Ecuador; acaricide; cattle; protective factor; risk factor; tick; tick-borne diseases; tropical; Immunology and Allergy; Molecular Biology; Immunology and Microbiology (all); Microbiology (medical); Infectious Diseases; General Immunology and Microbiology
Abstract :
[en] Decision-making on tick control practices is linked to the level of knowledge about livestock farming and to the social context in which individuals practice them. Tick infestation is one of the main problems in tropical livestock production. The objective of this study was to characterize tick-control related practices in two tropical livestock areas and their potential association with the level of tick infestation. A total of 139 farms were included in this survey. To determine this association, a multivariate logistic regression model was used. A stepwise model selection procedure was used and model validation was tested. Cattle husbandry as a main activity, the use of external paddocks, the use of amitraz, and the lack of mechanization on the farm were related with high tick infestation. On the other hand, owner involvement in the preparation of acaricide solution was identified as a protective factor against high tick infestation. At animal level, age (old), body condition status (thin), and lactation were also associated with high tick infestations, while Bos primigenius indicus cattle and their crosses reduced the probability of high tick infestations. The factors studied, such as herd size, education level of the owners, and veterinary guidance, varied from farm to farm. Nonetheless, these differences did not generate changes in the level of tick infestation. According to the area under the receiver operating characteristic curve (AUC-ROC), the model at farm level predicts a high level of infestation, with an accuracy of 72.00% and high sensitivity. In addition, at animal level, crossbreeding with indicus cattle and breeding selection for host resistance will be useful against high tick infestation. Likewise, the implementation of programs of capacitation and research on tick control for farmers, cowboys, and vets in these areas is necessary.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Paucar, Valeria ; Instituto de Investigación en Zoonosis (CIZ), Universidad Central del Ecuador, Quito 170521, Ecuador ; Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Sciences (UREAR-ULiège), Fundamental and Applied Research for Animals & Health (FARAH) Center, Faculty of Veterinary Medicine, University of Liege, 4000 Liège, Belgium
Pérez-Otáñez, Ximena; Instituto de Investigación en Zoonosis (CIZ), Universidad Central del Ecuador, Quito 170521, Ecuador ; Georges Lemaitre Centre for Earth and Climate Research, UCLouvain, 1348 Louvain-la-Neuve, Belgium
Rodríguez-Hidalgo, Richar; Instituto de Investigación en Zoonosis (CIZ), Universidad Central del Ecuador, Quito 170521, Ecuador ; Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito 170521, Ecuador
Perez, Cecilia; Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito 170521, Ecuador
Cepeda-Bastidas, Darío ; Facultad de Ciencias Agrícolas, Universidad Central del Ecuador, Quito 170521, Ecuador
Grijalva, Jorge; Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito 170521, Ecuador
Enríquez, Sandra; Instituto de Investigación en Zoonosis (CIZ), Universidad Central del Ecuador, Quito 170521, Ecuador
Arciniegas-Ortega, Susana; Facultad de Geología, Minas y Petróleo, Universidad Central del Ecuador, Quito 170521, Ecuador
Vanwambeke, Sophie O ; Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Sciences (UREAR-ULiège), Fundamental and Applied Research for Animals & Health (FARAH) Center, Faculty of Veterinary Medicine, University of Liege, 4000 Liège, Belgium
Ron-Garrido, Lenin ; Instituto de Investigación en Zoonosis (CIZ), Universidad Central del Ecuador, Quito 170521, Ecuador ; Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito 170521, Ecuador
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Language :
English
Title :
The Associated Decision and Management Factors on Cattle Tick Level of Infestation in Two Tropical Areas of Ecuador.
ARES - Academy for Research and Higher Education [BE]
Funding text :
Acknowledgments: Our thanks go to the Académie de Recherche et d’Enseignement Supérieur (ARES) for funding this research, the Universidad Central del Ecuador (UCE), UCLouvain and the University of Liège for hosting the project. In addition, our thanks go to all the farmers who participated, the community leaders, the field technicians, and the students of the Faculty of Veterinary Medicine and Agronomy of the Universidad Central del Ecuador, who participated in the field and laboratory work, thanks to whom this research was possible.Funding: This survey was funded by the Academy of Research and Higher Education (ARES) through the Research for Development Project (PRD) entitled ‘Socio-eco-epidemiology of ticks, tick-borne parasites, acaricide resistance and residual effects of acaricides in tropical Ecuadorian livestock: environmental, animal and public health impacts’, which involves universities from Ecuador (CIZ, Universidad Central del Ecuador) and Belgium (UCLouvain and ULiège).
