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RESEARCH ARTICLE

Resistance to the tick Rhipicephalus microplus and Babesia bovis infection levels in beef heifers raised in an endemic area of Sao Paulo state, Brazil

A. M. Maiorano A E , R. Giglioti A , M. C. S. Oliveira B , H. N. Oliveira A , J. N. S. G. Cyrillo C , M. E. Z. Mercadante C and J. A. I. I. V. Silva D
+ Author Affiliations
- Author Affiliations

A Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Jaboticabal, SP, Brazil.

B Empresa Brasileira de Pesquisa Agropecuária, São Carlos, SP, Brazil.

C Instituto de Zootecnia, Sertãozinho, SP, Brazil.

D Faculdade de Medicina Veterinária e Zootecnia, Universidade Estadual Paulista ‘Júlio de Mesquita Filho’, Botucatu, SP, Brazil.

E Corresponding author. Email: amanda_maiorano@hotmail.com

Animal Production Science 59(5) 938-944 https://doi.org/10.1071/AN17157
Submitted: 17 March 2017  Accepted: 2 March 2018   Published: 17 May 2018

Abstract

Repeatability coefficients (r) for tick resistance and Babesia bovis infection levels and the correlation (ρ) between these traits were estimated in beef heifers, using artificial infestations and short intervals between measurements. Forty heifers, including 20 Bos taurus taurus (Caracu) and 20 Bos taurus indicus (Nelore) animals, were submitted to three artificial infestations with Rhipicephalus microplus larvae at intervals of 14 days. The number of standard female was counted from the 19th through the 23rd day after each infestation, considering only the left side of each animal. Blood samples were collected on Days 0, 6, 20, 34 and 48 after the first infestation. The number of copies of B. bovis DNA (CN) was estimated from blood samples through the quantitative PCR technique to evaluate the level of infection in the animals. Total tick count (TTC), the percentage of return (PRij) and CN were analysed using the MIXED procedure of the SAS program. The r of the variables were estimated by intraclass correlation between measures of the same animal, with the variance component of the animal being divided by the phenotypic variance (residual + animal), using models with a CS structure matrix. Additionally, ρ among variables were estimated using the CORR procedure. The following results were obtained for Caracu and Nelore animals, respectively: 1.83 ± 0.37 and 0.63 ± 0.40 for TTC, 1.10 ± 0.23 and 0.47 ± 0.23 for PRij, and 2.29 ± 0.64 and 2.32 ± 0.58 for CN. The r was moderate for TTC (0.62) and PRij (0.53) and low for CN (0.10). The ρ between TTC and CN obtained in the same measurement day was not significant in either breed (P > 0.05; –0.07 for Caracu and 0.19 for Nelore). Results showed both breeds were able to develop resistance against B. bovis; however, Nelore exhibited higher tick resistance. The r obtained for CN and the weak association with tick resistance indicate that it is not possible to recommend the use of CN as a trait to predict tick resistance in these two breeds.

Additional keywords: artificial infestations, cattle, qPCR, repeatability.


References

Bennett GF (1974) Oviposition of Boophilus microplus (Canestrini) (Acari: Ixodidae). II. Influence of temperature, humidity and light. Acarologia 16, 250–257.

Bianchin I, Catto JB, Kichel AN, Torres RAA, Honer MR (2007) The effect of the control of endo- and ectoparasites on weight gains in crossbred cattle (Bos taurus taurus × Bos taurus indicus) in the central region of Brazil. Tropical Animal Health and Production 39, 287–296.
The effect of the control of endo- and ectoparasites on weight gains in crossbred cattle (Bos taurus taurus × Bos taurus indicus) in the central region of Brazil.Crossref | GoogleScholarGoogle Scholar |

Bilhassi TB, Oliveira HN, Ibelli AMG, Giglioti R, Regitano LCA, Oliveira-Sequeira TCG, Bressani FA, Malagó W, Resende FD, Oliveira MCS (2014) Quantitative study of Babesia bovis infection in beef cattle from São Paulo state, Brazil. Ticks and Tick-Borne Diseases 5, 234–238.
Quantitative study of Babesia bovis infection in beef cattle from São Paulo state, Brazil.Crossref | GoogleScholarGoogle Scholar |

Bock RE, de Vos AJ, Kingston TG, Mc Lellan DJ (1997) Effect of breed of catle on innate resistance to infection with Babesia bovis, Babesia bigemina, and Anaplasma marginale. Australian Veterinary Journal 75, 337–340.
Effect of breed of catle on innate resistance to infection with Babesia bovis, Babesia bigemina, and Anaplasma marginale.Crossref | GoogleScholarGoogle Scholar |

Brown WC, Palmer GH (1999) Designing blood-stage vaccines against Babesia bovis and Babesia bigemina. Parasitology Today (Personal Ed.) 15, 275–281.
Designing blood-stage vaccines against Babesia bovis and Babesia bigemina.Crossref | GoogleScholarGoogle Scholar |

