoptera, Apoidea, Crabronidae). Micron., 40: 719-723.
Araújo, V.A., Báo, S.N., Moreira. J., Neves, C.A. y Lino-Neto J. (2010). Ultrastructural characterization of the spermatozoa of Aethalion reticulatum Linnaeus 1767 Hemiptera: Auchenorrhyncha: Aethalionidae). Micron., 41: 306-311.
Araújo, V.A., Lino-Neto, J., Ramalho, F.S., Zanuncio, J.C. y Serrão, J.E. (2011). Ultrastructure and heteromorphism of spermatozoa in five species of bugs (Pentatomidae: Heteroptera). Micron., 42: 560-671.
Araújo, V.A., Serrão, J.E., Moreira, J., Báo, S.N. y Lino-Neto, J. (2012). Ultrastructure of spermatozoa in two solitary bee species with an emphasis on synapomorphic traits shared in the Family Apidae. Microsc. Res.Techniq., 75: 74-80.
Araújo, V.A., Oliveira, A.S., Cortes, I.C.H., Viteri-D, J. y Dias, L.G., (2020). Morphology of the male reproductive tract in two species of phytophagous bugs (Pentatomidae: Heteroptera). J. Entomol. Zool. Stud., 8: 1608-1614.
Ball, D.E. y Vinson, S.B. (1984). Anatomy and histology of the male reproductive system of the fire ant, Sonelopsis invicta Buren (Hymenoptera: Formicidae). Int. J.Morphol.Embriol., 13(4): 283-294.
Bartlett, C.R., Deitz, L.L., Dimitriex, D.A., Saborn, A.F., Perkins, A.S. y Wallace, M.S. (2018). The Diversity of the True Hoppers (Hemiptera: Auchenorrhyncha). In: Foottit, R. G., Adler, P. H. Insect Biodiversity: Science and Society, II. John Wiley y Sons.
Barônio, G.J., Pires, A.C.V. y Aoki, C. (2012). Trigona branneri (Hymenoptera: Apidae) as a collector of honeydew from Aethalion reticulatum (Hemiptera: Aethalionidae) on Bauhinia forficata (Fabaceae: Caesalpinoideae) in a Brazilian savanna. Sociobiology, 59: 407-414.
Brito, B. Zama, U., Dolder, H. y Lino-Neto, J. (2010). New characteristics of the male reproductive system in the Meliponini bee, Friesellas chrottkyi (Hymenoptera: Apidae): histological and physiological development during sexual maturation. Apidologie., 41(2): 203-214.
Buschini, M.L.T. (2007). Life-history and sex allocation in Trypoxylon (syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae). J. Zool. Syst.Evol. Res., 45: 206-213.
Bushrow, E.S., Fuller, C.L., Cowan, D.P. y Byrd, C.A. (2006). Anatomy of the male reproductive system and sperm morphology in the caterpillar-hunting wasp Ancistrocerus antilope (Hymenoptera,Vespidae). Invertebr. Biol., 125(4): 354-362.
Camilo, S.S., Soares, M.A., Assis-Júnior, S.L. y Pereira, E.S. (2013). Infestação de Aethalion reticulatum (L., 1767) (Hemiptera: Aethalionidae) em plantas de Dictyoloma vandellia num Adr. Juss. (Rutaceae). MG. Biota., 5: 4-12.
Candan, S., Ozyurt, N. y Suludere, Z. (2018). Morphological and histological structure of the male reproductive system of the water strider Gerris lacustres (Linnaeus 1758) (Gerridae, Heteroptera). Microsc. Res. Tech., 1-11.
Castanhole, M.M.U., Pereira, L.L.V., Souza, H.V., Bicuda, H.E.M.C., Costa, L.A.A. y Itoyama, M.M. (2008). Heteropicnotic chromatin and nucleolar activity in meiosis and spermiogenesis of Limnogonus aduncus (Heteroptera, Gerridae): a stained nucleolar organizing region that can serve as a model for studying chromosome behavior. Genet. Mol. Res., 7(4), 1398-1407.
Castanhole, M.M.U., Pereira, L.L.V., Souza, H.V. y Itoyama, M.M. (2010). Spermatogenesis and karyotypes of three species of water striders (Gerridae, Heteroptera). Genet. Mol. Res. 9(3):1343-1356.
Chawanji, A.S., Hodgson, A.N. y Villet, M.H. (2005). Sperm morphology in four species of African platypleurine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue Cell, 37: 257-267.
Chawanji, A.S., Hodgson, A.N. y Villet, M.H. (2006). Sperm morphology in five species of cicadettine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue Cell, 38: 373-388.