Franco Crespo, C.; Morales Carrasco, L.; Lascano Aimacaña, N.; Cuesta Chávez, A. Dinámica de los pequeños productores de leche en la Sierra centro de Ecuador. La. Granja. 2019, 30, 103–120. [CrossRef]
Banco Central del Ecuador, B. Boletín Estadístico 4.3.2. Producto Interno Bruto Por Industria; Banco Central del Ecuador: Quito, Ecuador, 2018.
Agrocalidad. Categorías de Población de Ganado Bovino de Ecuador; Ministerio de Agricultura y Ganadería: Quito, Ecuador, 2018; p. 1.
Pourrut, P.; Róvere, O.; Romo, I.; Villacrés, H. Los Climas del Ecuador-Fundamentos Explicativos; Ministerio de Agricultura y Ganadería: Quito, Ecuador, 1983; p. 3.
Torres, Y.; Rivas, J.; Pablos, C.; Perea, J.; Toro, P.; Angón, E.; García, A. Identificación e implementación de paquetes tecnológicos en ganadería vacuna de doble propósito. Caso Manabí-Ecuador. Rev. Mex. Cienc. Pecu. 2014, 5, 393–407. [CrossRef]
Gioia, G.V.; Vinueza, R.L.; Marsot, M.; Devillers, E.; Cruz, M.; Petit, E.; Boulouis, H.J.; Moutailler, S.; Monroy, F.; Coello, M.A.; et al. Bovine anaplasmosis and tick-borne pathogens in cattle of the Galapagos Islands. Transbound. Emerg. Dis. 2018, 65, 1262–1271. [CrossRef] [PubMed]
Rymaszewska, A.; Grenda, S. Bacteria of the genus Anaplasma–characteristics of Anaplasma and their vectors: A review. Veterinární Med. 2008, 53, 573–584. [CrossRef]
Greenberg, K.; Tahseen, M.; Davidson, A. Beware of Babesiosis: A rare and severe case causing death. Am. J. Emerg. Med. 2018, 36, 2337.e1–2337.e2. [CrossRef]
Minjauw, B.; Mcleod, A. Tick-Borne Diseases and Poverty. The Impact of Ticks and Tick-Borne Diseases on the Livelihood of Small-Scale and Marginal Livestock Owners in India and Eastern and Southern Africa; DFID Animal Health Programme, Centre for Tropical Veterinary Medicine, University of Edinburgh: Edinburgh, UK, 2003; p. 116.
Namgyal, J.; Tenzin, T.; Checkley, S.; Lysyk, T.J.; Rinchen, S.; Gurung, R.B.; Dorjee, S.; Couloigner, I.; Cork, S.C. A knowledge, attitudes, and practices study on ticks and tick-borne diseases in cattle among farmers in a selected area of eastern Bhutan. PLoS ONE 2021, 16, e0247302. [CrossRef]
Rodríguez-Hidalgo, R.; Pérez-Otáñez, X.; Garcés-Carrera, S.; Vanwambeke, S.O.; Madder, M.; Benítez-Ortiz, W. The current status of resistance to alpha-cypermethrin, ivermectin, and amitraz of the cattle tick (Rhipicephalus microplus) in Ecuador. PLoS ONE 2017, 12, e0174652. [CrossRef]
Torres, Y. Caracterización Socioeconómica de Pequeñas Explotaciones Ganaderas en la Provincia de Manabí; Universidad de Córdoba: Córdoba, Spain, 2012; p. 67.
Ferrari, M. Garrapata, La resistencia del huédped como forma de control. Marca Líquida 2002, 12, 17–20.
Bolaños, D. Distribución Geográfica y Caracterización Taxonómica de las Especies de Garrapatas Que Afectan al Ganado Bovino en la Provincia de Los Ríos; Universidad Central del Ecuador: Quito, Ecuador, 2016; p. 77.
