Skip to main content
Log in

Ultrastructure of the midgut in Heteroptera (Hemiptera) with different feeding habits

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Heteroptera have diverse feeding habits with phytophagous, zoophagous, and haematophagous species. This dietary diversity associated with the monophyly of Heteroptera makes these insects a good object for comparative studies of the digestive tract. This work compares the ultrastructure of the middle midgut region in the phytophagous Coptosoma scutellatum (Plataspidae), Graphosoma lineatum (Pentatomidae), Kleidocerys resedae (Lygaeidae), and zoophagous Rhynocoris iracundus (Reduviidae), Nabis rugosus (Nabidae), and Himacerus apterus (Nabidae), to verify if diet affects midgut cells in phylogenetically related insects. The middle region of the midgut was used for comparison because it is the main site for digestion and absorption of the midgut. The digestive cell ultrastructure was similar in the six species, with features of secretory, absorptive, transport, storage, and excretory cells, suggesting a stronger correlation of middle digestive cell ultrastructure with the phylogeny of these species than with the different heteropteran feeding habits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alberts B, Johnson A, Lewis J, Morgan D, Raff M, Roberts K, Walter P (2014) Molecular biology of the cell, 6 edn. Garland Science, New York ISBN: 9780815344322

    Google Scholar 

  • Azevedo DO, Neves CA, Santos-Mallet JR, Goncalves TCM, Serrão JE (2009) Notes on midgut ultrastructure of the tropical bed bug Cimex hemipterus Fabricius (Hemiptera: Cimicidae). J Med Entomol 46:435–441

    Article  PubMed  Google Scholar 

  • Billingsley PF (1988) Morphometric analysis of Rhodnius prolixus Stal (Hemiptera: Reduviidae) midgut cells during blood digestion. Tissue Cell 20:291–301

    Article  CAS  PubMed  Google Scholar 

  • Billingsley PF (1990) The midgut ultrastructure of hematophagous insects. Annu Rev Entomol 35:219–248

    Article  Google Scholar 

  • Billingsley PF, Downe AER (1989) Changes in the anterior midgut cells of the adult female Rhodnius prolixus (Hemiptera: Reduviidae) after feeding. J Med Entomol 26:104–108

    Article  Google Scholar 

  • Billingsley PF, Lehane MJ (1996) Structure and ultrastucture of the insect midgut. In: Billingsley PF, Lehane MJ (eds) Biology of the insect midgut. Chapman & Hall, London, pp 3–30

    Chapter  Google Scholar 

  • Bution ML, Caetano FH (2010) The midgut of Cephalotes ants (Formicidae: Myrmicinae): ultrastructure of the epithelium and symbiotic bacteria. Micron 41:448–445

    Article  PubMed  Google Scholar 

  • Capinera JL (2008) Bugs (Hemiptera). In: Capinera JL (ed) Encyclopedia of entomology, 2 edn. Springer, Berlin, pp 591–611

    Chapter  Google Scholar 

  • Chapman RF (2013) The insects: structure and function, 5. Edn. Cambridge University Press, New York

    Google Scholar 

  • Cristofoletti PT, Ribeiro AF, Deraison C, Rahbé Y, Terra WR (2003) Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 49:11–24

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Landim C (1971) Note on granules with concetric lamination present in the larval midgut of Trigona (Scaptotrigona) portico Latr. (Hymenoptera: Apidae). Rev Bras Pesqui Med Biol 4:13–16

    Google Scholar 

  • Cruz-Landim C, Serrão JE (1997) Ultrastructure and histochemistry of the mineral concretions in the midgut of bees (Hymenoptera: Apidae). Neth J Zool 47:21–29

    Article  Google Scholar 

  • Cryan JR, Urban JM (2012) Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic? Syst Entomol 37:7–21

    Article  Google Scholar 

  • Cunha FM, Caetano FH, Wanderley-Teixeira V, Torresa JB, Teixeira AAC, Alves LC (2012) Ultra-structure and histochemistry of digestive cells of Podisus nigrispinus (Hemiptera: Pentatomidae) fed with prey reared on bt-cotton. Micron 43:245–250

