Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-19T04:53:30.894Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructure of the Salivary Glands of the Stink Bug Predator Podisus distinctus

Published online by Cambridge University Press:  25 November 2015

Luis C. Martínez ,
José C. Zanuncio ,
Wagner C.C. Morais ,
Angelica Plata-Rueda ,
Pedro E. Cedeño-Loja  and
José E. Serrão
Luis C. Martínez
Affiliation:
Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
José C. Zanuncio
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
Wagner C.C. Morais
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
Angelica Plata-Rueda
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
Pedro E. Cedeño-Loja
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
José E. Serrão*
Affiliation:
Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-000, Brasil
*
*Corresponding author. jeserrao@ufv.br
Get access

Abstract

Podisus distinctus (Hemiptera: Pentatomidae) is a zoophytophagous insect with significant potential for use as a biological control agent in agriculture and forestry because their nymphs and adults actively prey on diverse insect species. The saliva of this insect possesses active substances that cause paralysis and death of the prey. As the first step in identifying compounds of P. distinctus saliva, this study describes the ultrastructure of the salivary glands of this predator. The salivary system of P. distinctus possesses a pair of main salivary glands with a short anterior lobe, a long posterior lobe, and a pair of tubular accessory glands. The main salivary gland of P. distinctus has no associated muscles, suggesting that the saliva-release mechanism occurs with the help of certain thorax muscles. The main salivary gland epithelium has a single layer of cells (varying from cubical to columnar) with cytoplasm rich in rough endoplasmic reticulum, spherical granules of different sizes, a nucleus with a predominance of decondensed chromatin, and nucleolus. The apical cell region has a few short microvilli and the basal region has plasma membrane infoldings. The epithelium of the accessory salivary glands possesses a single-layered epithelium of cubic cells delimiting a narrow lumen. The apical cell region has a high density of microvilli and pleomorphic mitochondria, whereas the central cell region is rich in rough endoplasmic reticulum with a well-developed nucleus and decondensed chromatin. The basal cell region is characterized by the presence of several basal plasma membrane infoldings associated with mitochondria and numerous openings to the hemocoel forming large channels. The ultrastructural characteristics suggest that the main salivary glands and accessory salivary glands play a vital role in protein synthesis for saliva production and that the accessory glands are involved in transport of materials of the hemolymph.