Canevari, J.T.; Mangold, A.J.; Guglielmone, A.A.; Nava, S. Population dynamics of the cattle tick Rhipicephalus (Boophilus) microplus in a subtropical subhumid region of Argentina for use in the design of control strategies. Med. Vet. Entomol. 2017, 31, 6–14. [CrossRef]
Nava, S.; Mastropaolo, M.; Guglielmone, A.A.; Mangold, A.J. Effect of deforestation and introduction of exotic grasses as livestock forage on the population dynamics of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in northern Argentina. Res. Vet. Sci. 2013, 95, 1046–1054. [CrossRef]
Broughan, J.M.; Judge, J.; Ely, E.; Delahay, R.J.; Wilson, G.; Clifton-Hadley, R.S.; Goodchild, A.V.; Bishop, H.; Parry, J.E.; Downs, S.H. A Review of risk factors for bovine tuberculosis infection in cattle in the UK and Ireland. Epidemiol. Infect. 2016, 144, 2899–2926. [CrossRef] [PubMed]
Escobar, A.; Cevallos, O.; Villarreal, P.; Carranza, M.; Carranza, H.; Pinargote, E. Prevalencia y detección por PCR anidada de Anaplasma marginale en bovinos y garrapatas en la zona central del Litoral Ecuatoriano. Cienc. Tecnol. 2015, 8, 11–17. [CrossRef]
Vasco, K. Standardization of Melting Curve Analysis for the Detection of Babesia in Ticks using Nucleotide Polymorphisms; Universidad Central del Ecuador: Quito, Ecuador, 2014; p. 83.
Guillén, N.; Muñoz, L. Estudio Taxonómico a Nivel de Género de Garrapatas en Ganado Bovino de la Parroquia Alluriquín-Santo Domingo de los Tsáchilas; Universidad de las Fuerzas Armadas de Ecuador: Sangolquí, Ecuador, 2013; p. 71.
Pérez, X. Resistencia a Alfa-Cipermetrina, Ivermectina y Amitraz en Garrapatas Rhipicephalus Microplus (Canestrini, 1887) Colectadas en Cuatro Localidades; Universidad Central del Ecuador: Quito, Ecuador, 2016; p. 56.
Maya-Delgado, A.; Madder, M.; Benítez-Ortíz, W.; Saegerman, C.; Berkvens, D.; Ron-Garrido, L. Molecular screening of cattle ticks, tick-borne pathogens and amitraz resistance in ticks of Santo Domingo de Los Tsáchilas province in Ecuador. Ticks Tick-Borne Dis. 2020, 11, 101492. [CrossRef] [PubMed]
Jacho, M. Dinámica Poblacional de la Garrapata Rhipicephalus (Boophilus) Microplus en Ganado Bovino Lechero en el Cantón San Miguel de los Bancos; Universidad Central del Ecuador: Quito, Ecuador, 2015.
Orozco, G. Distribución Espacial de Garrapatas que Afectan a las Ganaderías Ecuatorianas de las Tres Regiones, Usando Como Referencia la Línea Equinoccial; Universidad Central del Ecuador: Quito, Ecuador, 2018.
Nava, S.; Beati, L.; Labruna, M.B.; Cáceres, A.G.; Mangold, A.J.; Guglielmone, A.A. Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum Koch, 1844, and Amblyomma sculptum Berlese, 1888 (Ixodida: Ixodidae). Ticks Tick-Borne Dis. 2014, 5, 252–276. [CrossRef]
Aguilar-Domínguez, M.; Moo-Llanes, D.A.; Sánchez-Montes, S.; Becker, I.; Feria-Arroyo, T.P.; de León, A.P.; Romero-Salas, D. Potential distribution of Amblyomma Mixtum (Koch, 1844) in climate change scenarios in the Americas. Ticks Tick-Borne Dis. 2021, 12, 1–9. [CrossRef]
Pesquera, C.; Portillo, A.; Palomar, A.M.; Oteo, J.A. Investigation of tick-borne bacteria (Rickettsia spp., Anaplasma spp., Ehrlichia spp. and Borrelia spp.) in ticks collected from Andean tapirs, cattle and vegetation from a protected area in Ecuador. Parasit. Vectors 2015, 8, 46. [CrossRef]
Sistema de Información Aracnológica Registros de Ixodidae: Ixodes Montoyanus. Available online: http://entomologia.ec/arachnida/especie.php?especie=Ixodesmontoyanus&familia=Ixodidae (accessed on 13 January 2022).
