Abstract
Ximenia americana L. is popularly known as a plum or wild plum, which belongs to the Olacaceae family. Rhipicephalus (Boophilus) microplus represents one of the most important bovine ectoparasites that causes damage to the livestock sector. The objective of this study was to evaluate the acaricide effect of the X. americana stem bark hydroethanolic extract (EHXA) against R. (B.) microplus and its possible modulatory action when in association with cypermethrin, through the adult immersion test. The in vitro acaricide activity of the extract over R. (B.) microplus engorged females was tested using concentrations ranging from 5 to 80 mg mL− 1, which resulted in mortalities between 13.34 and 100 %, with a posture index (PI) between 0.038 and 0.226 and a posture inhibition index (PII) between 0.87 and 83.33 %. The modulatory effect of the EHXA (1.58 mg mL− 1) resulted in mortality between 0 and 46.6 %, with a posture index of 0.221 to 0.139 and a posture inhibition index between 3.01 and 38.49 %. The acaricide activity of the EHXA and its action on oviposition was demonstrated for the first time in this study, demonstrating the potential use of this extract as an auxiliary therapy in R. (B.) microplus control.
Similar content being viewed by others
References
Abdel-Shafy S, Zayed AA (2002) In vitro acaricidal effect of plant extract of neem seed oil (Azadirachta indica) on egg, immature, and adult stages of Hyalomma anatolicum excavatum (Ixodoidea: Ixodidae). Vet Parasitol 106:89–96. https://doi.org/10.1016/s0304-4017(02)00023-7
Aragão TP, Prazeres LDKTd, Brito SA, Neto PJR, Rolim LA, Almeida JRGdS, Caldas GFR, Wanderley AG (2018) Contribution of secondary metabolites to the gastroprotective effect of aqueous extract of Ximenia americana L. (Olacaceae) stem bark in rats. Molecules 23:112. https://doi.org/10.3390/molecules23010112
Almeida M.L.B., Freitas W.E.D.S., Morais P.L.D. De, Sarmento J.D.A. & Alves R.E. 2016. Bioactive compounds and antioxidant potential fruit of Ximenia americana L. Food Chem. 192: 1078–1082 - https://doi.org/10.1016/j.foodchem.2015.07.129
Babujanarthanam R, Kavitha P, Pandian MR (2010) Quercitrin, a bioflavonoid improves glucose homeostasis in streptozotocin-induced diabetic tissues by altering glycolytic and gluconeogenic enzymes. Fundam Clin Pharmacol 24:357–364. https://doi.org/10.1111/j.1472-8206.2009.00771.x
Brasileiro MT, Egito AA, Lima JR, Randau KP, Pereira GC, Neto PJR (2008) Ximenia americana L.: botânica, química e farmacologia no interesse da tecnologia farmacêutica. Rev Bras Farm 89:164–167
Campos FM, Couto JA, Figueiredo AR, Tóth IV, Rangel AOSS, Hogg TA (2009) Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol 135:144–151. https://doi.org/10.1016/j.ijfoodmicro.2009.07.031
Carolina A, Chagas DS, Cristina M, Oliveira DS, Giglioti R, Costa R, Santana M, Ribeiro H, Ervatti P, Celio F, Chaves M (2016) Efficacy of 11 Brazilian essential oils on lethality of the cattle tick Rhipicephalus (Boophilus) microplus. Ticks Tick Borne Dis 2016:1–6. https://doi.org/10.1016/j.ttbdis.2016.01.001
da Silva BAF, da Costa RHS, Fernandes CN, Leite LHI, Ribeiro-Filho J, Garcia TR, Coutinho HDM, Wanderley AG, de Menezes IRA (2015) HPLC profile and antiedematogenic activity of Ximenia americana L. (Olacaceae) in mice models of skin inflammation. Food Chem Toxicol 119:199–205. https://doi.org/10.1016/j.fct.2018.04.041
Dantas ACS, Machado DMR, Araujo AC, Oliveira-Junior RG, Lima-Saraiva SRG, Ribeiro LAA, Almeida J, Horta MC (2015) Acaricidal activity of extracts from the leaves and aerial parts of Neoglaziovia variegata (Bromeliaceae) on the cattle tick Rhipicephalus (Boophilus) microplus. Res Vet Sci 100:165–168. https://doi.org/10.1016/j.rvsc.2015.04.012
