Parasitology Research

, Volume 111, Issue 5, pp 1885–1894 | Cite as

Cytotoxic effects of andiroba oil (Carapa guianensis) in reproductive system of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females

  • Maria Cláudia Ramalho Vendramini
  • Maria Izabel Camargo-Mathias
  • Adriano Uemura de Faria
  • Gervásio Henrique Bechara
  • Patrícia Rosa de Oliveira
  • Gislaine Cristina RomaEmail author
Original Paper


The present study performed an analysis about the effects of andiroba seed oil (Carapa guianensis) in the ovary of Rhipicephalus sanguineus semi-engorged females; once, there are few studies about the action of natural products on the reproductive system, a vital organ for the biological success of this animal group. The results showed that andiroba oil is a potent natural agent which causes significant structural changes in the oocytes, such as the emergence of large vacuolated cytoplasmic regions, reduction in the number of yolk granules, changes in the shape of the cells, as well as impairment of genetic material. In addition, the ovary epithelium showed severe morphological changes, such as extreme structural disorganization, with highly vacuolated cells and picnotic nuclei, forming an amorphous mass. This study showed also that oocytes (mainly in the initial stages of development) and the ovary epithelium of R. sanguineus females subjected to different concentrations of andiroba oil presented morphological changes which became more numerous and intense as the concentration of the product increased. Based on the results, it can be inferred that although the defense mechanisms are developed by oocytes to recover the cellular integrity (presence of autophagic vacuoles), these cells are not able to revert the damage caused by this product. Thus, it can be concluded that although the damages caused to the oocytes by andiroba oil are comparatively less severe than the ones caused by synthetic acaricides, this product can be considered a potent natural agent that reduce and/or prevent the reproduction of R. sanguineus females, with the advantage of not causing environmental impact such as synthetic chemical acaricides.


Yolk Granule Ovary Epithelium Synthetic Acaricide Picnotic Nucleus Severe Morphological Change 
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.



The authors are grateful to Fundação de Amparo à Pesquisa do Estado de São Paulo (grant nos. 2011/07938-9, 2011/10427-6, 2010/51942-8, and 2011/06865-8) for the financial support.