Chen, P.S. (1984). The functional morphological and biochemistry of insect male acessory glands and their secretions. Annu. Rev. Entomol., 29: 233-255.
Cruz-Landim, C. y Kitajima, E.W. (1972). Ultrastructure of mature spermatozoa of corn leafhopper Dalbulus maidis Del. and W. (Homoptera, Cicadellidae). J. Submicrosc.Cytol., 4: 75-82.
Cryan, J.R. y Urban, J.M. (2012). Higher-level phylogeny of the insect order Hemiptera: is Auchenorryncha really paraphyletic? Syst. Entomol., 37, 7-21.
Dallacqua, R.P.y Cruz-Landim, C. (2003). Ultrastructure of the ducts of the reproductive tract of males of Melipona bicolor bicolor lepeletier (Hymenoptera, Apinae, Meliponini). J. Vet. Med. Series C., 32: 276-281.
Dallai, R. (2014). Overview on spermatogenesis and sperm structure of Hexapoda. Arthropod Struct. Dev., 43: 257-290.
Dallai, R., Gottardo, M. y Beutel, R.G. (2016). Structure and evolution of insect sperm: New interpretations in the age of phylogenomics. Annu. Rev.Entomol., 61: 1-23.
Dirks, T.F. y Sternburg, J.G. (1972). Male Reproductive system of three species Polistes (Hymenoptera: Vespidae). Int. J. Insect Morphol. Embryol., 1(4): 315-320.
Folliot, R. y Maillet, P. L. (1970). Ultrastructure de la spermiogenèse et du spermatozoide de divers insects Homoptères: 289-300 (en) BACCETTI, B., (ed.), Comparative Spermatology. Academic Press, New York.
Freitas, S.P.C., Santos-Mallet, J.R., Serrão, J.E., Lorosa, E.S. y Gonçalves, T.C.M. (2007). Morphometry of the testis follicles in Triatoma rubrofasciata (De Geer, 1773) (Hemiptera, Triatominae). Anim Biol. 57: 393-400.
Freitas, S.P.C., Gonçalves, T.C.M., Serrão, J.E.; Costa, J. y Santos-Mallet, J.R. (2010). Male reproductive system structure and accessory glands ultrastructure of two species of Triatoma (Hemiptera, Reduviidae, Triatominae). Micron., 41(5): 518-525.
Friedemann, K., Spangenberg, R., Yoshizawa, K. y Beutel, R.G. (2014). Evolution of attachment structures in the highly diverse Acercaria (Hexapoda). Cladistics., 30: 170-201.
Gallo, D., Nakano, O., Silveira-Neto, R.P.L., Carvalho, G.C., Batista, E., Berti-Filho, J.R.P., Parra, R.A., Zucchi, S.B., Alves, J.D., Vendramim, L.C., Marchini, J.R.S. y Omoto, C. (2002). Entomologia Agrícola. Piracicaba: FEALQ, 920p.
Gillot, C. (2003). Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annu. Rev.Entomol., 48: 163-184.
Gomes, M.O., Castanhole, M.M.U., Souza, H.V., Murakami, A.S., Firmino, T.S.S., Saran, P.S., Banho, C.A., Monteiro, L.S., Silva, J. C.P. y Itoyama, M.M. (2013). Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota. Neotrop. 13, 132-135.
Gottardo, M., Dallai, R.; Mercati, D., Horschemeyer, T. y Beutel, R.G. (2016). The evolution of insect sperm - an unusual character system in a megadiverse group. J. Zool. Syst. Evol. Res., 54: 237-256.
Grazia, J., Cavicchiolli, R.R., Wolff, V.R.S., Fernandes, J.A.M. y Takiya, D.M., (2012). Hemiptera, pp. 348-405 (en) Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B. y Casari, S. (Eds.), Os insetos do Brasil: Diversidade e taxonomia. Editora Holos, Ribeirão Preto.
Henry, T.J. (2009). Biodiversity of Heteroptera, pp. 223-268 (En) Insect biodiversity: Science and Society (Eds) Foottit, R. y Alder, P., John Wiley and Sons Oxford, UK.
Hodgson, A.N., Ridgeway, J.A. y Villet, M.H. (2016). Sperm ultrastructure and spermatodesm morphology of the spittle bug Locris transversa (Thunberg, 1822) (Hemiptera, Cercopidae). Invertebr.Reprod. Dev., 60: 87-94.
Jamieson, B.G.M., Dallai, R. y Afzelius, B.A. (1999). Insects: Their spermatozoa and phylogeny. 555 pp. Enfield. NH: Science Publishers, New Hampshire, USA.