de Menezes IRA, da Costa RHS, Boligon AA, Rolón M, Coronel C, Vega C, Coutinho HDM, da Costa MS, Tintino SR, Pereira RLS (2019) Ximenia americana L. enhances the antibiotic activity and inhibit the development of kinetoplastid parasites. Comp Immunol Microbiol Infect Dis 64:40–46. https://doi.org/10.1016/j.cimid.2019.02.007
Dias TLMF, Melo GMA, da Silva YKC, Queiroz AC, Goulart HF, Alexandre-Moreira MS, Santana AEG, Uchôa VT (2018) Antinociceptive and anti-inflammatory activities of the ethanolic extract, of fractions and of epicatechin isolated from the stem bark of Ximenia americana L. (Oleacaceae). Rev Virtual Quim 10:86–101. https://doi.org/10.21577/1984-6835.20180009
Drummond RO, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and B. microplus: laboratory tests of insecticides. J Econ Entomol 66:130–133. https://doi.org/10.1093/jee/66.1.130
Dutta S, Godara R, Katoch R, Yadav A, Katoch M, Singh NK (2017) Detection of amitraz and malathion resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Jammu region of India. Exp Appl Acarol 71:291–301. https://doi.org/10.1007/s10493-017-0111-4
El-Haddad D, Bitam I, Bouchenak O, Toubal S, Yahiaoui K, Arab K, Boumaza S (2018) Acaricidal activity of flavonoids extract of Borago officinalis L. (Boraginaceae) against brown dog tick, Rhipicephalus sanguineus (Latreille, 1806). Trop Biomed 35:383–391
Erdogan G, Karadag R (2005) Quercetin (3,3’,4’,5,7-pentahydroxyflavone) Complexes with Calcium (II) and Magnesium(II), Its Potentiometrie and Spectrophotometric studies. Rev Anal Chem 24:9–24. https://doi.org/10.1515/REVAC.2005.24.1.9
Fatope MO, Adoum OA, Takeda Y (2000) C18 acetylenic fatty acids of Ximenia americana with potential pesticidal activity. J Agric Food Chem 48:1872–1874. https://doi.org/10.1021/jf990550k
Frenkel N, Makky A, Sudji IR, Wink M, Tanaka M (2014) Mechanistic investigation of interactions between steroidal saponin digitonin and cell membrane models. J Phys Chem B 118:14632–14639. https://doi.org/10.1021/jp5074939
Gasparin FRS, Spitzner FL, Ishii-Iwamoto EL, Bracht A, Constantin J (2003) Actions of quercetin on gluconeogenesis and glycolysis in rat liver. Xenobiotica 33:903–911. https://doi.org/10.1080/0049825031000140878
Gazim ZC, Demarchi IG, Lonardoni MVC, Amorim ACL, Hovell AMC, Rezende CM, Ferreira GA, de Lima EL, de Cosmo FA, Cortez DAG (2011) Acaricidal activity of the essential oil from Tetradenia riparia (Lamiaceae) on the cattle tick Rhipicephalus (Boophilus) microplus (Acari; Ixodidae). Exp Parasitol 129:175–178. https://doi.org/10.1016/j.exppara.2011.06.011
Gemeda N, Mokonnen W, Lemma H, Tadele A, Urga K, Addis G, Debella A, Getachew M, Teka F, Yirsaw K (2014) Insecticidal activity of some traditionally used Ethiopian medicinal plants against sheep ked Melophagus ovinus. J Parasitol Res 2014. https://doi.org/10.1155/2014/978537
Ghosh S, Tiwari SS, Srivastava S, Sharma AK, Kumar S, Ray DD, Rawat AKS (2013) Acaricidal properties of Ricinus communis leaf extracts against organophosphate and pyrethroids resistant Rhipicephalus (Boophilus) microplus. Vet Parasitol 192:259–267. https://doi.org/10.1016/j.vetpar.2012.09.031
Giglioti R, Forim MR, Oliveira HN, Chagas ACS, Ferrezini J, Brito LG, Falcoski T, Albuquerque LG, Oliveira MCS (2011) In vitro acaricidal activity of neem (Azadirachta indica) seed extracts with known azadirachtin concentrations against Rhipicephalus microplus. Vet Parasitol 181:309–315. https://doi.org/10.1016/j.vetpar.2011.03.053
Godara R, Katoch R, Yadav A, Ahanger RR, Bhutyal ADS, Verma PK, Katoch M, Dutta S, Nisa F, Singh NK (2015) In vitro acaricidal activity of ethanolic and aqueous floral extracts of Calendula officinalis against synthetic pyrethroid resistant Rhipicephalus (Boophilus) microplus. Exp Appl Acarol 67:147–157. https://doi.org/10.1007/s10493-015-9929-9
