Revista Cienfica, FCV-LUZ / Vol. XXXV Recibido:11/11/2024 Aceptado:10/01/2025 Publicado: 18/03/2025 hps://doi.org/10.52973/rcfcv-e35569 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 6 Relaonship between racial predominance and ectoparasites in crossbreed cale herds in a dry tropical weather. Technical note Relación entre predominancia racial y ectoparásitos en rebaños bovinos meszos en un clima seco tropical. Nota técnica Jennifer Cedeño-Macías 1,2 , Víctor Montes-Zambrano 1,3 , Francisco Angulo-Cubillán* ¹Universidad Técnica de Manabí, Facultad de Posgrado, Estudiante Maestría en Medicina Veterinaria. Portoviejo, Ecuador. ²Universidad Técnica de Manabí, Facultad de Ciencias Veterinarias, Departamento de Veterinaria, Extensión Lodana. Santa Ana, Ecuador. ³Universidad del Zulia, Facultad de Ciencias Veterinarias, Departamento de Sanidad Animal. Maracaibo, Venezuela. *Corresponding author: francisco.angulo@utm.edu.ec ABSTRACT To esmate the ectoparasites prevalence and assess the impact of the racial predominance of Bos taurus taurus, Bos taurus indicus, and their crossbreeds on this prevalence in dual- purpose cale herds in a tropical dry weather in Venezuela, a cluster sampling was conducted. 564 animals from twenty- two cale producon systems were sampled, proporonally distributed across six age groups (<3, 3-6, 6-12, 12-18, 18-32, and >32 months, respecvely). The animals were evaluated for the presence of ectoparasites, with specimens collected for idenficaon using dichotomous keys. Addionally, the variables of age and racial predominance were analyzed. The overall prevalence of ectoparasites was 57.54%, with specific prevalences of 51.5% for Haematobia irritans, 20.6% for Rhipicephalus (Boophilus) microplus, and 1.06% for Stomoxys calcitrans. There was a significant effect of age and racial predominance on the prevalence of ectoparasites overall, parcularly for H. irritans and R. (B.) microplus, with a higher probability of infestaon observed in adult animals and those predominantly B.t. taurus. The predominance of B.t. indicus and their crossbreeds was found to be a protecve factor against ectoparasitosis. The relaonship between ectoparasite prevalence and cale racial predominance is clear, with B.t. indicus showing the highest resistance. Key words: Ectoparasites, prevalence, racial predominance, cale. RESUMEN Para esmar la prevalencia de ectoparásitos y evaluar el impacto del predominio racial de Bos taurus taurus, Bos taurus indicus y sus cruces en esta prevalencia en ganaderías de doble propósito en un clima tropical seco de Venezuela, se realizó un muestreo por conglomerados. Se muestrearon 564 animales de 22 sistemas de producción ganadera, distribuidos proporcionalmente en seis grupos etarios (<3, 3-6, 6-12, 12-18, 18-32 y >32 meses, respecvamente). Los animales fueron evaluados en cuanto a la presencia de ectoparásitos, recolectando especímenes para su idenficación mediante claves dicotómicas. Además, se analizaron las variables de edad y predominio racial. La prevalencia general de ectoparásitos fue del 57,54%, con prevalencias específicas de 51,5% para Haematobia irritans, 20,6% para Rhipicephalus (Boophilus) microplus y 1,06% para Stomoxys calcitrans. Se observó un efecto significavo de la edad y del predominio racial sobre la prevalencia de ectoparásitos en general, especialmente para H. irritans y R. (B.) microplus, con una mayor probabilidad de infestación en animales adultos y aquellos predominantemente B.t. taurus. El predominio de B.t. indicus, resultó ser un factor protector contra la ectoparasitosis. La relación entre la prevalencia de ectoparásitos y el predominio racial de B.t. indicus muestra mayor resistencia. Palabras clave: Ectoparásitos, prevalencia, predominio racial, bovinos.
Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION Arthropods of Veterinary importance, parcularly ixodid cks and hematophagous diptera, represent the main threat to the improvement of bovine producon in tropical and subtropical countries [1]. Addionally, these ectoparasites are responsible for transming various diseases of significant concern to both animal and public health [2 , 3], including babesiosis and anaplasmosis, caused by protozoa and blood rickesiae such as Babesia bovis, B. bigemina and Anaplasma marginale [1]. The range of losses caused by ectoparasites stems from direct effects, such as skin damage, toxin injecon, and anemia, which depend on the average intensity of the infestaon, as well as indirect effects resulng from the morbidity and mortality associated with arthropod-borne diseases [4 , 5]. The ck species Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) is characterized by having a single host in its biological cycle, producing up to six generaons per year [6], which contributes to its high prevalence and significant epidemiological importance in disease transmission [7]. The species Haematobia irritans (Diptera: Muscidae), an obligate parasite due to its blood-feeding habits, is notable for its high infestaon levels in livestock [3]. Another ectoparasic species belonging to the Muscidae family is Stomoxys calcitrans, in which both sexes are blood-feeders. This species has a wide geographical distribuon and poses serious health problems to animals, and occasionally to humans, as they serve as mechanical vectors for various pathogens [8]. The control of ectoparasites in livestock has primarily relied on the use of chemical acaricides and inseccides; however, their irraonal use has led to the selecon of isolates resistant to the mechanisms of acon of these drugs [9]. Several strategies contribute to the control of ectoparasites, including the use of resistant genotypes [4], which could serve as a biological control strategy [10]. Crossbreeding and selecon based on host resistance to ectoparasite infestaon aim to pass on to offspring the ability to resist infestaons and reduce the suscepbility of a populaon in a given area [4]. It is well established that the host’s immune response to ectoparasites causes the subspecies Bos taurus taurus and its crosses to be more suscepble, with greater infestaon intensity, than the Bos taurus indicus subspecies [2 , 4 , 5 , 10 , 11]. This difference in suscepbility between the subspecies or breeds affects the prevalence of ectoparasite infestaon [7]; addionally, a control strategy involving selecve treatment only for genecally suscepble animals, or the removal of such animals from the herd as a genec selecon variable, could reduce the parasite load in infestaons and improve the producvity of the producon system [12]. Based on the above, this study aimed to assess the effect of racial predominance (B. t. taurus, B. t. indicus, and their crossbreeds) on the prevalence of ectoparasite infestaon in dual-purpose bovine producon systems in a dry tropical weather in Zulia State, Venezuela. MATERIALS AND METHODS Study locaon The research was conducted in 22 livestock producon systems in the municipality of La Cañada de Urdaneta, located in Zulia State, Venezuela, on the western coast of Lake Maracaibo. The area covers approximately 2,073 km² with 10 meters above sea level and features a dry tropical weather, with an average annual temperature of 28°C. Rainfall varies across the region, increasing from north to south and from east to west, ranging between 600 and 1,200 mm³ annually [13]]. Units and sampling Using random cluster sampling [14], 22 livestock producon systems from the study area were selected, encompassing 564 crossbred animals of B.t. taurus and B.t. indicus. These systems were characterized as tradional dual-purpose operaons, where the primary diet consisted of grazing on pastures with introduced grasses such as Megathyrsus maximus, Cynodon nlemfuensis, and Andropogon gayanus, supplemented with feed and minerals. To search and quanfy ectoparasites on the animals, various anatomical areas were examined, including the head, ears, neck, back, abdomen, armpits, groin, mammary gland, scrotum, and the base of the tail. The number and species of ectoparasites observed were recorded, with species idenficaon based on their morphological characteriscs using the keys described [15]. The prevalence of ectoparasite infestaon were calculated both generally and by species, using epidemiological formulas as described by Margolis et al. [16]. Variables such as producon unit, age, sex, crossbreeding, racial predominance, and coat color were analyzed for stascal associaons with the presence of ectoparasites. Data analysis For descripve stascs, the calculaon of prevalence and the 95% Confidence Interval were used. Univariate analysis was performed, selecng those variables that had a p value <0.20 to be used in the final model. A generalized linear mixed regression model (GLMER) was built forward, the best model being the one that presented the lowest value in the Akaike Informaon Crite- rion (AIC), confusion variables