Jiang, Z. y Qin, D.Z. (2018). Sperm ultrastructure of Euricania clara Kato (Hemiptera: Fulgoroidea: Ricaniidae). ActaEntomol. Sin., 61(2): 246-254.
Jiang, Z., Liu, J. y Qin, D. (2019). Sperm ultrastructure of Pochazia shantungensis (Chou y Lu) and Ricania speculum (Walker) (Hemiptera, Ricaniidae) with phylogenetic implications. ZooKeys., 880, 43-59.
Karakaya, G., Özyurt, N., Candan, S. y Suludere, Z. (2012). Structure of the male reproductive system in Coreus marginatus (L.) (Hemiptera: Coreidae). Turk. J.Entomol., 36(2): 193-204.
Kaur, H. y Patial, N. (2012). Internal male reproductive organs of ten species of Heteroptera (Insecta: Hemiptera). Indian J. Fund. App. Life Sci., 2(1): 317-324.
Kaur, H. y Patial, N. (2016). Internal male reproductive organs in five species of Heteroptera (Insecta: Hemiptera). Indian J. Fund. App. Life Sci., 6(3): 30-35.
Klimes, P., Borovanska, M., Plowman, N.S. y Leponce, M. (2018). How common is trophobiosis with hoppers (Hemiptera: Auchenorrhyncha) inside ant nests (Hymenoptera: Formicidae)? Novel interactions from New Guinea and a worldwide overview. Myrmecol. News., 26: 31-45.
Kubo-Irie, M., Nakazawa, M. y Mohri, H. (2003). Ultrastructure and function of long and short sperm in Cicadidae (Hemiptera). J. Insect Physiol., 49: 983-991.
Kumar, R. (1965). Aspects of the morphology of Coreoidea and their value in its higher classification. Proc. R. Soc.Queensland., 76: 27-91.
Lemos, W.P., Serrão, J.E., Ramalho, F.S., Zanuncio, J.C. y Lacerda, M.C. (2005). Effect of diet on male reproductive tract of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). Braz. J. Biol., 65(1): 91-96.
Li, H., Leavengood, J.M., Chapman, E.G., Burkhardt, D., Song, F., Jiang, P., Liu, J., Zhou, X. y Cai, W. (2017). Mitochondrial Phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs. Proc. R. Soc., 284: 2017-1223.
Lima, M.A.P., Lino-Neto, J. y Campos, L.A.O. (2006). Sexual maturation in Melipona mondury males (Apidae: Meliponini). Braz. J.Morphol. Sci., 23(3-4): 369-375.
Lino-Neto, J., Dolder, H., Mancini K., Mercati, D. y Dallai, R. (2008). The short spermatodesm of Arge pagana (Hymenoptera: Symphyta). Tissue Cell, 40: 185-193.
Marques, L.A. (1928). Cigarrinha nociva a várias espécies vegetais: biologia do membracídeo Aethalium reticulatum (L.). Instituto Biológico de Defesa Agrícola e Animal, Boletim., 6: 27p.
Moreira, J., Zama, U. y Lino-Neto, J. (2004). Release, behavior and phylogenetic significance of spermatozoa in bundles in the seminal vesicle during sexual maturation in Aculeata (Hymenoptera). Braz. J.Morphol.Sci., 21(4): 185-189.
Moreira, P.A., Araújo, V.A., Zama, U. y Lino-Neto, J. (2008). Morphology of male reproductive system in three species of Trypoxylon (Trypargilum) Richards (Hymenoptera: Crabronidae). Neotrop.Entomol., 37(4): 429-435.
Munhoz, I.L.A., Serrão, J.E.; Dias, G., Lino-Neto, J., Melo, A.L. y Araújo, V.A., 2020.- Anatomy and histology of the male reproductive tract in giant water bugs of the genus Belostoma Latreille, 1807 (Heteroptera, Belostomatidae). Int J Trop Insect Sci., 40(2): 1608-1614.
Oto, M.M., Sakakibara, A.M., Santana, M.J.S., Carvalho, A.J.A. y Coutinho, M.L. (2009). Espécies de Membracoidea (Insecta: Hemiptera) associadas a erva-de-passarinho Struthantus marginatus (Desr.) Blume (Loranthaceae) em Cruz das Almas, Bahia. Magistra., 21: 219-221.
Özyurt, N., Candan, S. y Suludere, Z. (2013). The morphology and histology of the male reproductive system in Dolycoris baccarum Linnaeus 1758 (Heteroptera: Pentatomidae) - Light and scanning electron microscope studies. Micron., 44(1): 101-106.
