Epidemiological factors associated with the distribution of Rickettsia hosts in Ucú, Yucatan, Mexico

Abigail Arroyo-Ramírez, César Lugo-Caballero, Enrique Reyes-Novelo, Henry Noh-Pech, Alejandro Rafael Suárez-Galaz, Jesús Alonso Panti-May, Roger Iván Rodríguez-Vivas, Tana Osorio-Primo, Hugo Ruiz-Piña, Marco Torres-Castro

Abstract


Background. Rickettsioses are zoonoses caused by pathogenic bacteria of the genus Rickettsia transmitted through bites or feces of ectoparasites (ticks, fleas, lice, and hematophagous mites). Rodents and dogs play a role in the transmission of pathogenic species. However, little is known about the factors associated with the chances of infections and their spatial distribution at the local scale. Objective. To determine the frequency of Rickettsia Spotted Fever group (SFG) and Typhus group (TG) in dogs and rodents, their spatial distribution, and the factors associated with the Rickettsia infection at the local scale. Methods. DNA was obtained from 64 dog blood samples and 36 rodent spleens from 48 dwellings in Ucú, Yucatan, Mexico. Rickettsia was determined by multiplex semi-nested PCR (snPCR). The predictor variables for infection in dogs and rodents were analyzed using generalized linear models (GLM) (p<0.05). Results. SnPCR revealed Rickettsia in 28.1 % (18/64, 95 % CI 17.6 %-40.8 %) of the dogs and 27.8 % (10/36, 95 % CI 14.2 %-45.2 %) of the rodents. Rickettsia SFG was detected in dogs; rodents hosted both Rickettsia TG and SFG. According to the corresponding GLM, dogs living in the interior area of Ucú had a lower chance of infection by Rickettsia SFG (OR = 0.14) than those living in the other regions. The presence of opossums (Didelphis spp.) in dwelling premises increases the chances of Rickettsia TG infection in rodents (OR = 14), and the presence of SFG-infected dogs in dwelling premises increases the chances of Rickettsia SFG infection in rodents (OR = 21). Implications. The spatial distribution of Rickettsia hosts was assessed at Ucú. The specific Rickettsia species were not identified, nor were the probable vectors evaluated. While the results provide a local overview, they do not accurately represent the epidemiological conditions at other sites. The information is valuable and should be considered in developing prevention measures for Rickettsiosis. Conclusions. Statistical modelling revealed that the spatial location of the dwelling, the presence of infected dogs, and the presence of opossums in the same dwelling serve as proxies for the Rickettsia infection in the captured rodents.

Keywords


dogs; Rickettsia infections; Rodentia; Siphonaptera; ticks; Vector-borne diseases.

Full Text:

PDF

References


Aguilar-Tipacamú, G., Torres-Castro, M., Sánchez-Montes, S. and Colunga-Salas, P., 2025. El impacto de la Rickettsiosis y la Borreliosis en la salud pública. Bioagrociencias, 18, pp. 82–89. https://doi.org/10.56369/BAC.6434

Álvarez-Hernández G., 2010. La Fiebre Manchada de las Montañas Rocosas, una epidemia olvidada. Salud Pública de México, 52, pp. 01–03.

Arroyave, E., Cornwell, E.R., McBride, J.W., Díaz, C.A., Labruna, M.B. and Rodas, J.D., 2020. Detection of tick-borne rickettsial pathogens in naturally infected dogs and dog-associated ticks in Medellin, Colombia. Revista Brasileira de Parasitologia Veterinária, 29, p. e005320. https://doi.org/10.1590/s1984-29612020060

Arroyo-Ramírez, A., Lugo-Caballero, C., Bolio-González, M., Rodríguez-Vivas, R.I., Reyes-Novelo, E., Panti-May, J.A. and Torres-Castro, M.A., 2022. El género Rickettsia y reportes de infección en perros de Yucatán, México. Bioagrociencias, 15, pp. 65–76. https://dx.doi.org/10.56369/BAC.4266

Arroyo-Ramírez, A., Lugo-Caballero, C., Panti-May, J.A., Reyes-Novelo, E., Rodríguez-Vivas, R.I., Noh-Pech, H., Suárez-Galaz, A., Osorio-Primo, T., Puerto, F.I., Dzul-Rosado, K. and Torres-Castro, M., 2023. An unusual identification of Rickettsia parkeri in synanthropic rodents and domiciliated dogs of a rural community from Yucatán, Mexico. Zoonoses and Public Health, 70, pp. 594–603. https://doi.org/10.1111/zph.13068