Enríquez, S.; Guerrero, R.; Arrivillaga-Henríquez, J.; Araujo, P.; Villacrés, E.; Enríquez, A.; Benítez-Ortíz, W. New Records of Ticks of Genus Amblyomma Koch, 1844 (Acari: Ixodidae) for Ecuador. Acta Parasitol. 2020, 65, 430–440. [CrossRef]
Voltzit, O. A review of neotropical Amblyomma species (Acari: Ixodidae). Acarina 2007, 1, 3–134.
Duchi, T.; Guevara, V. Análisis de Factores que Determinan la Sotenibilidad y Sustentabilidad de la Economía Socialy Solidaria Para la Industrialización y Comercialización de la Leche y sus Derivados en los Cantones Los Bancos, Pedro Vicente Maldonado y Puerto Quito; Universidad Politécnica Salesiana: Quito, Ecuador, 2013; p. 208.
Jacome, E.; Morales, D. Diagnóstico Situacional de la Comercialización y Calidad del Ganado Bovino de Carne en Pacto, Gualea, Nanegal y Nanegalito Parroquias del Cantón Quito-Pichincha; Escuela Politécnica del Ejercito: Sangolquí, Ecuador, 2005; p. 98.
Vizcarra, R. La Leche del Ecuador; Universidad Central del Ecuador: Quito, Ecuador, 2015; p. 183.
Proaño, J.; Miño, R. Evaluación del Proyecto de Ganadería en el Cantón Quijos, Provincia de Napo (2007–2011), Ejecutado Por el Programa Regional Ecobona; Universidad Central del Ecuador: Quito, Ecuador, 2013; pp. 1–13.
Grijalva, J.; Arévalo, V.; Wood, C. Expansión y trayectorias de la ganadería en la Amazonía: Estudio en el Valle de los Quijos y Piedemonte, en la selva alta del Ecuador. Publ. Miscelánea INIAP 2004, 125, 201.
Leiva, T.; Barrionuevo, M. Relaciones de Género en los Sistemas Agropecuarios del Cantón Quijos; Escuela Politécnica del Ejercito: Sangolquí, Ecuador, 2010; pp. 1–63.
Arévalo, V.; Andino, M.; Grijalva, J. Geopolítica y transformaciones agrarias: El valle de Los Quijos en la amazonia Ecuatoriana. Publ. Miscelánea INIAP 2008, 142, 102.
Abbas, R.Z.; Zaman, M.A.; Colwell, D.D.; Gilleard, J.; Iqbal, Z. Acaricide resistance in cattle ticks and approaches to its management: The state of play. Vet. Parasitol. 2014, 203, 6–20. [CrossRef]
Rodriguez-Vivas, R.I.; Jonsson, N.N.; Bhushan, C. Strategies for the control of Rhipicephalus microplus ticks in a world of conventional acaricide and macrocyclic lactone resistance. Parasitol. Res. 2018, 117, 3–29. [CrossRef]
Calligaris, I.; Oliveira, P.; Gislaine, C.; Gervasio, H.; Camargo, M. Action of the insect growth regulator fluazuron, the active ingredient of the acaricide acatak, in Rhipicephalus Sanguineus Nymphs (Latreille, 1806) (Acari: Ixodidae). Microsc. Res. Tech. 2013, 76, 1177–1185. [CrossRef]
Frazzoli, C.; Mantovani, A. The environment-animal-human web: A “one health” view of toxicological risk. Frontiers in Public Health and Frontiers in Environmental Science. 2019, 5, 99–108. [CrossRef]
Pérez, X. Distribución de la Resistencia a Los Acaricidas Amitraz, Ivermectina y Alfacipermetrina en Garrapatas Boophilus Microplus y Posibles Factores de Riesgo Asociados, en la Zona ±0.5 Grados de Latitud de la Línea Equinoccial de Ecuador; Universidad Central del Ecuador: Quito, Ecuador, 2019.