    Article  PubMed  Google Scholar 

  • Davidová-Vilímová J, Štys P (1982) Bionomics of European Coptosoma species (Heteroptera, Plataspidae). Acta Univ Carol Biol 1980:463–484

    Google Scholar 

  • Ellis DS, Young C, Stamford S, Lehane MJ (1981) Notes on midgut cell nuclear coats in various tsetse species. J Med Hyg 84:209–214

    CAS  Google Scholar 

  • Fernandes KM, Neves CA, Serrão JE, Martins GF (2014) Aedes aegypti midgut remodeling during metamorphosis. Parasitol Int 63:506–512

    Article  PubMed  Google Scholar 

  • Fialho MCQ, Terra WR, Moreira NR, Zanuncio JC, Serrão JE (2013) Ultrastructure and immunolocalization of digesive enzymes in the midgut of Podisus nigrispinus (Heteroptera Pentatomidae). Arthropod Struct Dev 42:277–285

    Article  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

    Article  Google Scholar 

  • Gomes FM, Carvalho DB, Peron AC, Saito K, Miranda K, Machado EA (2012) Inorganic polyphosphates are stored in spherites within the midgut of Anticarsia gemmatalis and play a role in copper detoxification. J Insect Physiol 58:211–219

    Article  CAS  PubMed  Google Scholar 

  • Goodchild AJP (1966) Evolution of the alimentary canal in the Hemiptera. Biol Rev 41:97–140

    Article  Google Scholar 

  • Grazia J, Cavichioli RR, Wolff VRS, Fernandes JAM, Takyia DM (2012) Hemiptera Linnaeus, 1758. In: Rafael JA (ed) Insetos do Brasil: diversidade e taxonomia. Holos, Ribeirão Preto, pp 347–406

  • Guedes BAM, Zanuncio JC, Ramalho FS, Serrão JE (2007) Midgut morphology and enzymes of the obligate zoophytophagous stinkbug Brontocoris tabidus (Signoret, 1863) (Heteroptera: Pentatomidae). Pan-Pacific Ent 83(1):66–74

  • Hakim RS, Baldwin KM, Loeb M (2001) The role of stem cells in midgut growth and regeneration. In Vitro Cell Dev Biol-Anim 37:338–342

    CAS  PubMed  Google Scholar 

  • Henry TJ (2009) Biodiversity of Heteroptera. In: R Foottit, P Adler (eds) Insect biodiversity: Science and Society. Wiley-Blackwell, pp 223–263

  • Lipovsek S, Letofsky-Pabst I, Hofer F, Pabst MA (2002) Seasonal- and age-dependent changes of the structure and chemical composition of the spherites in the midgut gland of the harvestmen Gyas annulus (Opiliones). Micron 33:647–654

    Article  CAS  PubMed  Google Scholar 

  • Lipovsek S, Letofsky-Papst I, Hofer F, Pabst MA, Devetak D (2012) Application of analytical electron microscopic methods to investigate the function of spherites in the midgut of the larval antlion Euroleon nostras (Neuroptera: Myrmeolontidae). Microsc Res Tech 75:397–407

    Article  CAS  PubMed  Google Scholar 

  • Martins GF, Neves CA, Campos LAO, Serrão JE (2006) The regenerative cells during the metamorphosis in the midgut of bess. Micron 37:161–168

    Article  PubMed  Google Scholar 

  • Nardi JB, Bee CM, Miller LA (2010) Stem cells of the beetle midgut epithelium. J Insect Physiol 56:296–303

    Article  CAS  PubMed  Google Scholar 

  • Péricart J. (1987) Hémiptères Nabidae d’Europe occidentale et du Maghreb, Faune de France 71 edn. FFSSN, Paris, pp 185

  • Péricart J (1998) Hémiptères Lygaeidae Euro-Méditerranéens. In: Généralités. Systématique: Première partie vol 1, Faune de France 84A end. FFSSN, Paris, pp 468