Özyrt, N., Candan, S. y Suludere, Z. (2014). Structure of male reproductive system and spermatogenesis of Codophila varia (Fabricius, 1787) (Heteroptera: Pentatomidae) by light and scanning electron microscopy. J.Entomol. Res. Soc., 16: 101-110.
ÖZYURT, N.; CANDAN, S. y SULUDERE, Z., 2015.- Ultrastructure of male reproductive system of Eurydema ventrale Kolenati 1846 (Heteroptera: Pentatomidae). Microsc. Res. Techq., 78: 643-653.
Parra, J.R.P. (2014). Biological Control in Brazil: An overview. Sci.Agr., 71(5): 420-428.
Pendergrast, J.G. (1957). Studies on the reproductive organs of the Heteroptera with a consideration of their bearing on classification. Trans. Ent. Soc.Lond., 109: 1-63.
Pires, E.M., Ferreira, P.S.F., Guedes, N.C. y Serrão, J.E. (2007). Morphology of the phytophagous bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae). Neotrop. Entomol., 36(4): 510-513.
Quicke, D.L.J., Ingram, S.N., Baillie, H.S. y Gaitens, P.V. (1992). Sperm structure and ultrastructure in the Hymenoptera (Insecta). Zool. Scr., 21: 381-402.
Raina, A.B.K., Kingam, T.B.G. y Giebultowicz, J.M. (1994). Mating-induced loss of Sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantra dispar. Arch. Insect Biochem. Physiol., 25: 317-327.
Rando, J.S.S. y Lima, C.B. (2010). Detecção de Aethalion reticulatum (L., 1717) (Hemiptera: Aethalionidae) em alfavaca-cravo (Ocimum gratissimum L.) e observações sobre sua ocorrência. Rev. Bras.Plantas Med., 12: 239-242.
Robertson, A. y Gibbs, A J. (1937). Spermatogenesis and fertilization in Philaenus spumarius Fallen. J. Trop. Med. Hyg., 40: 257-262. Santana, D.L.Q., Ferreira, C.A., Martins, E.G. y Silva, H.D. (2005). Ocorrência de Aethalion reticulatum (Linnaeus, 1767) (Hemiptera: Aethalionidae) em Grevillea robusta. Boletim de Pesquisa Florestal., 50: 109-115.
Schuh, R.T. y Slater, J.A. (1995). The bugs of the world (Hemiptera: Heteroptera). Classification and natural history. Cornell University Press, Ithaca, New York, USA.
Song, N., Liang, A.P. y Bu, C.P. (2012). A molecular phylogeny of Hemiptera inferred from mitochondrial genome sequences. Plos One., 7: 48-77.
Su, M., Dietrich, C.H., Zhang, Y.L. y Dai, W. (2014). Ultrastructure of the spermatozoa of Psammotettix striatus (Linnaeus) and Exitianus nanus (Distant) (Hemiptera, Auchenorrhyncha, Cicadellidae, Deltocephalinae). Arthropod Struct. Dev., 43: 559-570.
Tian, R.G., Yuan, F. y Zhang, Y.L. (2006). Male reproductive system and spermatogenesis in Homoptera (Insecta, Hemiptera). Entomotaxonomia., 28(4): 241-253.
Uceli, L.F., Pirovani, V.D., Vicente, N.M.F., Pikart, T.G., Ferreira, P.S.F. y Serrão, J.E. (2011). Morphology of the reproductive and digestive tracts of Adparaproba gabrieli (Heteroptera: Miridae). Int. J. Trop. Insect Sc., 31(4): 219-224.
Urban, J.M. y Cryan, J.R. (2007). Evolution of the planthoppers (Insecta, Hemiptera, Fulgoroidea). Mol.Phylogenet.Evol., 42: 556-572.
Weirauch, C. y Schuh, R.T. (2011). Systematics and evolution of Heteroptera: 25 years of progress. Annu. Rev. Entomol., 56: 487-510.
Wheeler, D.E. y Krutzsch, P.H. (1992). Internal reproductive system in adult males of the genus Camponotus (Hymenoptera: Formicidae: Formicinae). J.Morphol., 211: 307-317.
Zhang, Z. (2011).- Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa., 3148: 1-237.
Araújo, V.A., Zama, U., N.,eves, C.A., Dolder, H. y Lino-Neto, J. (2005). Ultrastructural, histological and histochemical characteristics of the epithelial wall of the seminal vesicle of mature Scaptotrigona xanthotricha Moure males (Hymenoptera, Apidae, Meliponini). Braz. J.Morphol.Sci., 22: 129-137.