Betancur, J.; Giraldo, C. Economic and health impact ofthe ticks in production animals. IntechOpen. 2019, 1, 1–19. [CrossRef]
Jongejan, F.; Uilenberg, G. The global importance of ticks. Parasitology 2004, 129, S3–S14. [CrossRef]
Bianchi, M.W.; Barré, N.; Messad, S. Factors related to cattle infestation level and resistance to acaricides in Boophilus microplus tick populations in New Caledonia. Vet. Parasitol. 2003, 112, 75–89. [CrossRef]
Agrocalidad. Manual Para el Registro de Empresas y Productos de Uso Veterinario; Ministerio de Agricultura y Ganadería: Quito, Ecuador, 2021; pp. 1–246.
Bejarano, F. Los plaguicidas altamente peligrosos en México. Red Acción Sobre Plaguicidas Altern. En México C 2017, 17, 1–351.
Maryam, J.; Babar, M.E.; Nadeem, A.; Hussain, T. Genetic variants in interferon gamma (IFN-γ) gene are associated with resistance against ticks in Bos taurus and Bos indicus. Mol. Biol. Rep. 2012, 39, 4565–4570. [CrossRef]
Piper, E.K.; Jackson, L.A.; Bielefeldt-Ohmann, H.; Gondro, C.; Lew-Tabor, A.E.; Jonsson, N.N. 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 cattle. Int. J. Parasitol. 2010, 40, 431–441. [CrossRef]
de Castro, J.J. Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet. Parasitol. 1997, 71, 77–97. [CrossRef]
Burrow, H.M.; Mans, B.J.; Cardoso, F.F.; Birkett, M.A.; Kotze, A.C.; Hayes, B.J.; Mapholi, N.; Dzama, K.; Marufu, M.C.; Githaka, N.W.; et al. Towards a new phenotype for tick resistance in beef and dairy cattle: A review. Anim. Prod. Sci. 2019, 59, 1401. [CrossRef]
Condori, R.; Ibáñez, T.; Hernández, R.; Ochoa, R.; Loza-Murguia, M.G. Frecuencia relativa de Boophilus microplus (Canestrini 1888) & Amblyomma cajennense (Fabricius 1787) (Acari: Ixodida) en ganado bovino, en la zona de colonización de Yucumo, Provincia Gral. José Ballivián Departamento Del Beni, Bolivia. J. Selva Andina Res. Soc. 2010, 1, 13–22. [CrossRef]
Shyma, K.P.; Gupta, J.P.; Singh, V. Breeding strategies for tick resistance in tropical cattle: A sustainable approach for tick control. J. Parasit. Dis. 2015, 39, 1–6. [CrossRef] [PubMed]
Hughes, S.; Kelly, P. Interactions of malnutrition and immune impairment, with specific reference to immunity against parasites. Parasite Immunol. 2006, 28, 577–588. [CrossRef]
Sutherst, R.W.; Kerr, J.D.; Maywald, G.F.; Stegeman, D.A.; Tolleson, D.R.; Carstens, G.E.; Welsh, T.H.; Teel, P.D.; Strey, O.F.; Longnecker, M.T.; et al. The effect of season and nutrition on the resistance of cattle to the tick Boophilus microplus. Aust. J. Agric. Res. 1983, 90, 3442–3450. [CrossRef]
Tolleson, D.R.; Carstens, G.E.; Welsh, T.H.; Teel, P.D.; Strey, O.F.; Longnecker, M.T.; Prince, S.D.; Banik, K.K. Plane of nutrition by tick-burden interaction in cattle: Effect on growth and metabolism. J. Anim. Sci. 2012, 90, 3442–3450. [CrossRef]
Frisch, J.E.; O’Neill, C.J.; Kelly, M.J. Using genetics to control cattle parasites—the Rockhampton experience. Int. J. Parasitol. 2000, 30, 253–264. [CrossRef]
Manjunathachar, H.V.; Saravanan, B.C.; Kesavan, M.; Karthik, K.; Rathod, P.; Gopi, M.; Tamilmahan, P.; Balaraju, B.L. Economic importance of ticks and their effective control strategies. Asian Pac. J. Trop. Dis. 2014, 4, S770–S779. [CrossRef]
