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Anatomy, Histology, and Ultrastructure of Salivary Glands of the Burrower Bug, Scaptocoris castanea (Hemiptera: Cydnidae)

Part of: Micrographia Collection

Published online by Cambridge University Press:  01 October 2019

Jamile Fernanda Silva Cossolin ,
Luis Carlos Martínez ,
Monica Josene Barbosa Pereira ,
Lucia Madalena Vivan ,
Hakan Bozdoğan ,
Muhammad Fiaz  and
José Eduardo Serrão Open the ORCID record for José Eduardo Serrão [Opens in a new window]
Jamile Fernanda Silva Cossolin
Affiliation:
Department of General Biology, Federal University of Viçosa, Viçosa, Minas Gerais 36570-900, Brazil
Luis Carlos Martínez
Affiliation:
Department of General Biology, Federal University of Viçosa, Viçosa, Minas Gerais 36570-900, Brazil
Monica Josene Barbosa Pereira
Affiliation:
Department of Agronomy, State University of Mato Grosso, Tangará da Serra, Mato Grosso 78300-000, Brazil
Lucia Madalena Vivan
Affiliation:
Fundação de Apoio a Pesquisa Agropecuária de Mato Grosso, Rondonópolis, Mato Grosso 78750-360, Brazil
Hakan Bozdoğan
Affiliation:
Department of Plant and Animal Production, Vocational School of Technical Sciences, Kirsehir Ahi Evran University, 40100 Kirsehir, Turkey
Muhammad Fiaz
Affiliation:
Department of Entomology, Federal University of Viçosa, Viçosa, Minas Gerais 36570-900, Brazil
José Eduardo Serrão*
Affiliation:
Department of General Biology, Federal University of Viçosa, Viçosa, Minas Gerais 36570-900, Brazil
*
*Author for correspondence: José Eduardo Serrão, E-mail: [email protected]
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Abstract

The burrower bug Scaptocoris castanea Perty, 1830 (Hemiptera: Cydnidae) is an agricultural pest feeding on roots of several crops. The histology and ultrastructure of the salivary glands of S. castanea were described. The salivary system has a pair of principal salivary glands and a pair of accessory salivary glands. The principal salivary gland is bilobed with anterior and posterior lobes joined by a hilus where an excretory duct occurs. The accessory salivary gland is tubular with a narrow lumen that opens into the hilus near the excretory duct, suggesting that its secretion is stored in the lumen of the principal gland. The cytoplasm of the secretory cells is rich in the rough endoplasmic reticulum, secretory vesicles with different electron densities and mitochondria. At the base of the accessory gland epithelium, there were scattered cells that do not reach the gland lumen, with the cytoplasm rich in the rough endoplasmic reticulum, indicating a role in protein production. Data show that principal and accessory salivary glands of S. castanea produce proteinaceous saliva. This is the first morphological description of the S. castanea salivary system that is similar to other Hemiptera Pentatomomorpha, but with occurrence of basal cells in the accessory salivary gland.

Keywords

accessory salivary glandextra-oral digestioninsect glands anatomyphytophagous bugprincipal salivary glandsecretory cells
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 25 , Issue 6 , December 2019 , pp. 1482 - 1490
Copyright
Copyright © Microscopy Society of America 2019 