Araújo, V.A., Moreira, J. y Lino-Neto, J. (2009). Structure and ultrastructure of the spermatozoa of Trypoxylon (Trypargilum) albitarse Fabricius 1804 (Hymenoptera, Apoidea, Crabronidae). Micron., 40: 719-723.
Araújo, V.A., Báo, S.N., Moreira. J., Neves, C.A. y Lino-Neto J. (2010). Ultrastructural characterization of the spermatozoa of Aethalion reticulatum Linnaeus 1767 Hemiptera: Auchenorrhyncha: Aethalionidae). Micron., 41: 306-311.
Araújo, V.A., Lino-Neto, J., Ramalho, F.S., Zanuncio, J.C. y Serrão, J.E. (2011). Ultrastructure and heteromorphism of spermatozoa in five species of bugs (Pentatomidae: Heteroptera). Micron., 42: 560-671.
Araújo, V.A., Serrão, J.E., Moreira, J., Báo, S.N. y Lino-Neto, J. (2012). Ultrastructure of spermatozoa in two solitary bee species with an emphasis on synapomorphic traits shared in the Family Apidae. Microsc. Res.Techniq., 75: 74-80.
Araújo, V.A., Oliveira, A.S., Cortes, I.C.H., Viteri-D, J. y Dias, L.G., (2020). Morphology of the male reproductive tract in two species of phytophagous bugs (Pentatomidae: Heteroptera). J. Entomol. Zool. Stud., 8: 1608-1614.
Ball, D.E. y Vinson, S.B. (1984). Anatomy and histology of the male reproductive system of the fire ant, Sonelopsis invicta Buren (Hymenoptera: Formicidae). Int. J.Morphol.Embriol., 13(4): 283-294.
Bartlett, C.R., Deitz, L.L., Dimitriex, D.A., Saborn, A.F., Perkins, A.S. y Wallace, M.S. (2018). The Diversity of the True Hoppers (Hemiptera: Auchenorrhyncha). In: Foottit, R. G., Adler, P. H. Insect Biodiversity: Science and Society, II. John Wiley y Sons.
Barônio, G.J., Pires, A.C.V. y Aoki, C. (2012). Trigona branneri (Hymenoptera: Apidae) as a collector of honeydew from Aethalion reticulatum (Hemiptera: Aethalionidae) on Bauhinia forficata (Fabaceae: Caesalpinoideae) in a Brazilian savanna. Sociobiology, 59: 407-414.
Brito, B. Zama, U., Dolder, H. y Lino-Neto, J. (2010). New characteristics of the male reproductive system in the Meliponini bee, Friesellas chrottkyi (Hymenoptera: Apidae): histological and physiological development during sexual maturation. Apidologie., 41(2): 203-214.
Buschini, M.L.T. (2007). Life-history and sex allocation in Trypoxylon (syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae). J. Zool. Syst.Evol. Res., 45: 206-213.
Bushrow, E.S., Fuller, C.L., Cowan, D.P. y Byrd, C.A. (2006). Anatomy of the male reproductive system and sperm morphology in the caterpillar-hunting wasp Ancistrocerus antilope (Hymenoptera,Vespidae). Invertebr. Biol., 125(4): 354-362.
Camilo, S.S., Soares, M.A., Assis-Júnior, S.L. y Pereira, E.S. (2013). Infestação de Aethalion reticulatum (L., 1767) (Hemiptera: Aethalionidae) em plantas de Dictyoloma vandellia num Adr. Juss. (Rutaceae). MG. Biota., 5: 4-12.
Candan, S., Ozyurt, N. y Suludere, Z. (2018). Morphological and histological structure of the male reproductive system of the water strider Gerris lacustres (Linnaeus 1758) (Gerridae, Heteroptera). Microsc. Res. Tech., 1-11.
Castanhole, M.M.U., Pereira, L.L.V., Souza, H.V., Bicuda, H.E.M.C., Costa, L.A.A. y Itoyama, M.M. (2008). Heteropicnotic chromatin and nucleolar activity in meiosis and spermiogenesis of Limnogonus aduncus (Heteroptera, Gerridae): a stained nucleolar organizing region that can serve as a model for studying chromosome behavior. Genet. Mol. Res., 7(4), 1398-1407.
Castanhole, M.M.U., Pereira, L.L.V., Souza, H.V. y Itoyama, M.M. (2010). Spermatogenesis and karyotypes of three species of water striders (Gerridae, Heteroptera). Genet. Mol. Res. 9(3):1343-1356.