Graham OH, Drummond RO (1964) Laboratory screening of insecticides for the prevention of reproduction of Boophilus ticks. J Econ Entomol 57:335–339. https://doi.org/10.1093/jee/57.3.335
Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, León AAP, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Rev Bras Parasitol Vet 23:150–156. https://doi.org/10.1590/s1984-29612014042
Gross AD, Temeyer KB, Day TA, de León AAP, Kimber MJ, Coats JR (2015) Pharmacological characterization of a tyramine receptor from the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Biochem Mol Biol. https://doi.org/10.1016/j.ibmb.2015.04.008
Leopoldini M, Russo N, Chiodo S, Toscano M (2006) Iron chelation by the powerful antioxidant flavonoid quercetin. J Agric Food Chem 54:6343–6351. https://doi.org/10.1021/jf060986h
Lucilania M, Almeida B, Edelky W, Freitas DS, Lígia P, Morais D, Dárcio J, Sarmento A, Elesbão R (2016) Bioactive compounds and antioxidant potential fruit of Ximenia americana L. Food Chem 192:1078–1082. https://doi.org/10.1016/j.foodchem.2015.07.129
Lüdecke D, Ben-Shachar M, Patil I, Makowski D (2020) Extracting, computing and exploring the parameters of statistical models using R. J Open Source Softw 5:2445. https://doi.org/10.21105/joss.02445
Maikai VA (2010a) Antitrypanosomal activity of flavonoid extracted from Ximenia americana stem bark. Int J Biol 3:115. https://doi.org/10.5539/ijb.v3n1p115
Maikai VA (2010b) In vitro and in vivo evaluation of anti-trypanosomal activity of stem bark of Ximenia americana. Int J Biol 2:50. https://doi.org/10.5539/ijb.v2n2p50
Maikai VA, Maikai BV, Kobo PI (2014) In vitro effect of aqueous extract and fraction IV portion of Ximenia americana stem bark on Trypanosoma congolense DNA. J Parasitol Res 2014. https://doi.org/10.1155/2014/904318
Martinez-Velazquez M, Castillo-Herrera GA, Rosario-Cruz R, Flores-Fernandez JM, Lopez-Ramirez J, Hernandez-Gutierrez R, del C Lugo-Cervantes E (2011) Acaricidal effect and chemical composition of essential oils extracted from Cuminum cyminum, Pimenta dioica and Ocimum basilicum against the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitol Res 108:481–487. https://doi.org/10.1007/s00436-010-2069-6
Mbaya AW, Ogwiji M (2014) In-vivo and In-vitro activities of medicinal plants on ecto, endo and haemoparasitic infections: a review. Curr Clin Pharmacol 9:271–282. https://doi.org/10.2174/1574884709999140606161757
Melzig MF, Bader G, Loose R (2001) Investigations of the mechanism of membrane activity of selected triterpenoid saponins. Planta Med 67:43–48. https://doi.org/10.1055/s-2001-10632
Minho AP, Domingues LF, Gainza YA, Figueiredo A, Boligon AA, Domingues R, Chagas ACS (2020) In vitro screening of plant extract on Haemonchus contortus and Rhipicephalus (Boophilus) microplus. J Essent Oil Res 32:269–278. https://doi.org/10.1080/10412905.2020.1746414
Pirali-Kheirabadi K, da Silva JAT (2010) Lavandula angustifolia essential oil as a novel and promising natural candidate for tick (Rhipicephalus (Boophilus) annulatus) control. Exp Parasitol 126:184–186. https://doi.org/10.1016/j.exppara.2010.04.012
Ribeiro VLS, Avancini C, Gonçalves K, Toigo E, von Poser G (2008) Acaricidal activity of Calea serrata (Asteraceae) on Boophilus microplus and Rhipicephalus sanguineus. Vet Parasitol 151:351–354. https://doi.org/10.1016/j.vetpar.2007.11.007
Rodríguez A, Rodríguez C, Cruz A (2010) The acaricide effect of ethanolic extracts of some plants on tics Rhipicephalus (Boophilus) microplus. Rev MVZ Córdoba 15:2175–2184
Rodríguez-Vivas RI, Mata-Mendez Y, Pérez-Gutierrez E, Wagner G (2004) The effect of management factors on the seroprevalence of Anaplasma marginale in Bos indicus cattle in the Mexican tropics. Trop Anim Health Prod 36:135–143. https://doi.org/10.1023/b:trop.0000012105.19518.80