  1. Arnosti A, Brienza PD, Furquim KCS, Chierice G, Bechara GH, Calligaris IB, Camargo-Mathias MI (2010) Effects of ricinoleic acid esters from castor oil Ricinus communis on the vitellogenesis of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick. Exp Parasitol 127:575–580PubMedCrossRefGoogle Scholar
  2. 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 4:61–66Google Scholar
  3. Briton LP, Oliver JH (1971) Fine structure of oogonial and oocytes development in Demacentor andersoni Stile (Acari: Ixodidae). J Parasitol 57:720–747CrossRefGoogle Scholar
  4. Chagas ACS, Leite RC, Furlong J, Prates HT, Passos WM (2003) Sensibility of Boophilus microplus tick to solvents. Cienc Rural 33:109–114CrossRefGoogle Scholar
  5. Costa-Silva JH, Lima CR, Araújo AV, Fraga MCCA, Ribeiro e Ribeiro A, Arruda AC, Lafayette SSL, Wanderley AG (2008) Acute and subacute toxicity of the Carapa guianensis Aublet (Meliaceae) seed oil. J Ethnopharmacol 116:495–500PubMedCrossRefGoogle Scholar
  6. Coutinho MTZ, Bueno LL, Sterzik A, Fujiwara RT, Botelho JR, De Maria M, Genaro O, Linardi PM (2005) Participation of Rhipicephalus sanguineus (Acari: Ixodidae) in the epidemiology of canine leishmaniasis. Vet Parasitol 128:149–155PubMedCrossRefGoogle Scholar
  7. Cui X, Mao S, Liu M, Yuan H, Du Y (2008) Mechanism of surfactant micelle formation. Langmuir 24:10771–10775PubMedCrossRefGoogle Scholar
  8. Dantas-Torres F (2008) Canine vector-borne diseases in Brazil. Parasit Vectors 1:25. doi: 10.1186/1756-3305-1-25 PubMedCrossRefGoogle Scholar
  9. Dantas-Torres F (2010) Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors 3:26PubMedCrossRefGoogle Scholar
  10. Dantas-Torres F, Latrofa MS, Weigl S, Tarallo VD, Lia RP, Otranto D (2012) Hepatozoon canis infection in ticks during spring and summer in Italy. Parasitol Res 110:695–698PubMedCrossRefGoogle Scholar
  11. Demma LJ, Traeger MS, Nicholson WL, Paddock CD, Blau DM, Eremeeva ME, Dasch GA, Levin ML, Singleton J, Zaki SR, Cheek JE, Swerdlow DL, McQuiston JH (2005) Rocky mountain spotted fever from an unexpected tick vector in Arizona. N Engl J Med 353:587–594PubMedCrossRefGoogle Scholar
  12. 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
  13. Diehl PA (1970) Zur oogenese bei Ornithodoros moubata (Murray) (Ixodoidea: Argasidae) unter besonderer berücksichtigung der vitellogenese. Acta Trop 27:301–355PubMedGoogle Scholar
  14. Farias MPO, Sousa DP, Arruda AC, Arruda MSP, Wanderley AG, Alves LC, Faustino MAG (2007) Eficácia in vitro do óleo da Carapa guianensis Aubl. (andiroba) no controle de Boophilus microplus (Acari: Ixodidae). Rev Bras Plantas Medic 9:68–71Google Scholar
  15. Farias MPO, Sousa DP, Arruda AC, Wanderley AG, Teixeira WC, Alves LC, Faustino MAG (2009) Potencial acaricida do óleo de andiroba Carapa guianensis Aubl. sobre fêmeas adultas ingurgitadas de Anocentor nitens Neumann, 1897 e Rhipicephalus sanguineus Latreille, 1806. Arq Bras Med Vet Zootec 61:877–882CrossRefGoogle Scholar
  16. Freitas DRJ, Pohl PC, Vaz IS (2005) Characterization of acaricide resistance in Boophilus microplus. Acta Sci Vet 33:109–117Google Scholar
  17. Friesen KJ, Kaufman WR (2003) Cypermethrin inhibits eggs development in the ixodid tick Amblyomma hebraeum. Pest Biochem Physiol 76:25–35CrossRefGoogle Scholar
  18. Friesen KJ, Suri R, Kaufman WR (2003) Effects of the avermectin, MK-243, on ovary development and salivary gland degeneration in the ixodid tick Amblyomma hebraeum. Pest Biochem Physiol 76:82–90CrossRefGoogle Scholar
  19. Furquim KCS, Bechara GH, Camargo-Mathias MI (2008) Degeneration of salivary glands of males of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari, Ixodidae). Vet Parasitol 154:325–335PubMedCrossRefGoogle Scholar
  20. Furquim KC, Camargo-Mathias MI, Hebling LMGF, Roma GC, Bechara GH (2011) Ticks' response to feeding on host immunized with glandular extracts of Rhipicephalus sanguineus females fed for 2, 4 and 6 days. I. Inactivity or early degeneration of salivary glands? Parasitol Res 109:147–162PubMedCrossRefGoogle Scholar
  21. Guerra MS (1985) Receituário caseiro: alternativas para o controle de pragas e doenças de plantas cultivadas e seus produtos. Embrater, BrasíliaGoogle Scholar
  22. Hammer MLA, Johns EA (1993) Tapping an Amazonian plethora: four medicinal plants of Marajó Islands, Pará (Brazil). J Ethnopharmacol 40:53–75PubMedCrossRefGoogle Scholar
  23. Harwood RF, James MT (1979) Entomology in human and animal health. Macmillan, New YorkGoogle Scholar
  24. Häuserman W, Friedel T, Hess EA, Strong MB (1992). A new active ingredient for a new approach to protect cattle against ticks. Proceedings of XIX International Congress of Entomology (Beijing, China) p. 138Google Scholar