Chawanji, A.S., Hodgson, A.N. y Villet, M.H. (2005). Sperm morphology in four species of African platypleurine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue Cell, 37: 257-267.
Chawanji, A.S., Hodgson, A.N. y Villet, M.H. (2006). Sperm morphology in five species of cicadettine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue Cell, 38: 373-388.
Chen, P.S. (1984). The functional morphological and biochemistry of insect male acessory glands and their secretions. Annu. Rev. Entomol., 29: 233-255.
Cruz-Landim, C. y Kitajima, E.W. (1972). Ultrastructure of mature spermatozoa of corn leafhopper Dalbulus maidis Del. and W. (Homoptera, Cicadellidae). J. Submicrosc.Cytol., 4: 75-82.
Cryan, J.R. y Urban, J.M. (2012). Higher-level phylogeny of the insect order Hemiptera: is Auchenorryncha really paraphyletic? Syst. Entomol., 37, 7-21.
Dallacqua, R.P.y Cruz-Landim, C. (2003). Ultrastructure of the ducts of the reproductive tract of males of Melipona bicolor bicolor lepeletier (Hymenoptera, Apinae, Meliponini). J. Vet. Med. Series C., 32: 276-281.
Dallai, R. (2014). Overview on spermatogenesis and sperm structure of Hexapoda. Arthropod Struct. Dev., 43: 257-290.
Dallai, R., Gottardo, M. y Beutel, R.G. (2016). Structure and evolution of insect sperm: New interpretations in the age of phylogenomics. Annu. Rev.Entomol., 61: 1-23.
Dirks, T.F. y Sternburg, J.G. (1972). Male Reproductive system of three species Polistes (Hymenoptera: Vespidae). Int. J. Insect Morphol. Embryol., 1(4): 315-320.
Folliot, R. y Maillet, P. L. (1970). Ultrastructure de la spermiogenèse et du spermatozoide de divers insects Homoptères: 289-300 (en) BACCETTI, B., (ed.), Comparative Spermatology. Academic Press, New York.
Freitas, S.P.C., Santos-Mallet, J.R., Serrão, J.E., Lorosa, E.S. y Gonçalves, T.C.M. (2007). Morphometry of the testis follicles in Triatoma rubrofasciata (De Geer, 1773) (Hemiptera, Triatominae). Anim Biol. 57: 393-400.
Freitas, S.P.C., Gonçalves, T.C.M., Serrão, J.E.; Costa, J. y Santos-Mallet, J.R. (2010). Male reproductive system structure and accessory glands ultrastructure of two species of Triatoma (Hemiptera, Reduviidae, Triatominae). Micron., 41(5): 518-525.
Friedemann, K., Spangenberg, R., Yoshizawa, K. y Beutel, R.G. (2014). Evolution of attachment structures in the highly diverse Acercaria (Hexapoda). Cladistics., 30: 170-201.
Gallo, D., Nakano, O., Silveira-Neto, R.P.L., Carvalho, G.C., Batista, E., Berti-Filho, J.R.P., Parra, R.A., Zucchi, S.B., Alves, J.D., Vendramim, L.C., Marchini, J.R.S. y Omoto, C. (2002). Entomologia Agrícola. Piracicaba: FEALQ, 920p.
Gillot, C. (2003). Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annu. Rev.Entomol., 48: 163-184.
Gomes, M.O., Castanhole, M.M.U., Souza, H.V., Murakami, A.S., Firmino, T.S.S., Saran, P.S., Banho, C.A., Monteiro, L.S., Silva, J. C.P. y Itoyama, M.M. (2013). Morphological aspects of the testes of 18 species of terrestrial of Heteroptera from Northwestern São Paulo (Brazil). Biota. Neotrop. 13, 132-135.
Gottardo, M., Dallai, R.; Mercati, D., Horschemeyer, T. y Beutel, R.G. (2016). The evolution of insect sperm - an unusual character system in a megadiverse group. J. Zool. Syst. Evol. Res., 54: 237-256.
Grazia, J., Cavicchiolli, R.R., Wolff, V.R.S., Fernandes, J.A.M. y Takiya, D.M., (2012). Hemiptera, pp. 348-405 (en) Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B. y Casari, S. (Eds.), Os insetos do Brasil: Diversidade e taxonomia. Editora Holos, Ribeirão Preto.
Henry, T.J. (2009). Biodiversity of Heteroptera, pp. 223-268 (En) Insect biodiversity: Science and Society (Eds) Foottit, R. y Alder, P., John Wiley and Sons Oxford, UK.