  • Péricart J (2010) Hémiptères Pentatomoidea Euro-Méditerranéens. In: Systématique Troisième partie. Sous-families Podopinae et Asopinae vol 3, Faune de France 93 end. FFSSN, Paris, pp 291

  • Pigino G, Migliorini M, Paccagnini E, Bernini F, Leonzio C (2005) Fine structure of the midgut and Malpighian papillae in Campodea (Monocampa) quilisi Silvestri, 1932 (Hexapoda, Diplura) with special reference to the metal composition and physiological significance of midgut intracellular electron-dense granules. Tissue Cell 37:223–232

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro DO, Conte H, Gregório EA (2008) Spherites in the midgut epithelial cells of the sugarcane borer parasitized by Cotesia flavipes. Biocell 32:61–67

    Google Scholar 

  • Pradhan S (1940) The alimentary canal and pro-epithelial regeneration in Coccinella septempunctata with a comparison of carnivorous and phytophagous. Q J Microsc Sci 81:451–478

    Google Scholar 

  • Putshkov PV, Moulet P (2009) Hémiptères Reduviidae d’Europe occidentale, Faune de France 92 end. FFSSN, Paris, pp 668

  • Ribeiro AF, Ferreira C, Terra WR (1990) Morphological basis of insect digestion. In: Mellinger J (ed) Animal Nutrition and Transport Processes. Karger, Basel, pp 96–105

  • Richards PA, Richards AG (1969) Intranuclear crystals in the midgut epithelium of a flea. Ann Entomol Soc Am 62:249–250

    Article  Google Scholar 

  • Rocha LLV, Neves CA, Zanuncio JC, Serrão JE (2010) Digestive cells in the midgut of Triatoma vitticeps (Stal, 1859) in different starvation periods. C R Biologies 333:405–415

    Article  PubMed  Google Scholar 

  • Rocha LLV, Neves CA, Zanuncio JC, Serrão JE (2014) Endocrine and regenerative cells in the midgut of Chagas’ disease vector Triatoma vitticeps during different starvation periods. Folia Biol (Krakow) 62:259–267

    Article  Google Scholar 

  • Rost MM (2006) Comparative studies on regeneration of the midgut epithelium in Lepismasa saccharina L. and Thermobia domestica Packard (Insecta, Zygentoma). Ann Entomol Soc Am 99:910–916

    Article  Google Scholar 

  • Rost-Roszkowska MM (2008) Degeneration of the midgut epithelium in Allacmafusca L. (Insecta, Collembola, Symphypleona): apoptosis and necrosis. Zool Sci 25:753–759

    Article  PubMed  Google Scholar 

  • Rost-Roszkowska M, Jansta P, Vilimova J (2010b) Fine structure of the midgut epithelium in two Archaeognatha, Lepismachilis notata and Machilis hrabei (Insecta) in relation to its degeneration and regeneration. Protoplasma 247:91–101

    Article  CAS  PubMed  Google Scholar 

  • Rost-Roszkowska M, Vilimova J, Chajec Ł (2010a) Fine structure of the midgut epithelium and midgut stem cells differentiation in Atelura formicaria (Insecta, Zygentoma, Ateluridae). Zool Stud 49:10–18

    Google Scholar 

  • Rost-Roszkowska MM, Vilimova J, Włodarczyk A, Sonakowska L, Kamińska K, Kaszuba F, Marchewka A, Sadílek D (2016) Investigation of the midgut structure and ultrastructure in Cimex lectularius and Cimex pipistrelli (Hemiptera, Cimicidae). Neotropical Entomology (in press)

  • Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera): classification and natural history. Cornell University Press, New York, pp. 20–22

    Google Scholar 

  • Serrão JE, Cruz-Landim C (1995) Gut structures in adult workers of necrophorous neotropical stingless bees (hymenoptera: Apidae, Meliponinae). Entomol Gen 19:261–265