Beristain-Ruiz, D.M., Garza-Hernández, J.A., Figueroa-Millán, J.V., Lira-Amaya, J.J., Quezada-Casasola, A., Ordoñez-López, S., Laredo-Tiscareño, S.V., Alvarado-Robles, B., Castillo-Luna, O.R., Floriano-López, A., Hernández-Triana, L.M., Martínez-Ibáñez, F., Rivera-Barreno, R. and Rodríguez-Alarcón, C.A., 2022. Possible association between selected tick-borne pathogen prevalence and Rhipicephalus sanguineus sensu lato infestation in dogs from Juarez City (Chihuahua), northwest Mexico-US Border. Pathogens, 11, p. 552. https://doi.org/10.3390/pathogens11050552

Bermúdez, C.S.E. and Troyo, A., 2018. A review of the genus Rickettsia in Central America. Research and Reports in Tropical Medicine, 9, pp. 103–112. https://doi.org/10.2147/RRTM.S160951

Bezerra-Santos, M.A., Ramos, R.A.N., Campos, A.K., Dantas-Torres, F. and Otranto, D., 2021. Didelphis spp. opossums and their parasites in the Americas: A One Health perspective. Parasitology Research, 120, pp. 4091–4111. https://doi.org/10.1007/s00436-021-07072-4

Binder, L.C., Ramírez-Hernández, A., Serpa, M.C.A., Moraes-Filho, J., Pinter, A., Scinachi, C.A. and Labruna, M.B., 2021. Domestic dogs as amplifying hosts of Rickettsia rickettsii for Amblyomma aureolatum ticks. Ticks and Tick-Borne Diseases, 12, p. 101824. https://doi.org/10.1016/j.ttbdis.2021.101824

Carrasquilla M.C., Ortiz, M.I., Amórtegui-Hernández, D., García-Restrepo, S., León, C., Méndez-Cardona, S. and González, C., 2013. Pathogens, reservoirs, and vectors involved in the transmission of vector-borne and zoonotic diseases in a Colombian region. Brazilian Journal of Microbiology, 54, pp. 1145–1156. https://doi.org/10.1007/s42770-023-00903-9

Chiang, P.S., Su, S.W., Yang, S.L., Shu, P.Y., Lee, W.P., Li, S.Y. and Teng, H.J., 2022. Delayed correlation between the incidence rate of indigenous murine typhus in humans and the seropositive rate of Rickettsia typhi infection in small mammals in Taiwan from 2007-2019. PLoS Neglected Tropical Diseases, 16, p. e0010394. https://doi.org/10.1371/journal.pntd.0010394

Choi, Y.J., Jang, W.J., Kim, J.H., Ryu, J.S., Lee, S.H., Park, K.H., Paik, H.S., Koh, Y.S., Choi, M.S. and Kim, I.S., 2005. Spotted fever group and typhus group rickettsioses in humans, South Korea. Emerging Infectious Diseases, 11, pp. 237–244. https://doi.org/10.3201/eid1102.040603

Dzul-Rosado, K.R., Reyes-Novelo, E., Lugo-Caballero, C., Cuxim-Koyoc, A.D., Collí-Padrón, F., Tello-Martín, R., López-Ávila, K.B., Palma-Chan, A., Peniche-Lara, G. and Ruiz-Piña, H.A., 2021. Urban ecology of hosts and vectors of Rickettsia in a rickettsiosis-endemic city of the Yucatan peninsula, Mexico. Acta Tropica, 216, p. 105832. https://doi.org/10.1016/j.actatropica.2021.105832

Fernandes-Martins, T., Gea-Peres, M., Borges-Costa, F., Silva-Bacchiega, T., Michele-Appolinario, C., Azevedo de Paula-Antunes, J.M., Ferreira-Vicente, A., Megid, J. and Labruna, M.B., 2016. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Ciência Rural, 46, pp. 871–875. https://doi.org/10.1590/0103-8478cr20150671

Foley, J., Tinoco-Gracia, L., Rodriguez-Lomelí, M., Estrada-Guzmán, J., Fierro, M., Mattar-Lopez, E., Peterson, A., Pascoe, E., Gonzalez, Y., Hori-Oshima, S., Armstrong, P.A., Lopez, G., Jacome-Ibarra, M., Paddock, C.D. and Zazueta, O.E., 2019. Unbiased assessment of abundance of Rhipicephalus sanguineus sensu lato ticks, canine exposure to spotted fever group Rickettsia, and risk factors in Mexicali, México. American Journal of Tropical Medicine and Hygiene, 101, pp. 22–32. https://doi.org/10.4269/ajtmh.18-0878