Hodgson, A.N., Ridgeway, J.A. y Villet, M.H. (2016). Sperm ultrastructure and spermatodesm morphology of the spittle bug Locris transversa (Thunberg, 1822) (Hemiptera, Cercopidae). Invertebr.Reprod. Dev., 60: 87-94.
Jamieson, B.G.M., Dallai, R. y Afzelius, B.A. (1999). Insects: Their spermatozoa and phylogeny. 555 pp. Enfield. NH: Science Publishers, New Hampshire, USA.
Jiang, Z. y Qin, D.Z. (2018). Sperm ultrastructure of Euricania clara Kato (Hemiptera: Fulgoroidea: Ricaniidae). ActaEntomol. Sin., 61(2): 246-254.
Jiang, Z., Liu, J. y Qin, D. (2019). Sperm ultrastructure of Pochazia shantungensis (Chou y Lu) and Ricania speculum (Walker) (Hemiptera, Ricaniidae) with phylogenetic implications. ZooKeys., 880, 43-59.
Karakaya, G., Özyurt, N., Candan, S. y Suludere, Z. (2012). Structure of the male reproductive system in Coreus marginatus (L.) (Hemiptera: Coreidae). Turk. J.Entomol., 36(2): 193-204.
Kaur, H. y Patial, N. (2012). Internal male reproductive organs of ten species of Heteroptera (Insecta: Hemiptera). Indian J. Fund. App. Life Sci., 2(1): 317-324.
Kaur, H. y Patial, N. (2016). Internal male reproductive organs in five species of Heteroptera (Insecta: Hemiptera). Indian J. Fund. App. Life Sci., 6(3): 30-35.
Klimes, P., Borovanska, M., Plowman, N.S. y Leponce, M. (2018). How common is trophobiosis with hoppers (Hemiptera: Auchenorrhyncha) inside ant nests (Hymenoptera: Formicidae)? Novel interactions from New Guinea and a worldwide overview. Myrmecol. News., 26: 31-45.
Kubo-Irie, M., Nakazawa, M. y Mohri, H. (2003). Ultrastructure and function of long and short sperm in Cicadidae (Hemiptera). J. Insect Physiol., 49: 983-991.
Kumar, R. (1965). Aspects of the morphology of Coreoidea and their value in its higher classification. Proc. R. Soc.Queensland., 76: 27-91.
Lemos, W.P., Serrão, J.E., Ramalho, F.S., Zanuncio, J.C. y Lacerda, M.C. (2005). Effect of diet on male reproductive tract of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). Braz. J. Biol., 65(1): 91-96.
Li, H., Leavengood, J.M., Chapman, E.G., Burkhardt, D., Song, F., Jiang, P., Liu, J., Zhou, X. y Cai, W. (2017). Mitochondrial Phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs. Proc. R. Soc., 284: 2017-1223.
Lima, M.A.P., Lino-Neto, J. y Campos, L.A.O. (2006). Sexual maturation in Melipona mondury males (Apidae: Meliponini). Braz. J.Morphol. Sci., 23(3-4): 369-375.
Lino-Neto, J., Dolder, H., Mancini K., Mercati, D. y Dallai, R. (2008). The short spermatodesm of Arge pagana (Hymenoptera: Symphyta). Tissue Cell, 40: 185-193.
Marques, L.A. (1928). Cigarrinha nociva a várias espécies vegetais: biologia do membracídeo Aethalium reticulatum (L.). Instituto Biológico de Defesa Agrícola e Animal, Boletim., 6: 27p.
Moreira, J., Zama, U. y Lino-Neto, J. (2004). Release, behavior and phylogenetic significance of spermatozoa in bundles in the seminal vesicle during sexual maturation in Aculeata (Hymenoptera). Braz. J.Morphol.Sci., 21(4): 185-189.
Moreira, P.A., Araújo, V.A., Zama, U. y Lino-Neto, J. (2008). Morphology of male reproductive system in three species of Trypoxylon (Trypargilum) Richards (Hymenoptera: Crabronidae). Neotrop.Entomol., 37(4): 429-435.
Munhoz, I.L.A., Serrão, J.E.; Dias, G., Lino-Neto, J., Melo, A.L. y Araújo, V.A., 2020.- Anatomy and histology of the male reproductive tract in giant water bugs of the genus Belostoma Latreille, 1807 (Heteroptera, Belostomatidae). Int J Trop Insect Sci., 40(2): 1608-1614.
Oto, M.M., Sakakibara, A.M., Santana, M.J.S., Carvalho, A.J.A. y Coutinho, M.L. (2009). Espécies de Membracoidea (Insecta: Hemiptera) associadas a erva-de-passarinho Struthantus marginatus (Desr.) Blume (Loranthaceae) em Cruz das Almas, Bahia. Magistra., 21: 219-221.