Bilkis, M.; Mondal, M.; Rony, S.; Islam, M.; Begum, N. Host determinant based prevalence of ticks and lice in cattle (Bos indicus) at Bogra district of Bangladesh. Prog. Agric 2011, 22, 65–73. [CrossRef]
Taye, D.R.; Assefa, K.; Hika, W. Prevalence of major ectoparasites of calves and associated risk factors in and around Bishoftu town. Afr. J. Agric. Res. 2015, 10, 1127–1135. [CrossRef]
Rehman, A.; Nijhof, A.M.; Sauter-Louis, C.; Schauer, B.; Staubach, C.; Conraths, F.J. Distribution of ticks infesting ruminants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan. Parasit. Vectors 2017, 10, 190. [CrossRef] [PubMed]
Da Silva, J.B.; Rangel, C.P.; De Azevedo Baêta, B.; Da Fonseca, A.H. Influence of the physiological state on infestation by Rhipicephalus microplus in dairy cows. Ticks Tick-Borne Dis. 2013, 4, 52–56. [CrossRef]
González, F.; Becerril, C.; Torres, G.; Díaz, P.; Santellano, E.; Rosendo, A. Infestación natural por Amblyomma cajennense y Boophilus microplus en bovinos criollo lechero tropical durante la epoca de lluvias. Agrociencia 2009, 43, 577–584.
Utech, K.B.W.; Wharton, R.H. Breeding for resistance to Boophilus microplus in Australian Illawarra Shorthorn and Brahman X Australian Illawarra Shorthorn cattle. Aust. Vet. J. 1982, 58, 41–46. [CrossRef] [PubMed]
Jonsson, N.N.; Mayer, D.G.; Green, P.E. Possible risk factors on queensland dairy farms for acaricide resistance in cattle tick (Boophilus microplus). Vet. Parasitol. 2000, 88, 79–92. [CrossRef]
Miyama, T.; Byaruhanga, J.; Okamura, I.; Uchida, L.; Muramatsu, Y.; Mwebembezi, W.; Vudriko, P.; Makita, K. Effect of chemical tick control effect of chemical tick control practices on tick infestation and Theileria parva infection in an intensive dairy production region of Uganda. Ticks Tick-Borne Dis. 2020, 11, 101438. [CrossRef]
Heath, A.C.G. Biology, Ecology and distribution of the tick, Haemaphysalis longicornis Neumann (Acari: Ixodidae) in New Zealand. N. Z. Vet. J. ISSN 2016, 64, 10–20. [CrossRef]
Zannou, O.M.; Ouedraogo, A.S.; Biguezoton, A.S.; Lempereur, L.; Patrick, K.; Emmanuel, Y.; Sébastien, A.; Lenaert, M.; Toe, P.; Farougou, S.; et al. First digital characterization of the transhumance corridors through benin used by cattle herds from Burkina Faso and associated risk scoring regarding the invasion of Rhipicephalus (Boophilus) microplus. Transbound. Emerg. Dis. 2021, 68, 2079–2093. [CrossRef]
Kamran, K.; Ali, A.; Villagra, C.A.; Bazai, Z.A.; Iqbal, A.; Sajid, M.S. Hyalomma Anatolicum resistance against ivermectin and fipronil is associated with indiscriminate use of acaricides in southwestern Balochistan, Pakistan. Parasitol. Res. 2021, 120, 15–25. [CrossRef] [PubMed]
Sánchez, A.; Vayas, T.; Mayorga, F.; Freire, C. Sector Ganadero: Análisis 2014–2019; Universidad Técnica de Ambato: Ambato, Ecuador, 2019; p. 5.
Banco Central del Ecuador, Reporte de coyuntura sector agropecuario. Dir. Nac. Sínt. Macroeconómica Gest. Coyunt. Previs. Económicas Diseño 2020, 93, 12.
Ruiz, F.Á.; Gz-Janica, H.L. Efectos Ambientales y Socio-Económicos del Sistema de Producción Ganadero con Enfoque Ambientalmente Sostenible y El Sistema Tradicional, Implementados en las Fincas Escocia y Alejandría, Respectivamente en el Municipio de Montería, Departamento de Córdob; Pontificia Universidad Javeriana: Bogotá, Colombia, 2012; p. 107.