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References

Ambrose, DP & Maran, PM (2000). Polymorphic diversity in salivary and haemolymph proteins and digestive physiology of assassin bug Rhynocoris marginatus (Fab.) (Het., Reduviidae). J Appl Entomol 124, 315–317.Google Scholar
Ammar, ED (1986). Ultrastructure of the salivary glands of the planthopper, Peregrinus maidis (Ashmead) (Homoptera: Delphacidae). Int J Insect Morphol Embryol 15, 417–428.Google Scholar
Amutkan, D, Ozyurt, N, Polat, I, Suludere, Z & Candan, S (2017). Morphology and ultrastructure of the salivary glands of Piezodorus lituratus (Fabricius, 1794) (Heteroptera: Pentatomidae). Acta Zool Bulg 69, 193–200.Google Scholar
Azevedo, DO, Zanuncio, JC, Zanuncio, JS Jr., Martins, GF, Marques-Silva, S, Sossai, MF & Serrão, JE (2007). Biochemical and morphological aspects of salivary glands of the predator Brontocoris tabidus (Heteroptera: Pentatomidae). Braz Arch Biol Technol 50, 469–477.Google Scholar
Baptist, BA (1941). The morphology and physiology of the salivary glands of Hemiptera-Homoptera. Q J Microsc Sci 83, 91–139.Google Scholar
Baumann, O & Walz, B (2001). Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205, 149–214.Google Scholar
Becker, M (1996). Uma nova espécie de percevejo-castanho (Heteroptera: Cydnidae: Scaptocorinae). An Soc Entomol Bras 25, 95–102.Google Scholar
Bell, HA, Down, RD, Edwards, JP, Gatehouse, JA & Gatehouse, AMR (2005). Digestive proteolytic activity in the gut and salivary glands of the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae); effect of proteinase inhibitors. Eur J Entomol 102, 139–145.Google Scholar
Bové, JM, Renaudin, J, Saillard, C, Foissac, X & Granier, M (2003). Spiroplasma citri, a plant pathogenic molligute: Relationships with its two hosts, the plant and the leafhopper vector. Annu Rev Phytopathol 41, 483–500.Google Scholar
Boyd, DW (2003). Digestive enzymes and stylet morphology of Deraeocoris nigritulus (Uhler) (Hemiptera: Miridae) reflect adaptations for predatory habits. Ann Entomol Soc Am 96, 667–671.Google Scholar
Castellanos, N, Martínez, LC, Silva, EH, Teodoro, AV, Serrão, JE & Oliveira, EE (2017). Ultrastructural analysis of salivary glands in a phytophagous stink bug revealed the presence of unexpected muscles. PLoS One 12, e0179478.Google Scholar
Chapin, JW, Sanders, TH, Dean, LO, Hendrix, KW & Thomas, JS (2006). Effect of feeding by a burrower bug, Pangaeus bilineatus (Say) (Heteroptera: Cydnidae), on peanut flavor and oil quality. J Entomol Sci 41, 33–39.Google Scholar
Chapman, RF (2013). The Insects: Structure and Function, 5th ed. New York: Cambridge University Press.Google Scholar
Cohen, AC (1990). Feeding adaptations of some predaceous Heteroptera. Ann Entomol Soc Am 83, 1215–1223.Google Scholar
Cohen, AC (1998). Solid-to-liquid feeding: The inside story of extra-oral digestion in predaceous Heteroptera. Am Entomol 44, 103–117.Google Scholar
Dai, L, Yang, B, Wang, J, Zhang, Z, Yang, R, Zhang, T, Ren, Z & Lin, C (2019). The anatomy and ultrastructure of the digestive tract and salivary glands of Hishimonus laemllatus (Hemiptera: Cicadellidae). J Insect Sci 19, 1–9.10.1093/jisesa/iez061Google Scholar
De Castro, AA, Canevari, GC, Pikart, TG, Ribeiro, RC, Serrão, JE, Zanuncio, TV & Zanuncio, JC (2013). Salivary gland histology of the predator Supputius cincticeps (Heteroptera: Pentatomidae). Ann Entomol Soc Am 106, 273–277.Google Scholar
Dias, TKR, Wilcken, CF, Soliman, EP, Barbosa, LR, Serrão, JE & Zanuncio, JC (2014). Predation of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) by Atopozelus opsimus (Hemiptera: Reduviidae) in Brazil. Invertebr Surv J 11, 224–227.Google Scholar