Keywords

salivaextra-oral digestionsalivary glandsecretory cellszoophytophagy
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 21 , Issue 6 , December 2015 , pp. 1514 - 1522
Copyright
© Microscopy Society of America 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Azevedo, D.O., Zanuncio, J.C., Zanuncio, J.J.S., Martins, G.F., Marques-Silva, S., Sossai, M.F. & Serrão, J.E. (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, B.A. (1941). The morphology and physiology of the salivary glands of Hemiptera-Heteroptera. Q J Microsc Sci 83, 91–139.Google Scholar
Cohen, A.C. (1990). Feeding adaptations of some predaceous Heteroptera. Ann Entomol Soc Am 83, 1215–1223.Google Scholar
Cohen, A.C. (1995). Extra-oral digestion in predaceous terrestrial Arthropoda. Annu Rev Entomol 40, 85–103.CrossRefGoogle Scholar
Cohen, A.C. (1998). Solid-to-liquid feeding: The inside story of extra-oral digestion in predaceous Heteroptera. Am Entomol 44, 103–117.Google Scholar
Coll, M. & Guershon, M. (2002). Omnivory in terrestrial arthropods: Mixing plant and prey diets. Annu Rev Entomol 47, 267–297.Google Scholar
De Castro, A.A., Canevari, G.C., Pikart, T.G., Ribeiro, R.C., Serrão, J.E., Zanuncio, T.V. & Zanuncio, J.C. (2013). Salivary gland histology of the predator Supputius cincticeps (Heteroptera: Pentatomidae). Ann Entomol Soc Am 106, 273–277.Google Scholar
De Clercq, P. (2002). Dark clouds and their silver linings: Exotic generalista predators in augmentative biological control. Neotrop Entomol 31, 169–176.CrossRefGoogle Scholar
Del Bene, G., Dallai, R. & Marchini, D. (1991). Ultrastructure of the midgut and the adhering tubular salivary gland of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Int J Insect Morphol Embryol 20, 15–24.Google Scholar
Eubanks, M. & Denno, R.F. (1999). The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80, 1253–1266.CrossRefGoogle Scholar
Eubanks, M.D., Styrsky, J.D. & Denno, R.F. (2003). The evolution of omnivory in heteropteran insects. Ecology 84, 2549–2556.Google Scholar
Fialho, M.C.Q., Terra, W.R., Moreira, N.R., Zancunico, J.C. & Serrão, J.E. (2013). Ultrastructure and immunolocalization of digestive enzymes in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae). Arthropod Struct Dev 42, 277–285.Google Scholar
Fialho, M.C.Q., Zanuncio, J.C., Neves, C.A., Ramalho, F.S. & Serrão, J.E. (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
Fialho, M.C.Q., Zanuncio, J.C., Neves, C.A., Ramalho, F.S. & Serrão, J.E. (2012). Prey digestion in the midgut of the predatory bug Podisus nigrispinus (Hemiptera: Pentatomidae). J Insect Physiol 58, 850–856.Google Scholar
Ghanim, M., Rosell, R.C., Campbell, L.R., Czosnek, H., Brown, J.K. & Ullman, D.E. (2001). Digestive, salivary, and reproductive organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) B type. J Morphol 248, 22–40.Google Scholar
Guedes, B.A.M., Zanuncio, J.C., Ramalho, F.S. & Serrão, J.E. (2007). Midgut morphology and enzymes of the obligate zoophytophagous stinkbug Brontocoris tabidus (Signoret, 1863) (Heteroptera: Pentatomidae). Pan-Pac Entomol 83, 66–74.Google Scholar
Jesus, F.G., Boica, A.L., Alves, G.C.S. & Zanuncio, J.C. (2014). Behavior, development, and predation of Podisus nigrispinus (Hemiptera: Pentatomidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) fed transgenic and conventional cotton cultivars. Ann Entomol Soc Am 107, 601–606.Google Scholar
Lacerda, M.C., Ferreira, A.M.R.M., Zanuncio, T.V., Zanuncio, J.C., Bernardio, A.S. & Espindula, M.C. (2004). Development and reproduction of Podisus distinctus (Heteroptera: Pentatomidae) fed on larva of Bombyx mori (Lepidoptera: Bombycidae). Braz J Biol 64, 237–242.CrossRefGoogle ScholarPubMed
Lemos, W.P., Ramalho, F.S., Serrão, J.E. & Zanuncio, J.C. (2003). Effects of diet on development of Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae), a predator of the cotton leafworm. J Appl Entomol 127, 389–395.Google Scholar
Lemos, W.P., Ramalho, F.S., Serrão, J.E. & Zanuncio, J.C. (2005). Morphology of female reproductive tract of the predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) fed on different diets. Braz Arch Biol Technol 48, 129–138.Google Scholar
Martínez, L.C., Fialho, M.C.Q., Zanuncio, J.C. & Serrão, J.E. (2014). Ultrastructure and cytochemistry of salivary glands of the predator Podisus nigrispinus (Hemiptera: Pentatomidae). Protoplasma 251, 535–543.Google Scholar
Matos Neto, F.C., Oliveira, H.N., Zanuncio, J.C. & Holtz, A.M. (2004). Ganância de peso del depredador Podisus distinctus (Heteroptera: Pentatomidae) en combinaciones de las presas Tenebrio molitor (Coleoptera: Tenebrionidae) e Musca domestica (Diptera: Muscidae). Rev Biol Trop 52, 1–8.Google Scholar
Memmott, J., Martinez, N.D. & Cohen, J.E. (2000). Predators, parasitoids and pathogens: Species richness, trophic generality and body sizes in a natural food web. J Anim Ecol 69, 1–15.CrossRefGoogle Scholar
Miles, P.W. (1972). The saliva of Hemiptera. Adv Insect Physiol 9, 183–255.CrossRefGoogle Scholar
Miles, P.W. & Slowiak, D. (1976). The accessory salivary gland as the source of water in the saliva of Hemiptera: Heteroptera. Experientia 15, 1011–1012.Google Scholar
Mohaghegh, J., De Clercq, P. & Tirry, L. (2001). Functional response of the predators Podisus maculiventris (Say) and Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) to the beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae): Effect of temperature. J Appl Entomol 125, 131–134.Google Scholar