Özyurt, N., Candan, S. y Suludere, Z. (2013). The morphology and histology of the male reproductive system in Dolycoris baccarum Linnaeus 1758 (Heteroptera: Pentatomidae) - Light and scanning electron microscope studies. Micron., 44(1): 101-106.
Özyrt, N., Candan, S. y Suludere, Z. (2014). Structure of male reproductive system and spermatogenesis of Codophila varia (Fabricius, 1787) (Heteroptera: Pentatomidae) by light and scanning electron microscopy. J.Entomol. Res. Soc., 16: 101-110.
ÖZYURT, N.; CANDAN, S. y SULUDERE, Z., 2015.- Ultrastructure of male reproductive system of Eurydema ventrale Kolenati 1846 (Heteroptera: Pentatomidae). Microsc. Res. Techq., 78: 643-653.
Parra, J.R.P. (2014). Biological Control in Brazil: An overview. Sci.Agr., 71(5): 420-428.
Pendergrast, J.G. (1957). Studies on the reproductive organs of the Heteroptera with a consideration of their bearing on classification. Trans. Ent. Soc.Lond., 109: 1-63.
Pires, E.M., Ferreira, P.S.F., Guedes, N.C. y Serrão, J.E. (2007). Morphology of the phytophagous bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae). Neotrop. Entomol., 36(4): 510-513.
Quicke, D.L.J., Ingram, S.N., Baillie, H.S. y Gaitens, P.V. (1992). Sperm structure and ultrastructure in the Hymenoptera (Insecta). Zool. Scr., 21: 381-402.
Raina, A.B.K., Kingam, T.B.G. y Giebultowicz, J.M. (1994). Mating-induced loss of Sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantra dispar. Arch. Insect Biochem. Physiol., 25: 317-327.
Rando, J.S.S. y Lima, C.B. (2010). Detecção de Aethalion reticulatum (L., 1717) (Hemiptera: Aethalionidae) em alfavaca-cravo (Ocimum gratissimum L.) e observações sobre sua ocorrência. Rev. Bras.Plantas Med., 12: 239-242.
Robertson, A. y Gibbs, A J. (1937). Spermatogenesis and fertilization in Philaenus spumarius Fallen. J. Trop. Med. Hyg., 40: 257-262. Santana, D.L.Q., Ferreira, C.A., Martins, E.G. y Silva, H.D. (2005). Ocorrência de Aethalion reticulatum (Linnaeus, 1767) (Hemiptera: Aethalionidae) em Grevillea robusta. Boletim de Pesquisa Florestal., 50: 109-115.
Schuh, R.T. y Slater, J.A. (1995). The bugs of the world (Hemiptera: Heteroptera). Classification and natural history. Cornell University Press, Ithaca, New York, USA.
Song, N., Liang, A.P. y Bu, C.P. (2012). A molecular phylogeny of Hemiptera inferred from mitochondrial genome sequences. Plos One., 7: 48-77.
Su, M., Dietrich, C.H., Zhang, Y.L. y Dai, W. (2014). Ultrastructure of the spermatozoa of Psammotettix striatus (Linnaeus) and Exitianus nanus (Distant) (Hemiptera, Auchenorrhyncha, Cicadellidae, Deltocephalinae). Arthropod Struct. Dev., 43: 559-570.
Tian, R.G., Yuan, F. y Zhang, Y.L. (2006). Male reproductive system and spermatogenesis in Homoptera (Insecta, Hemiptera). Entomotaxonomia., 28(4): 241-253.
Uceli, L.F., Pirovani, V.D., Vicente, N.M.F., Pikart, T.G., Ferreira, P.S.F. y Serrão, J.E. (2011). Morphology of the reproductive and digestive tracts of Adparaproba gabrieli (Heteroptera: Miridae). Int. J. Trop. Insect Sc., 31(4): 219-224.
Urban, J.M. y Cryan, J.R. (2007). Evolution of the planthoppers (Insecta, Hemiptera, Fulgoroidea). Mol.Phylogenet.Evol., 42: 556-572.
Weirauch, C. y Schuh, R.T. (2011). Systematics and evolution of Heteroptera: 25 years of progress. Annu. Rev. Entomol., 56: 487-510.
Wheeler, D.E. y Krutzsch, P.H. (1992). Internal reproductive system in adult males of the genus Camponotus (Hymenoptera: Formicidae: Formicinae). J.Morphol., 211: 307-317.
Zhang, Z. (2011).- Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa., 3148: 1-237.
