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Parasitology Research

, Volume 112, Issue 1, pp 415–425 | Cite as

Morphology of the midgut of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) adult ticks in different feeding stages

  • R. N. Remedio
  • B. R. Sampieri
  • M. C. R. Vendramini
  • N. M. Souza
  • L. A. Anholeto
  • T. A. G. B. Denardo
  • M. I. Camargo-Mathias
Original Paper

Abstract

The intestinal epithelial cells of ticks are fundamental for their full feeding and reproductive success, besides being considered important sites for the development of pathogens. Rhipicephalus sanguineus ticks are known for their great medical and veterinary importance, and for this reason, the knowledge of their intestinal morphology may provide relevant subsidies for the control of these animals, either by direct acaricidal action over these cells or by the production of vaccines. Therefore, this study aimed to describe the midgut morphology of male and female R. sanguineus ticks in different feeding stages, by means of histological analysis. Significant differences were observed between the genders, and such alterations may refer mainly to the distinct demands for nutrients, much higher in females, which need to develop and carry out the egg-laying process. In general, the midgut is coated by a thin muscle layer and presents a pseudostratified epithelium, in which two basic types of cells can be observed, connected to a basal membrane—generative or stem and digestive cells. The latter was classified as follows: residual, deriving from the phase anterior to ecdysis; pinocytic, with vesicles containing liquid or pre-digested components of blood; phagocytic, with entire cells or remnants of nuclear material inside cytoplasmic vesicles; and mature, free in the lumen. Digestion is presumably intracellular and asynchronous and corresponds to a process which starts with the differentiation of generative cells into pinocytic digestive cells, which subsequently start to phagocytize intact blood cells and finally detach from the epithelium, being eliminated with feces.

Keywords

Generative Cell Visceral Leishmaniasis Tick Species Residual Body Digestive Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their financial support.

Conflict of interest

None.