  25. Hilton HE (1982) Biology of insect egg shells. Pergamon, OxfordGoogle Scholar
  26. Jiang Y, Chen H, Mao S, Luo P, Du Y, Liu M (2011) Dynamics of mixed surfactants in aqueous solutions. J Phys Chem 115:1986–1990CrossRefGoogle Scholar
  27. Labruna MB (2004) Biologia-ecologia de Rhipicephalus sanguineus (Acari: Ixodidae). Rev Soc Bras Med Trop 13:123–124Google Scholar
  28. Lorenzi H (2002) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Instituto Plantarum, Nova OdessaGoogle Scholar
  29. Maniasso N (2001) Ambientes micelares em química analítica. Quim Nova 24:87–93CrossRefGoogle Scholar
  30. Nodari EF, Roma GC, Furquim KCS, Bechara GH, Camargo-Mathias MI (2011) Cytotoxic effects of permethrin in salivary glands of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) of semi-engorged females. Exp Parasitol 128:151–158PubMedCrossRefGoogle Scholar
  31. 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
  32. Oliveira PR, Camargo-Mathias MI, Bechara GH (2007) Vitellogenesis in the tick Amblyomma triste (Koch, 1844) (Acari: Ixodidae): Role for pedicel cells. Vet Parasitol 143:134–139PubMedCrossRefGoogle Scholar
  33. Oliveira PR, Bechara GH, Camargo-Mathias MI (2008) Evaluation of cytotoxic effects of fipronil on ovaries of semi-engorged Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) tick female. Food Chem Toxicol 46:2459–2465PubMedCrossRefGoogle Scholar
  34. Oliveira PR, Bechara GH, Marin-Morales MA, Camargo-Mathias MI (2009) Action of the chemical agent fipronil on the reproductive process of semi-engorged females of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Ultrastructural evaluation of ovary cells. Food Chem Toxicol 47:1255–1264PubMedCrossRefGoogle Scholar
  35. Paz GF, Labruna MB, Leite RC (2008) Ritmo de queda de Rhipicephalus sanguineus (Acari: Ixodidae) de cães artificialmente infestados. Ver Bras Parasitol Vet 17:139–144Google Scholar
  36. Revilla J (2001) Plantas da Amazônia: oportunidades econômicas e sustentáveis. Inpa, Sebrae, ManausGoogle Scholar
  37. Rey L (1973) Parasitologia. Guanabara Koogan, Rio de JaneiroGoogle Scholar
  38. Ribeiro FA, Fernandes JI, Correia TR (2006) Eficácia “in vitro” de diferentes acaricidas no controle de fêmeas ingurgitadas de Rhipicephalus sanguineus. In: Congresso Brasileiro de Parasitologia Veterinária e Simpósio Latino Americano, Ribeirão Preto, pp 225Google Scholar
  39. Roma GC, Oliveira PR, Pizano MA, Camargo-Mathias MI (2009) Determination of LC50 of permethrin acaricide in semi-engorged females of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 123:269–272PubMedCrossRefGoogle Scholar
  40. Roma GC, Furquim KCS, Bechara GH, Camargo-Mathias MI (2010a) Permethrin-induced morphological changes in oocytes of Rhipicephalus sanguineus (Acari: Ixodidae) semi-engorged females. Food Chem Toxicol 48:825–830PubMedCrossRefGoogle Scholar
  41. Roma GC, Bechara GH, Camargo-Mathias MI (2010b) Permethrin-induced ultrastructural changes in oocytes of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) semi-engorged females. Ticks Tick-Borne Dis 1:113–123PubMedCrossRefGoogle Scholar
  42. 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
  43. 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. doi: 10.1007/s00436-012-2962-2
  44. Ruppert EE, Fox RS, Barnes RD (2005) Zoologia dos invertebrados. Uma abordagem funcional-evolutiva, RocaGoogle Scholar
  45. Said EA (1992) A contribution to the anatomy and histology of the female reproductive system of Amblyomma cajennense (Acarina: Ixodidae). J Egypt Soc Parasitol 22:385–393Google Scholar
  46. Sanches GS, Bechara GH, Camargo-Mathias MI (2010) Ovary and oocyte maturation of the tick Amblyomma brasiliense Aragão, 1908 (Acari: Ixodidae). Micron 41:84–89CrossRefGoogle Scholar
  47. Sonenshine DE (1991) The female reproductive system. In: Sonenshine DE (ed) Biology of ticks. Oxford University Press, New York, pp 280–304Google Scholar
  48. Walker A (1994) The arthropods of humans and domestic animals. A guide to preliminary identification. Chapman and Hall, LondonGoogle Scholar
  49. Walker JB, Keirans JE, Horak IG (2000) The genus Rhipicephalus (Acari: Ixodidae): a guide to the brown ticks of the world. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Maria Cláudia Ramalho Vendramini
    • 1
  • Maria Izabel Camargo-Mathias
    • 1
  • Adriano Uemura de Faria
    • 1
  • Gervásio Henrique Bechara
    • 1
  • Patrícia Rosa de Oliveira
    • 1
  • Gislaine Cristina Roma
    • 1
    Email author
  1. 1.UNESP—Univ. Estadual PaulistaSão PauloBrazil

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