    Article  Google Scholar 

  • Serrão JE, Cruz-Landim C (1996) A comparative study of digestive cells in different midgut regions of stingless bees (Hymenoptera: Apidae: Meliponinae). J Adv Zool 17:1–6

    Google Scholar 

  • Serrão JE, Cruz-Landim C (1998) Electrophoretic analysis of the protein in the midgut of stingless bees (Apidae, Meliponinae) with a comparison of necrophagous and feeding pollen workers. J Adv Zool 19(1):33–36

    Google Scholar 

  • Serrão JE, Cruz-Landim C (2000) Ultrastrucuture of the midgut epithelium of Meliponinae larvae with different developmental stages and diets (Hymenoptera, Apidae). J Apic Res 39:9–17

    Article  Google Scholar 

  • Shanbhag S, Tripathi S (2009) Review: epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J Exp Biol 212:1731–1744

    Article  CAS  PubMed  Google Scholar 

  • Silva CP, Silva JR, Vasconcelos FF, Petretski MDA, DaMatta RA, Ribeiro AF, Terra WR (2004) Occurrence of midgut perimicrovillar membranes in paraneopteran insect orders with comments on their function and evolutionary significance. Arthropod Struct Dev 33(2):139–148

    Article  PubMed  Google Scholar 

  • Silva CPR, Ribeiro AF, Gulbenkian S, Terra WR (1995) Organization, origin and function of the outer microvillar (perimicrovillar) membranes of Dysdercus peruvianus (Hemiptera) midgut cells. J Insect Physiol 41:1093–1103

    Article  CAS  Google Scholar 

  • Sosinka A, Rost-Roszkowska MM, Vilimova J, Tajovský K, Kszuk-Jendrysik M, Chajec Ł, Sonakowska L, Kamińska K, Hyra M, Poprawa I (2014) The ultrastructure of the midgut epithelium in millipedes (Myriapoda, Diplopoda). Arthropod Struct Dev 43:477–492

    Article  CAS  PubMed  Google Scholar 

  • Teixeira AD, Fialho MCQ, Zanuncio JC, Ramalho FS, Serrão JE (2013) Degeneration and cell regeneration in the midgut of Podisus nigrispinus (Heteroptera: Pentatomidae) during post-embryonic development. Arthropod Struct Dev 42(3):237–246

    Article  PubMed  Google Scholar 

  • Terra WR (1988) Physiology and biochemistry of insect digestion: an evolutionary perspective. Braz J Med Biol Res 21:675–734

    CAS  PubMed  Google Scholar 

  • Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200

    Article  Google Scholar 

  • Terra WR, Ferreira C (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Phys B 109:1–62

    Article  Google Scholar 

  • Zhuang Z, Linser PJ, Harvey WR (1999) Antibody to H(+) V-ATPase subunit E colocalizes with portasomes in alkaline larval midgut of a freshwater mosquito (Aedes aegypti). J Exp Biol 202:2449–2460

    CAS  PubMed  Google Scholar 

  • Zimmermann B, Dames P, Walz B, Baumann O (2003) Distribution and serotonin-induced activation of vacuolar-type H+-ATPase in the salivary glands of the blowfly Calliphora vicina. J Exp Biol 206:1867–1876. doi:10.1242/jeb.00376

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Brazilian funding agencies: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), the Financiadora de Estudos e Projetos FINEP, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG). We would like to also thank the Microscopy and Microanalysis Center of UFV by the use of equipment and technical assistance and Karen Salazar Niño for the production of digestive cells illustrations. We are grateful to Magdalena Rosińska (University of Silesia, Poland) for her technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Eduardo Serrão.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with animals and human participants performed by any of the authors.

Additional information

Handling Editor: Margit Pavelka

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, H.P., Rost-Roszkowska, M., Vilimova, J. et al. Ultrastructure of the midgut in Heteroptera (Hemiptera) with different feeding habits. Protoplasma 254, 1743–1753 (2017). https://doi.org/10.1007/s00709-016-1051-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-016-1051-2

Keywords

Navigation