References

  1. Agbede RIS, Kemp DH (1985) Digestion in the cattle-tick Boophilus microplus: light microscope study of the gut cells in nymphs and females. Int J Parasitol 15(2):147–157PubMedCrossRefGoogle Scholar
  2. Agbede RIS, Kemp DH (1987) Ultrastructure of secretory cells in the gut of the cattle-tick Boophilus microplus. Int J Parasitol 17(6):1089–1098PubMedCrossRefGoogle Scholar
  3. Agyei AD, Runham NW (1995) Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipicephalus appendiculatus during digestion of the blood meal. Int J Parasitol 25(1):55–62PubMedCrossRefGoogle Scholar
  4. Arnosti A, Brienza PD, Furquim KCS, Chierice GO, Bechara GH, Calligaris IB, Camargo-Mathias MI (2010a) Effects of ricinoleic acid esters form castor oil of Ricinus communis on the vitellogenesis of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) ticks. Exp Parasitol 27(2):575–580Google Scholar
  5. Arnosti A, Brienza PD, Furquim KCS, Chierice GO, Neto SC, Bechara GH, Sampieri BR, Camargo-Mathias MI (2010b) Effects of Ricinus communis oil esters on salivary glands of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 27:569–574Google Scholar
  6. Bechara GH, Szabó MPJ, Ferreira BR, Garcia MV (1995) Rhipicephalus sanguineus tick in Brazil: feeding and reproductive aspects under laboratorial conditions. Braz J Vet Parasitol 4(2):61–66Google Scholar
  7. Blagburn BL, Dryden MW (2009) Biology, treatment and control of flea and tick infestations. Vet Clin Small Anim 39:1173–1200CrossRefGoogle Scholar
  8. Caperucci D, Bechara GH, Camargo-Mathias MI (2009) Histopathology and ultrastructure features of the midgut of adult females of the tick Amblyomma cajennense Fabricius, 1787 (Acari: Ixodidae) in various feeding stages and submitted to three infestations. Ultrastruct Pathol 33:249–259PubMedCrossRefGoogle Scholar
  9. Caperucci D, Bechara GH, Camargo-Mathias MI (2010) Ultrastructure features of the midgut of the female adult Amblyomma cajennense ticks Fabricius, 1787 (Acari: Ixodidae) in several feeding stages and subjected to three infestations. Micron 41:710–721PubMedCrossRefGoogle Scholar
  10. Coons LB, Alberti G (1999) The acari-ticks. In: Harrison FW, Foelix R (eds) Microscopic anatomy of invertebrates. Chelicerate Arthropoda, Wiley, NewYork, pp 267–514Google Scholar
  11. Coutinho MTZ, Bueno LL, Sterzik A, Fujiwara RT, Botelho JR, Maria M, Genaro O, Linardi PM (2005) Participation of Rhipicephalus sanguineus (Acari: Ixodidae) in the epidemiology of canine visceral leishmaniasis. Vet Parasitol 128:149–155PubMedCrossRefGoogle Scholar
  12. Cunha NC, Fonseca AH, Rezende J, Rozental T, Favacho ARM, Barreira JD, Massard CL (2009) Lemos ERS (2009) First identification of natural infection of Rickettsia rickettsii in the Rhipicephalus sanguineus tick, in the state of Rio de Janeiro. Pesq Vet Bras 29(2):105–108CrossRefGoogle Scholar
  13. Dantas-Torres F (2010) Biology and ecology of the Brown dog tick, Rhipicephalus sanguineus. Parasite Vector 3(26):1–11Google Scholar
  14. Dantas-Torres F, Figueiredo LA, Brandão-Filho SP (2006) Rhipicephalus sanguineus (Acari: Ixodidae), the brown dog tick, parasitizing humans in Brazil. Rev Soc Bras Med Tro 39(1):64–67CrossRefGoogle Scholar
  15. Dantas-Torres F, Lorusso V, Testini G, Paiva-Cavalcanti M, Figueiredo LA, Stanneck D, Mencke N, Brandão-Filho SP, Alves LC, Otranto D (2010) Detection of Leishmania infantum in Rhipicephalus sanguineus tick from Brazil and Italy. Parasitol Res 106:857–860PubMedCrossRefGoogle Scholar
  16. Denardi SE, Bechara GH, Oliveira PR, Camargo-Mathias MI (2010) Azadirachta indica A. Juss (neem) induced morphological changes on oocytes of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick females. Exp Parasitol 126:462–470PubMedCrossRefGoogle Scholar
  17. Junqueira LCU, Junqueira LMMS (1983) Técnicas Básicas de Citologia e Histologia. Editora Santos, São PauloGoogle Scholar
  18. Koh K, Mori T, Shiraishi S, Uchida TA (1991) Ultrastructural changes of the midgut epithelial cells in feeding and moulting nymphs of the tick Haemaphysalis longicornis. Int J Parasitol 21(1):23–36PubMedCrossRefGoogle Scholar
  19. Kongsuwan K, Josh P, Zhu Y, Pearson R, Gough J, Colgrave ML (2010) Exploring the midgut proteome of partially fed female cattle tick Rhipicephalus (Boophilus) microplus. J Insect Physiol 56:212–226PubMedCrossRefGoogle Scholar
  20. Lara FA, Lins U, Paiva-Silva G, Almeida IC, Braga CM, Miguens FC, Oliveira PL, Dansa-Petretski M (2003) A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. J Exp Biol 206:1707–1715PubMedCrossRefGoogle Scholar
  21. Matsuo T, Sato M, Inoue N, Yokoyama N, Taylor D, Fujisaki K (2003) Morphological studies on the extracellular structure of the midgut of a tick, Haemaphysalis longicornis (Acari: Ixodidae). Parasitol Res 90:243–248PubMedGoogle Scholar
  22. Oliveira PR, Bechara GH, Denardi SE, Nunes ET, Camargo-Mathias MI (2005) Morphological characterization of the ovary and oocytes vitellogenesis of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 110:146–156PubMedCrossRefGoogle Scholar
  23. Paz GF, Labruna MB, Leite RC (2008) Ritmo de queda de Rhipicephalus sanguineus (Acari: Ixodidae) de cães artificialmente infestados. Rev Bras Parasitol Vet 17(3):139PubMedGoogle Scholar
  24. Roma GC, Nunes PH, Remedio RN, Camargo-Mathias MI (2012a) Synganglion histology in different stages of Rhipicephalus sanguineus ticks (Acari: Ixodidae). Parasitol Res 110:2455–2463PubMedCrossRefGoogle Scholar
  25. Roma GC, Nunes PH, Oliveira PR, Remedio RN, Bechara GH, Camargo-Mathias MI (2012b) Central nervous system of Rhipicephalus sanguineus ticks (Acari: Ixodidae): an ultrastructural study. Parasitol Res 111:1277–1285PubMedCrossRefGoogle Scholar
  26. Vendramini MCR, Camargo-Mathias MI, Faria AU, Bechara GH, Oliveira PR, Roma GC (2012) Cytotoxic effects of andiroba oil (Carapa guianensis) in reproductive system of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females. Parasitol Res (in press)Google Scholar
  27. Walker AR, Fletcher JD (1987) Histology of digestion in nymphs of Rhipicephalus appendiculatus fed on rabbits and cattle naïve and resistant to the ticks. Int J Parasitol 17(8):1393–1411PubMedCrossRefGoogle Scholar
  28. Wigglesworth VB (1954) The fate of haemoglobin in Rhodnius prolixus (Hemiptera) and other blood-sucking arthropods. P R Soc London 131:313–339CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • R. N. Remedio
    • 1
  • B. R. Sampieri
    • 1
  • M. C. R. Vendramini
    • 1
  • N. M. Souza
    • 1
  • L. A. Anholeto
    • 1
  • T. A. G. B. Denardo
    • 1
  • M. I. Camargo-Mathias
    • 1
  1. 1.Laboratório de HistologiaUniversidade Estadual Paulista “Júlio de Mesquita Filho”Jardim Bela Vista, Rio ClaroBrazil

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