Buling A, Criado-Fornelio A, Acenzo G, Benitez D, Barba-Carretero JC, Florin-Cristensen M (2007) A quantitative PCR assay for the detection and quantification of B. bovis and B. bigemina. Veterinary Parasitology 147, 16–25.
A quantitative PCR assay for the detection and quantification of B. bovis and B. bigemina.Crossref | GoogleScholarGoogle Scholar |

Castro-Janer E, Martins JR, Mendes MC, Namindome A, Klafke GM, Schumaker TT (2010) Diagnoses of fipronil resistance in Brazilian cattle ticks (Rhipicephalus (Boophilus) microplus) using in vitro larval bioassays. Veterinary Parasitology 173, 300–306.
Diagnoses of fipronil resistance in Brazilian cattle ticks (Rhipicephalus (Boophilus) microplus) using in vitro larval bioassays.Crossref | GoogleScholarGoogle Scholar |

Dalgliesh RJ (1993) Babesiosis. In ‘Immunology and molecular biology of parasitic infections’. (Ed. KS Warren) pp. 352–383. (Blackwell: Oxford)

Fraga AB, Alencar MM, Figueiredo LA, Razook AG, Cyrillo JNSG (2003) Análise de fatores genéticos e ambientais que afetam a infestação de fêmeas bovinas da raça Caracu por carrapatos (Boophilus microplus). Revista Brasileira de Zootecnia 32, 1578–1586.
Análise de fatores genéticos e ambientais que afetam a infestação de fêmeas bovinas da raça Caracu por carrapatos (Boophilus microplus).Crossref | GoogleScholarGoogle Scholar |

Frisch JE (1997) Como criar productivamente ganado de carne en el sub-tropico. In ‘Congreso Internacional de Transferencia Tecnológica Agropecuaria, Asunción, Paraguay’. pp. 137–162.

Frisch JE, O’Neill CJ, Kelly MJ (2000) Using genetics to control cattle parasites: the Rockhampton experience. International Journal for Parasitology 30, 253–264.
Using genetics to control cattle parasites: the Rockhampton experience.Crossref | GoogleScholarGoogle Scholar |

Giglioti R, Oliveira HN, Santana CH, Ibelli AMG, Néo TA, Bilhassi TB, Rabelo MD, Machado RZ, Brito LG, Oliveira MCS (2016) Babesia bovis and Babesia bigemina infection levels estimated by qPCR in Angus cattle from an endemic area of São Paulo state, Brazil. Ticks and Tick-Borne Diseases 7, 657–662.
Babesia bovis and Babesia bigemina infection levels estimated by qPCR in Angus cattle from an endemic area of São Paulo state, Brazil.Crossref | GoogleScholarGoogle Scholar |

Gonzales JC (1993) ‘O Controle do Carrapato do Boi.’ (Mestre Jou: Porto Alegre, RS, Brazil)

Grisi L, Leite RC, Martins JR, Barros AT, Andreotti R, Cançado PH, León AAP, Pereira JB, Villela HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Revista Brasileira de Parasitologia Veterinária 23, 150–156.
Reassessment of the potential economic impact of cattle parasites in Brazil.Crossref | GoogleScholarGoogle Scholar |

Guglielmone AA (1995) Epidemiology of babesiosis and anaplasmosis in South and Central America. Veterinary Parasitology 57, 109–119.
Epidemiology of babesiosis and anaplasmosis in South and Central America.Crossref | GoogleScholarGoogle Scholar |

Ibelli AMG, Ribeiro ARB, Giglioti R, Regitano LCA, Alencar MM, Chagas ACS, Paço AL, Oliveira HN, Duarte JMS, Oliveira MCS (2012) Resistance of cattle of various genetic groups to the tick Rhipicephalus microplus and the relationship with coat traits. Veterinary Parasitology 186, 425–430.
Resistance of cattle of various genetic groups to the tick Rhipicephalus microplus and the relationship with coat traits.Crossref | GoogleScholarGoogle Scholar |

Jonsson NN, Bock RE, Jorgensesn WK (2008) Productivity and health effects of anaplasmosis and babesioses on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia. Veterinary Parasitology 155, 1–9.
Productivity and health effects of anaplasmosis and babesioses on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia.Crossref | GoogleScholarGoogle Scholar |

Jonsson NN, Bock RE, Jorgensen WK, Morton JM, Stear MJ (2012) Is endemic stability of tick-borne disease in cattle a useful concept? Trends in Parasitology 28, 85–89.
Is endemic stability of tick-borne disease in cattle a useful concept?Crossref | GoogleScholarGoogle Scholar |

Ke GM, Cheng HL, Ke LY, Ji WT, Chulu JLC, Liao MH, Chang TJ, Liu HJ (2006) Development of a quantitative Light Cycler real-time RT-PCR for detection of avian reovirus. Journal of Virological Methods 133, 6–13.
Development of a quantitative Light Cycler real-time RT-PCR for detection of avian reovirus.Crossref | GoogleScholarGoogle Scholar |