Ferreira, C, Ribeiro, AF & Terra, WR (1981). Fine structure of the larval midgut of the fly Rhynchosciara and its physiological implications. J Insect Physiol 27, 559–570.Google Scholar
Fialho, MCQ, Moreira, NR, Zanuncio, JC, Ribeiro, AF, Terra, WR & Serrão, JE (2012). Prey digestion in the midgut of the predatory bug Podisus nigrispinus (Hemiptera: Pentatomidae). J Insect Physiol 58, 850–856.Google Scholar
Fialho, MCQ, Zanuncio, JC, Neves, CA, Ramalho, FS & Serrão, JE (2009). Ultrastructure of the digestive cells in the midgut of the predator Brontocoris tabidus (Heteroptera: Pentatomidae) after different feeding periods on prey and plants. Ann Entomol Soc Am 102, 119–127.Google Scholar
Ghanim, M, Rosell, RC, Campell, LR, Czosnek, H, Brown, J & Ullman, D (2001). Digestive, salivary, and reproductive organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) B type. J Morphol 248, 22–40.Google Scholar
Habibi, J, Backus, EA, Croudon, TA & Brandt, SL (2001). Effect of different host substrates on hemipteran salivary protein profiles. Entomol Exp Appl 98, 369–375.Google Scholar
Ji, R, Ye, W, Chen, H, Zeng, J, Li, H, Yu, H, Li, J & Lou, Y (2017). A salivary endo-beta-1,4-glucanase acts as an effector that enables the brown planthopper to feed on rice (1 [OPEN]). Plant Physiol 173, 1920–1932.Google Scholar
Kumar, SM & Sahayaraj, K (2012). Gross morphology and histology of head and salivary apparatus of the predatory bug Rhynocoris marginatus. J Insect Sci 12, 1–12.Google Scholar
Lacombe, D (1999). Anatomia e histologia das glândulas salivares nos Triatomíneos. Mem Inst Oswaldo Cruz 94, 557–564.Google Scholar
Li, W, Zhao, X, Yuan, W & Wu, K (2017). Activities of digestive enzymes in the omnivorous pest Apolygus lucorum (Hemiptera: Miridae). J Econ Entomol 110, 101–110.Google Scholar
Liu, X, Zhou, H, Zhao, J, Hua, H & He, Y (2016). Identification of the secreted watery saliva proteins of the rice brown planthopper, Nilaparvata lugens (Stal) by transcriptome and shotgun LC-MS/MS approach. J Insect Physiol 89, 60–69.Google Scholar
Lu, Y, Wu, KM, Jiang, YY, Xia, B, Li, P, Feng, HQ, et al. (2010). Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328, 1151–1154.Google Scholar
Marana, SR, Ribeiro, AF, Terra, WR & Ferreira, C (1997). Ultrastructure and secretory activity of Abracis flavolineata (Orthoptera: Acrididae) midguts. J Insect Physiol 43, 465–473.Google Scholar
Martínez, LC, Fialho, MCQ, Zanuncio, JC & Serrão, JE (2014). Ultrastructure and cytochemistry of salivary glands of the predator Podisus nigrispinus (Hemiptera: Pentatomidae). Protoplasma 251, 535–543.Google Scholar
Martínez, LC, Zanuncio, JC, Morais, WCC, Plata-Rueda, A, Cedeño-Loja, PE & Serrão, JE (2015). Ultrastructure of the salivary glands of the stink bug predator Podisus distinctus. Microsc Microanal 21, 1514–1522.Google Scholar
Martínez, LC, Fialho, MCQ, Barbosa, LCA, Oliveira, LL, Zanuncio, JC & Serrão, JE (2016). Stink bug predator kills prey with salivary non-proteinaceous compounds. Insect Biochem Mol Biol 68, 71–78.Google Scholar
Matias, FI, Sampaio, MV, Coelho, L & Grazia, J (2011). Occurrence of Scaptocoris castanea Perty (Hemiptera: Cydnidae) damaging Azadirachta indica (Meliaceae) seedlings in Brazil. Neotrop Entomol 40, 288–289.Google Scholar
Miles, PW & Slowiak, D (1976). The accessory salivary gland as the source of water in the saliva of Hemiptera: Heteroptera. Experientia 15, 1011–1012.Google Scholar
Nunes, PH & Camargo-Mathias, MI (2006). Ultrastructural study of the salivary glands of the sugarcane spittlebug Mahanarva fimbriolata (Stal, 1854) (Euhemiptera: Cercopidae). Micron 37, 57–66.Google Scholar