Rosado-Aguilar JA, Aguilar-Caballero A, Rodriguez-Vivas RI, Borges-Argaez R, Garcia-Vazquez Z, Mendez-Gonzalez M (2010) Acaricidal activity of extracts from Petiveria alliacea (Phytolaccaceae) against the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Vet Parasitol 168:299–303. https://doi.org/10.1016/j.vetpar.2009.11.022
Shettar AK, Sateesh MK, Kaliwal BB, Vedamurthy AB (2017) In vitro antidiabetic activities and GC-MS phytochemical analysis of Ximenia americana extracts. South African J Bot 111:202–211. https://doi.org/10.1016/j.sajb.2017.03.014
Silva WC, de Souza Martins JR, de Souza HEM, Heinzen H, Cesio MV, Mato M, Albrecht F, de Azevedo JL, de Barros NM (2009) Toxicity of Piper aduncum L.(Piperales: Piperaceae) from the Amazon forest for the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Vet Parasitol 164:267–274. https://doi.org/10.1016/j.vetpar.2009.06.006
Silva KMA, Chaves TP, Santos RL, Brandã DO, Fernandes FHA, Ramos-Júnior FJL, Dos-Santos VL, Felismino DC, Medeiros ACD (2015) Modulation of the erythromycin resistance in Staphylococcus aureus by ethanolic extracts of Ximenia americana L and Schinopsis brasiliensis Engl. Bol Latinoam Caribe Plant Med Aromat 14:92–98
Singh NK, Vemu B, Nandi A, Singh H, Kumar R, Dumka VK (2014) Acaricidal activity of Cymbopogon winterianus, Vitex negundo and Withania somnifera against synthetic pyrethroid resistant Rhipicephalus (Boophilus) microplus. Parasitol Res 113:341–350. https://doi.org/10.1007/s00436-013-3660-4
Uchôa VT (2009) Estudo fitoquímico e farmacológico das espécies Ximenia americana L. Cecropia pachystachya Tréc. Tese, Universidade Federal de Alagoas
Uekusa Y, Kamihira M, Nakayama T (2007) Dynamic behavior of tea catechins interacting with lipid membranes as determined by NMR spectroscopy. J Agric Food Chem 55:9986–9992. https://doi.org/10.1021/jf0712402
Wagner C, Vargas AP, Roos DH, Morel AF, Farina M, Nogueira CW, Aschner M, Rocha JB (2010) Comparative study of quercetin and its two glycoside derivatives quercitrin and rutin against methylmercury (MeHg)-induced ROS production in rat brain slices. Arch Toxicol 84:89–97. https://doi.org/10.1007/s00204-009-0482-3
Zhang Y, Dong L, Li J, Chen X (2008) Studies on the interaction of gallic acid with human serum albumin in membrane mimetic environments. Talanta 76:246–253. https://doi.org/10.1016/j.talanta.2008.02.033
Acknowledgements
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES—Finance Code 001), National Council for Scientific and Technological Development (CNPq), Cearense Foundation to Support Scientific and Technological Development (FUNCAP), and Financier of Studies and Projects (FINEP).
Author information
Authors and Affiliations
Contributions
Roger Henrique Sousa da Costa, Felipe Francelino Ferreira, Francisca Fabiana Costa dos Santos: Conceptualization, Methodology, Roger Henrique Sousa da Costa,: Writing- Original draft preparation. Francisco Assis Bezerra da Cunha: Visualization; Roger Henrique Sousa da Costa, Maria Rayane Correia de Oliveira, Isabel Sousa Alcântara: Investigation. Irwin Rose Alencar de Menezes, Henrique Douglas Melo Coutinho: Supervision.; Gyllyandeson de Araújo Delmondes: Validation.:Anita Oliveira Brito Pereira Bezerra Martins: Writing- Reviewing and Editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
da Costa, R.H.S., Martins, A.O.B.P.B., de Oliveira, M.R.C. et al. Acaricide activity of the Ximenia americana L. (Olacaceae) stem bark hydroethanolic extract against Rhipicephalus (Boophilus) microplus. Biologia 77, 1667–1674 (2022). https://doi.org/10.1007/s11756-021-00862-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00862-2