Cingolani, A.M.; Noy-Meir, I.; Renison, D.D.; Cabido, M. La ganadería extensiva, ¿es compatible con la conservación de la biodiversidad y de los suelos? Ecol. Austral 2008, 18, 253–271.
Fawcett, T. An introduction to ROC analysis. Pattern Recognit. Lett. 2006, 27, 861–874. [CrossRef]
Swets, J. Measuring the accuracy of diagnostic systems. Science 1988, 240, 1285–1293. [CrossRef] [PubMed]
Reserva de Biósfera Chocó Andino de Pichincha. Available online: https://www.chocoandinopichincha.com (accessed on 23 September 2021).
Consejo Municial PVM. Caracterización Cantonal y Parroquial: Cantón Pedro Vicente Maldonado; Gobierno Provincial de Pichincha: Quito, Ecuador, 2011; pp. 165–182.
Echeverría, J. Conociendo Quito: El Noroccidente del DMQ, un territorio de alta biodiversidad, cultura y empredimientos sostenibles. Inst. Ciudad 2017, 1, 1–8.
HCPP. Proyecto de Desarrollo Rural Integral del Occidente de Pichincha-Fase II; Unidad de Desarrollo Integral: León, Mexico, 2000.
Cárdenas, J. Informe de educación ambiental EcoFondo-Napo. EcoFondo 2010, 7, 1–7.
Guamán, S.; Gonzáles, R.; Carrasco, R.; Guamán, F. Caracterización de los sistemas ganaderos de aptitud lechera en El Valle del Quijos, provincia del Napo, Ecuador. Eur. Sci. J. 2019, 15, 279–292. [CrossRef]
Epicollect, Epicollect 5. Imp. Coll. 2021. Available online: https://five.epicollect.net (accessed on 24 September 2021).
Wondatir Workie, Z.; Gibson, J.P.; van der Werf, J.H.J. Analysis of culling reasons and age at culling in australian dairy cattle. Anim. Prod. Sci. 2021, 61, 680. [CrossRef]
Zijlstra, J.; Jiayang, M.; Zhijun, C.; Van der Fels, B. Longevity and culling rate: How to improve? Available online: https://www.wur.nl/en/Publication-details.htm?publicationId=publication-way-353135313130 (accessed on 19 March 2022).
Ferguson, J.D.; Galligan, D.T.; Thomsen, N. Principal descriptors of body condition score in holstein cows. J. Dairy Sci. 1994, 77, 2695–2703. [CrossRef]
Hüe, T.; Fontfreyde, C. Development of a new approach of pasture management to control infestation. Trop. Anim. Health Prod. 2019, 51, 1989–1995. [CrossRef] [PubMed]
Guerrero, R. Las garrapatas de Venezuela (Acarina: Ixodoidea): Listado de especies y claves para su identificación. Bol Dir Malariol Saneam Ambient 1996, 36, 1–24.
Barros-Battesti, D.; Arzua, M.; Bechara, H. Carrapatos de Importância Médico-Veterinária da Região Neotropical: Um Guia Ilustrado Para Identificação de Espécies; University of São Paulo: São Paulo, Brazil, 2006; p. 223.
Venables, W.N.; Ripley, B.D. Modern Applied Statistics with S; Springer: Berlin/Heidelberg, Germany, 2002.
R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria; Available online: https://www.R-project.org/(accessed on 17 June 2021).
Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting linear mixed-effects models using Lme4. J. Stat. Softw. 2015, 67, 1–48. [CrossRef]
Petrie, A. Regclass: Tools for an Introductory Class in Regression and Modeling; Wiley-Black Well: Hoboken, NJ, USA, 2020.
Daoud, J.I. Multicollinearity and regression analysis. J. Phys. Conf. Ser. 2018, 949, 012009. [CrossRef]
Mandeville, P.B.; Concato, J. ¿Por qué se deben centrar las covariables en regresión lineal? Cienc. UANL 2008, XI, 300–305.
StataCorp. Stata statistical software: Release 14.2. College Station. 2015; Available online: https://www.stata.com/(accessed on 8 February 2022).