were also evaluated in the final model, with the help of the R soſtware and the GLMER stascal package. RESULTS AND DISCUSSION When evaluang the effect of racial predominance in dual- purpose bovine producon systems, in a dry tropical weather, on epidemiological aspects of infestaon by ectoparasites, moderate prevalence was shown for ixodideans, high for the dipteran H. irritans and low for S. calcitrans. The overall prevalence of ectoparasites in the study was 57.54%, with the individual ectoparasites species prevalence being 51.5, 20.6 and 1.06%, for Haematobia irritans, Rhipicephalus Boophilus microplus and Stomoxys calcitrans, respecvely (TABLE I). The prevalence is considered high in the case of ectoparasites in general and H. irritans, moderate for R.B. microplus and mild in the case of S. calcitrans. 2 of 7
Relaonship between racial predominance and ectoparasites / Cedeño et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico TABLE I. General and species-specific prevalence (%) of ectoparasites in the bovine producon systems evaluated Ectoparasites Haematobia irritans Rhipicephalus Boophilus microplus Stomoxys calcitrans 57.54 51.5 20.6 1.06 Regarding the producon units studied, the prevalence of ectoparasites showed a range between 6.7 and 100% of the animals evaluated and 95% of the herds were affected by H. irritans, with intrafarm prevalence ranging since 30 to 100%; 60% of the herds were affected by R.B. microplus, where its intra-farm prevalence was since 3.3 to 64.3%, and in the case of S. calcitrans 15% of the herds were affected and its intra-farm prevalence was since 3.3 to 13.6%, with significant differences between producon units, for ectoparasites in general and for each species in parcular (P<0.05) (TABLE II). TABLE II. Ectoparasites prevalence (%) and confidence Interval (CI) in general and species specific according to the bovine producon systems evaluated Farm General CI95% H. irritans CI95% R.B. microplus CI95% S. calcitrans CI95% 1 78.6 63.4-93.8 57.1 38.8-75.5 64.3 46.5-82.0 0 2 57.1 38.8-75.5 57.1 38.8-75.5 0 . 3.6 -3.3-10.4 3 6.7 -2.3-15.6 0 3.3 -3.1-9.8 3.3 -3.2-10.1 4 66.7 44.9-88.4 55.6 32.6-78.5 33.3 11.6-55.1 0 5 73.0 56.0-90.1 73.1 56.0-90.1 4.0 -3.5-11.2 0 6 31.0 14.2-47.9 31.0 14.2-47.9 0 0 7 48.0 28.4-67.6 48.0 28.4-67.6 0 0 8 95.6 87.3-100 95.6 87.3-100.0 0 0 9 100.0 100 0 0 10 53.6 33.5-69.9 51.7 33.5-69.9 0 0 11 48.0 28.4-67.6 36.0 17.2-54.8 33.3 17.2-54.8 0 12 62.5 43.1-81.9 33.3 14.5-52.2 41.7 21.9-61.4 0 13 61.1 38.6-83.6 61.1 38.6-83.6 55.6 32.6-78.5 0 14 50.0 32.1-67.9 43.3 25.6-61.1 33.3 16.5-50.2 13.3 1.2-25.5 15 68.4 47.5-89.3 68.4 47.5-89.3 0 0 16 56.7 38.9-74.4 50.0 32.1-67.9 13.3 1.2-25.5 0 17 78.6 63.4-93.8 75.0 59.0-91.0 7.1 -2.4-16.7 0 18 41.4 23.5-59.3 31.0 14.2-47.9 17.2 3.5-31.0 0 19 30.0 9.9-50.1 30.0 9.9-50.1 0 0 20 50.0 32.1-67.9 43.3 25.6-61.1 23.3 8.2-38.5 0 21 80.0 65.7-94.3 80.0 65.7-94.3 60.0 42.5-77.5 0 22 63.3 46.1-80.6 50.0 32.1-67.9 50.0 32.1-67.9 0 The characteriscs that were included in the final model corresponded to age and racial predominance, which were used as predictor variables, the producon unit variable was used as a random effect within the model. Three models were obtained using the occurrence of ectoparasites, the presence of H. irritans and R.B. microplus as dependent variable. The mixed model of the occurrence of ectoparasites in bovine producon systems showed that age is a risk factor OR: 16.8 (P<0.001) for the presence of ectoparasites, which increases as age increases of the animal advances (TABLE III). Similar to the case of ectoparasites, in the occurrence of H. irritans (TABLE IV) and R.B. microplus (TABLE V), it was observed that age is a risk factor (P<0.001), where the older the person, the greater the probability of being parasized. The racial predominance of B.t.indicus was shown to be a protecve factor against infestaon by H. irritans (P<0.001), while in the case of R.B. microplus, B.t.taurus X B.t.indicus crossbreeds are less likely to be infested, compared to B.t.taurus animals. Other authors have observed a posive relaonship between the presence of ectoparasites and the age of hosts, suggesng the hypothesis that adult animals, due to their larger size and therefore greater surface area, might exhibit an increased infestaon rate by the larval stage (Rocha et al., 2019); Added to the fact that young animals exhibit a lower ability to move compared to adults, reducing the risk of being infested by the infecve stages of R.B. microplus. 3 of 6
Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico TABLE III. Results of the mixed model of ectoparasite occurrence in bovine producon systems according to age and racial predominance Variable Category OR CI95% Valor p Age < 3 months Ref. 4 a 6 m 16.8 5.58-50.86 < 0.0001*** 7 a 12 m 60.7 18.87-195.79 <0.0001*** 13 a 18 m 175.12 51.65-593.79 < 0.0001*** 19 a 32 m 306.8 83.86-1,123.11 < 0.0001*** > 32 m 435.0 118.40-1,599.09 < 0.0001*** Racial predominance B.t.taurus Ref. B.t.indicus 0.44 0.24-0.79 0.00645 ** B.t.taurus X B.t.indicus 0.33 0.16-0.68 0.00257 ** OR: Odss Rao CI: Confidense interval TABLE IV. Results of the mixed model of occurrence of Haematobia irritans in bovine producon systems according to age and racial predominance Variable Category OR CI95% Valor p Age < 3 months Ref. 4 a 6 m 3.20 1.85 4.56 < 0.0001*** 7 a 12 m 4.24 2.84 5.64 < 0.0001*** 13 a 18 m 5.44 4.01 6.88 < 0.0001*** 19 a 32 m 6.12 4.60 7.64 < 0.0001*** > 32 m 6.53 5.01 8.06 < 0.0001*** Racial predominance B.t.taurus Ref. B.t.indicus 0.89 -1.47 -0.30 0.00292 ** B.t.taurus X B.t.indicus 1.04 -1.73 -0.33 0.00364 ** OR: Odss Rao CI: Confidense interval TABLE V. Results of the mixed model of occurrence of Rhipicephalus Boophilus microplus in bovine producon systems according to age and racial predominance Variable Category OR IC95% Valor p Age < 3 months Ref. 4 a 6 m 10.7 2.11 54.28 0.004219 ** 7 a 12 m 39.1 7.61 201.36 < 0.0001*** 13 a 18 m 68.1 1.36 340.60 < 0.0001*** 19 a 32 m 53.5 1.04 275.12 < 0.0001*** > 32 m 24.6 4.86 124.52 0.000108 *** Racial predominance B.t.taurus Ref. B.t.indicus 0.57 2.97 1.13 0.108193 B.t.taurus X B.t.indicus 0.40 0.18 0.91 0.029085 * OR: Odss Rao CI: Confidense interval 4 of 6
Relaonship between racial predominance and ectoparasites / Cedeño et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico In the case of racial predominance, there were differences between animals with racial predominance B.t.indicus and its crossbreeds, respect to the predominant B.t.taurus, added to the fact that the characterisc predominance of B.t.indicus, behaves as a protecve factor for ectoparasite infestaon. Infestaon by ectoparasites poses significant challenges for animal welfare, as it affects their health and producon, in addion to the profitability of the producon system. Variaons on these aspects have been reported, with respect to subspecies, breed and/or racial predominance in cale, with differences observed between animals belonging to or predominant to B.t. taurus and B.t. indicus, the laer showing greater resistance to infestaon by ectoparasites in general and R.B. microplus or H. irritans in parcular [10 , 11]. It has been indicated that these differences could be explained by morphological variaons of the skin, characteriscs of each subspecies and their crosses, in addion to heat tolerance due to a greater number and volume of sweat glands by the B.t. indicus, which would reduce chronic heat stress and its effect on the immune response against ectoparasites [5 , 17 , 18], and the length and density of hair among the subspecies, could favor ck infestaon in B.t. taurus [7]. It has been determined that the immune response against ectoparasites is different between the subspecies, indicang that in the case of B.t. taurus is an innate inflammatory response, while in B.t. indicus is acquired mediated by T lymphocytes [1]. The above suggests that genec factors play a main role in the sensivity of infestaon by ectoparasites, providing support that resistance to ectoparasites has a genec basis, with the presence of specific haplotypes that negavely influence the favorable aack of ectoparasites [19]. Cale exhibit heritable phenotypes regarding infestaon with R.B. microplus, which may have arisen from the coevoluon between both species and genec selecon within each. This differences in resistance between the subspecies B.t. taurus and B.t. indicus to R. B. microplus [20]. (20 Tabor, 2017), it has been hypothesized that traits such as skin thickness, hair density, or the specific immune response of each subspecies to ck infestaon could have a significant effect related to genec factors [21]. The presence of proteins associated with innate immunity at the parasite-host interacon site enables resistant cale to develop a protecve response to R. B. microplus infestaon, linked to an early increase in larval rejecon [22]. However, this resistance may be compromised if the host experiences a high parasic burden [23]. The difference observed in the ectoparasites prevalence between the producon units evaluated, which could lead to the conclusion that they may be influenced by microecological and management condions, such as management pracces, control strategies, local climate and breeders awareness [10 , 11 , 24]. The knowledge gained may prove useful for selecng ck resistant cale or manipulang suscepble cale to develop a protecve immune response, thereby reducing the negave impact of R. B. microplus infestaons on cale welfare [20]. CONCLUSIONS The relaonship between the prevalence of ectoparasites and the racial predominance of cale is evident, with the subspecies B.T. indicus and its crosses, showing lower parasite loads. Genec resistance, influenced by both intrinsic factors and ecological condions, must be taken into account in genec improvement programs, since they could reduce the impact of ectoparasites on health and producon in livestock producon systems. ACKNOWLEDGEMENTS To Universidad Técnica de Manabí and Universidad del Zulia, for co-financing this research. Conflict of Interest The authors declare that they have no conflicts of interest. BIBLIOGRAPHICAL REFERENCES [1] Piper E, Jonsson N, Gondro C, Lew-Tabor A, Moolhuijzen P, Vance M, Jackson L. 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