Nunes, P.H. & Camargo-Mathias, M.I. (2006). Ultrastructural study of the salivary glands of the sugarcane spittlebug Mahanarva fimbriolata (Stal, 1854) (Euhemiptera: Cercopidae). Micron 37, 57–66.Google Scholar
Oliveira, J.A., Oliveira, M.G.A., Guedes, R.N.C. & Soares, M.J. (2006). Morphology and preliminary enzyme characterization of the salivary glands from the predatory bug Podisus nigrispinus (Heteroptera: Pentatomidae). Bull Entomol Res 96, 251–258.Google Scholar
Pires, E.M., Azevedo, D.O., Lima, E.R., Pelúzio, R.J.E., Serrão, J.E. & Zanuncio, J.C. (2009). Desenvolvimento, reprodução e performance predatória do percevejo zoofitófago Podisus distinctus (Hemiptera: Pentatomidae) alimentado com larvas de Musca domestica (Diptera: Muscidae) imobilizadas ou soltas. Rev Bras Biocienc 7, 280–284.Google Scholar
Pires, E.M., Ferreira, P.S.F., Guedes, R.N.C. & Serrao, J.E. (2007). Morphology of the phytophagous bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae). Neotrop Entomol 36, 510–513.Google Scholar
Reis, M.M.M., Meirelles, R.M. & Soares, M.J. (2003). Fine structure of the salivary glands of Triatoma infestans (Hemiptera, Reduviidae). Tissue Cell 35, 393–400.Google Scholar
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208–212.Google Scholar
Richter, M.R. (2000). Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu Rev Entomol 45, 121–150.Google Scholar
Roma, G.C., Camargo-Mathias, M.I., Arrigoni, E.B. & Marin-Morales, M.A. (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
Sá, V.G.M., Zanuncio, J.C., Soares, M.A., Rosa, C.S. & Serrão, J.E. (2013). Morphology and postdepositional dynamics of eggs of the predator Podisus distinctus (Stål) (Heteroptera: Pentatomidae: Asopinae). Zootaxa 3641, 282–288.Google Scholar
Sais, T.C., Moraes, R.M., Ribolla, P.E., Bianchi, A.G., Marinotti, O. & Bijovsky, A.T. (2003). Morphological aspects of Culex quinquefasciatus salivary glands. Arthropod Struct Dev 32, 219–226.Google Scholar
Santos, G.P., Zanuncio, T.V., Ribeiro, G.T., Silva, E.P. & Zanuncio, J.C. (2004). Influência da temperatura no desenvolvimento ninfal de Podisus distinctus (Dallas) (Heteroptera: Pentatomidae). Rev Cerne 10, 213–221.Google Scholar
Serrão, J.E., Castrillon, M.I., Santos-Mallet, J.R., Zanuncio, J.C. & Gonçalves, T.C. (2008). Ultrastructure of the salivary gland in Cimex hemipterus (Hemiptera: Cimicidae). J Med Entomol 45, 991–999.CrossRefGoogle ScholarPubMed
Serrão, J.E. & Cruz-Landim, C. (1995). Gut structures in adult workers of necrophorous Neotropical stingless bees (Hymenoptera: Apidae, Meliponinae). Ent Gen 19, 261–265.Google Scholar
Serrão, J.E. & Cruz-Landim, C. (2000). Ultrastructure of the midgut epithelium of Meliponinae larvae with different developmental stages and diets. J Apicult Res 39, 9–17.Google Scholar
Silva, C.P., Ribeiro, A.F., Gulbenkian, S. & Terra, W.R. (1995). Organization, origin and function of the outer microvillar (perimicrovillar) membranes of Dysdercus peruvianus (Hemiptera) midgut cells. J Insect Physiol 41, 1093–1103.Google Scholar
Stefanini, M., De Martino, C. & Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174.Google Scholar
Swart, C.C. & Felgenhauer, B.E. (2003). Structure and function of the mouthparts and salivary gland complex of the giant waterbug, Belostoma lutarium (Stall) (Hemiptera: Belostomatidae). Ann Entomol Soc Am 96, 870–882.Google Scholar
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002). Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47, 561–594.Google Scholar
Terra, W.R. & Ferreira, C. (1994). Insect digestive enzymes: Properties, compartmentalization and function. Comp Biochem Physiol B 109, 1–62.CrossRefGoogle Scholar
Torres, J.B., Barros, E.M., Coelho, R.R. & Pimentel, R.M.M. (2010). Zoophytophagous pentatomids feeding on plants and implications for biological control. Arthropod Plant Interact 4, 219–227.Google Scholar
Torres, J.B. & Boyd, D.W. (2009). Zoophytophagy in predatory Hemiptera. Braz Arch Biol Technol 52, 1199–1208.CrossRefGoogle Scholar
Uceli, L.F., Pirovani, V.D., Vicente, N.M.F., Pikart, T.G., Ferreira, P.S.F. & Serrão, J.E. (2011). Morphology of the reproductive and digestive tracts of Adparaproba gabrieli (Hemiptera: Miridae). Int J Trop Insect Sci 31, 219–224.Google Scholar
Zanuncio, J.C., Alves, J.B., Zanuncio, T.V. & García, J.L. (1994). Hemipterous predators of eucalypt defoliator caterpillars. Forest Ecol Manag 65, 65–73.Google Scholar
Zanuncio, J.C., Jusselino-Filho, P., Ribeiro, R.C., Castro, A.A., Zanuncio, T.V. & Serrão, J.E. (2013). Fertility and life expectancy of a predatory stinkbug to sublethal doses of a pyrethroid. Bull Environ Contam Toxicol 90, 39–45.Google Scholar
Zanuncio, J.C., Jusselino-Filho, P., Ribeiro, R.C., Zanuncio, T.V., Ramalho, F.S. & Serrão, J.E. (2011). Hormetic responses of a stinkbug predator to sublethal doses of pyrethroid. Bull Environ Contam Toxicol 87, 608–614.Google Scholar
Zanuncio, J.C., Silva, C.A.D., Lima, E.R., Pereira, F.F., Ramalho, F.S. & Serrão, J.E. (2008). Predation rate of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae with and without defense by Podisus nigrispinus (Heteroptera: Pentatomidae). Braz Arch Biol Technol 51, 121–125.Google Scholar
Zeng, F. & Cohen, A.C. (2000). Comparison of a-amylase and protease activities of a zoophytophagous and two phytozoophagous Heteroptera. Comp Biochem Physiol A 126, 101–106.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.CrossRefGoogle ScholarPubMed