Oliveira, LJ & Malaguido, AB (2004). Fluctuation and vertical distribution of population of the brown root stink bug, Scaptocoris castanea Perty (Hemiptera: Cydnidae), within soil profile, in soybean fields in Mid Western and Southeastern Brazil. Neotrop Entomol 33, 283–291.Google Scholar
Peiffer, M & Felton, GW (2014). Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS One 9, e88483.Google Scholar
Pereira, MFA, Peres, RM & Borges, RS (2012). Population of Scaptocoris castanea Perty (Hemiptera: Cydnidae) in a crop–livestock integration system. Neotrop Entomol 41, 409–413.Google Scholar
Pires, EM, Ferreira, PSF, Guedes, RNC & Serrão, JE (2007). Morphology of the phytophagous bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae). Neotrop Entomol 36, 510–513.Google Scholar
Reis, MM, Meirelles, RM & Soares, MJ (2003). Fine structure of the salivary glands of Triatoma infestans (Hemiptera: Reduviidae). Tissue Cell 35, 393–400.Google Scholar
Reynolds, ES (1963). The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J Cell Biol 17, 208–2012.Google Scholar
Riis, L, Belotti, AC & Arias, B (2005). Bionomics and population growth statistics of Cyrtomenus bergi (Hemiptera: Cydnidae) on different host plants. Fla Entomol 88, 1–10.Google Scholar
Roma, GC, Camargo-Mathias, MI, Arrigoni, EB & Marin-Morales, MA (2003). Little cicada of sugarcane Mahanarva posticata (Homoptera: Cercopidae). A Brazilian agricultural pest. Morpho-histological study of salivary glands. Cytologia 68, 101–114.Google Scholar
Serrão, JE, Castrillon, MI, Santos-Mallet, JR, Zanuncio, JC & Gonçalves, TCM (2008). Ultrastructure of the salivary glands in Cimex hemipterus (Hemiptera: Cimicidae). J Med Entomol 45, 991–999.Google Scholar
Silva, F, Silva, J, Depieri, R & Panizzi, AR (2012). Feeding activity, salivary amylase activity, and superficial damage to soybean seed by adult Edessa meditabunda (F.) and Euschistus heros (F.) (Hemiptera: Pentatomidae). Neotrop Entomol 41, 386–390.Google Scholar
Stefanini, M, Demartino, C & Zamboni, L (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174.Google Scholar
Terra, WR & Ferreira, C (1994). Insect digestive enzymes: Properties, compartmentalization and function. Comp Biochem Physiol 109, 1–62.Google Scholar
Walker, BW & Allen, ML (2010). Expression of RNA interference of salivary polygalacturonase genes in the tarnished plant bug, Lygus lenolaris. J Insect Sci 10, 173.Google Scholar
Weintraub, PG & Beanland, L (2006). Insect vectors of phytoplasmas. Annu Rev Entomol 51, 91–111.Google Scholar
Zeng, F & Cohen, AC (2000). Comparison of a-amylase and protease activities of a zoophytophagous and two phytozoophagous Heteroptera. Comp Biochem Physiol 126, 101–106.Google Scholar
Zhang, W, Liu, B, Lu, L & Liang, G (2017). Functional analysis of two polygalacturonase genes in Apolygus lucorum associated with eliciting plant injury using RNA interference. Arch Insect Biochem Physiol 94, e21382.Google Scholar
Zhong, H, Wei, C & Zhang, Y (2013). Gross morphology and ultrastructure of salivary glands of the mute cicada Karenia caelatata Distant (Hemiptera: Cicadoidea). Micron 45, 83–91.Google Scholar
Zhong, H, Zhang, Y & Wei, C (2014). Morphology and ultrastructure of the salivary glands of the spittlebug Lepyronia coleopterata (L.) (Hemiptera: Aphrophoridae). Zool Sci 31, 213–222.Google Scholar
Zhu, YC, Yao, J & Luttrell, R (2016). Identification of genes potentially responsible for extra-oral digestion and overcoming plant defense from salivary glands of the tarnished plant bug (Hemiptera: Miridae) using cDNA sequencing. J Insect Sci 60, 1–11.Google Scholar
Zhu, YC, Zeng, F & Oppert, B (2003). Molecular cloning of trypsin-like cDNAs and comparison of proteinase activities in the salivary glands and gut of the tarsidhed plant bug Lygus lineolaris (Heteroptera: Miridae). Insect Biochem Mol Biol 33, 889–899.Google Scholar