Klafke G, Webster A, Agnol BD, Pradel E, Silva J, Canal LHL, Becker M, Osório MF, Mansson M, Barreto R, Scheffer R, Souza UA, Corassini VB, Santos J, Reck J, Martins JR (2017) Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil. Ticks and Tick-Borne Diseases 8, 73–80.
Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Kubista M, Andrade JM, Begtsson M, Forootan A, Jonak J, Lind K, Sindelka R, Sjoback R, Sjogreen B, Strombom L, Stahlberg A, Zoric N (2006) The real time polymerase chain reaction. Molecular Aspects of Medicine 27, 95–125.
The real time polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar |

Lima MLP, Bonilha Neto LM, Figueiredo LA, Razook AG (1992) Os bovinos da raça Caracu. Zootecnia 30, 1–12.

Mackinnon MJ, Meyer K, Hetzel DJS (1991) Genetic variation and covariation for growth, parasite resistance and heat tolerance in tropical cattle. Livestock Production Science 27, 105–122.
Genetic variation and covariation for growth, parasite resistance and heat tolerance in tropical cattle.Crossref | GoogleScholarGoogle Scholar |

Nari A (1995) Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America. Veterinary Parasitology 57, 153–165.
Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America.Crossref | GoogleScholarGoogle Scholar |

Oliveira GP, Alencar MM (1987) Resistencia de bovinos ao carrapato Boophilus microplus. 1. Infestação artificial. Pesquisa Agropecuária Brasileira 22, 433–438.

Oliveira MCS, Oliveira-Sequeira TCG, Regitano LCA, Alencar MM, Neo TA, Silva AM, Oliveira HN (2008) Detection of Babesia bigemina in cattle of different genetic groups and in Rhipicephalus (Boophilus) microplus tick. Veterinary Parasitology 155, 281–286.
Detection of Babesia bigemina in cattle of different genetic groups and in Rhipicephalus (Boophilus) microplus tick.Crossref | GoogleScholarGoogle Scholar |

Oliveira MCS, Alencar MM, Giglioti R, Beraldo MCD, Aníbal FF, Correia RO, Boschini L, Chagas ACS, Bilhassi TB, Oliveira HN (2013) Resistance of beef cattle of two genetic groups to ectoparasites and gastrointestinal nematodes in the state of São Paulo, Brazil. Veterinary Parasitology 197, 168–175.
Resistance of beef cattle of two genetic groups to ectoparasites and gastrointestinal nematodes in the state of São Paulo, Brazil.Crossref | GoogleScholarGoogle Scholar |

Piper EK, Jackson LA, Bielefeldt-Ohmann H, Gondro C, Lew-Tabor AE, Jonsson NN (2010) Tick-susceptible Bos taurus cattle display an increased cellular response at the site of larval Rhipicephalus (Boophilus) microplus attachment, compared with tick-resistant Bos indicus. International Journal for Parasitology 40, 431–441.
Tick-susceptible Bos taurus cattle display an increased cellular response at the site of larval Rhipicephalus (Boophilus) microplus attachment, compared with tick-resistant Bos indicus.Crossref | GoogleScholarGoogle Scholar |

Silva AM, Alencar MM, Regitano LCA, Oliveira MCS, Barioni Júnior W (2007) Artificial infestation of Boophilus microplus in beef cattle heifers of four genetic groups. Genetics and Molecular Biology 30, 1150–1155.
Artificial infestation of Boophilus microplus in beef cattle heifers of four genetic groups.Crossref | GoogleScholarGoogle Scholar |

Silva AM, Alencar MM, Regitano LCA, Oliveira MCS (2010) Infestação natural de fêmeas bovinas de corte por ectoparasitas na Região Sudeste do Brasil. Revista Brasileira de Zootecnia 39, 1477–1482.
Infestação natural de fêmeas bovinas de corte por ectoparasitas na Região Sudeste do Brasil.Crossref | GoogleScholarGoogle Scholar |

Sondgeroth KS, McElwain TF, Allen AJ, Chen AV, Lau AO (2013) Loss of neurovirulence is associated with reduction of cerebral capillary sequestration during acute Babesia bovis infection. Parasites & Vectors 6, 181–185.
Loss of neurovirulence is associated with reduction of cerebral capillary sequestration during acute Babesia bovis infection.Crossref | GoogleScholarGoogle Scholar |

Utech KBW, Wharton RH, Kerr JD (1978) Resistance to Boophilus microplus (Canestrini) in different breeds of cattle. Australian Journal of Agricultural Research 29, 885–895.
Resistance to Boophilus microplus (Canestrini) in different breeds of cattle.Crossref | GoogleScholarGoogle Scholar |

Wang W, Chen K, Xu C (2006) DNA quantification using EvaGreen and a real-time PCR instrument. Analytical Biochemistry 356, 303–305.
DNA quantification using EvaGreen and a real-time PCR instrument.Crossref | GoogleScholarGoogle Scholar |