Forshey, B.M., Stewart, A., Morrison, A.C., Gálvez, H., Rocha, C., Astete, H., Eza, D., Chen, H.W., Chao, C.C., Montgomery, J.M., Bentzel, D.E., Ching, W.M. and Kochel, T.J., 2010. Epidemiology of spotted fever group and typhus group rickettsial infection in the Amazon basin of Peru. American Journal of Tropical Medicine and Hygiene, 82, pp. 683–690. https://doi.org/10.4269/ajtmh.2010.09-0355

Instituto Nacional para el Federalismo y el Desarrollo Municipal (INAFED), 2021. Enciclopedia de los Municipios y Delegaciones (Ucú) 2021. Disponible en: https://www.inafed.gob.mx/work/enciclopedia/EMM31yucatan/municipios/31038a.html [Consultado 2025 marzo 31].

Katz, M.H., 2011. Multivariable Analysis: A Practical Guide for Clinicians and Public Health Researchers, 3rd Ed, Cambridge: Cambridge University Press.

Leulmi, H., Socolovschi, C., Laudisoit, A., Houemenou, G., Davoust, B., Bitam, I., Raoult, D. and Parola, P., 2014. Detection of Rickettsia felis, Rickettsia typhi, Bartonella species and Yersinia pestis in fleas (Siphonaptera) from Africa. PLoS Neglected Tropical Diseases, 8, p. e3152. https://doi.org/10.1371/journal.pntd.0003152

Lledó, L., Gegúndez, I., Ruiz, E., Rodríguez, L., Bacellar, F. and Saz, J.V., 2003. Rickettsia typhi infection in wild rodents from central Spain. Annals of Tropical Medicine and Parasitology, 9, pp. 411–414. https://doi.org/10.1179/000349803235002344

López-Pérez, A.M., Chaves, A., Sánchez-Montes, S., Foley, P., Uhart, M., Barrón-Rodríguez, J., Becker, I., Suzán, G. and Foley, J., 2022. Diversity of rickettsiae in domestic, synanthropic, and sylvatic mammals and their ectoparasites in a spotted fever-epidemic region at the western US-Mexico border. Transboundary Emerging Diseases, 69, pp. 609–622. https://doi.org/10.1111/tbed.14027

Lugo-Caballero, C., Torres-Castro, M., López-Ávila, K., Hernández-Betancourt, S., Noh-Pech, H., Tello-Martín, R., Puerto-Manzano, F. and Dzul-Rosado, K., 2021. Molecular identification of zoonotic Rickettsia species closely related to R. typhi, R. felis, & R. rickettsii in bats from Mexico. Indian Journal of Medical Research, 154, pp. 536-538. https://doi.org/10.4103/ijmr.IJMR_1083_19

Martínez-Ortiz, D., Torres-Castro, M., Koyoc-Cardeña, E., López, K., Panti-May, A., Rodríguez-Vivas, I., Puc, A., Dzul, K., Zavala-Castro, J., Medina-Barreiro, A., Chablé-Santos, J. and Manrique-Saide, P., 2016. Detección molecular de Rickettsia typhi en perros de una comunidad rural de Yucatán, México. Biomedica, 36, pp. 45-50. https://doi.org/10.7705/biomedica.v36i2.2913

Martínez-Ortiz, D., Torres-Castro, M., López-Ávila, K., Koyoc-Cardeña, E. and Manrique-Saide, P. 2019. Rickettsia spp. en garrapatas (Acari: Ixodidae) que infestan perros de una comunidad rural con antecedentes de rickettsiosis, Yucatán, México. Revista Biomédica, 30, pp. 43–50. https://doi.org/10.32776/revbiomed.v30i2.650

Milagres, B.S., Padilha, A.F., Montandon, C.E., Freitas, R.N., Pacheco, R., Walker, D.H., Labruna, M.B., Mafra, C.L. and Galvão, M.A., 2013. Spotted fever group Rickettsia in small rodents from areas of low endemicity for Brazilian spotted fever in the eastern region of Minas Gerais State, Brazil. American Journal of Tropical Medicine and Hygiene, 88, pp. 937–939. https://doi.org/10.4269/ajtmh.12-0609

Moraes-Filho, J., Costa, F.B., Gerardi, M., Soares, H.S. and Labruna, M.B., 2018. Rickettsia rickettsii co-feeding transmission among Amblyomma aureolatum ticks. Emerging Infectious Diseases, 24, pp. 2041–2048. https://doi.org/10.3201/eid2411.180451

Neves, L.C., Paula, W.V.F., de Paula, L.G.F., da Silva, B.B.F., Días, S.A., Pereira, B.G., Silva, B.S.A., Sevá, A.D.P., Dantas-Torres, F., Labruna, M.B. and Krawczak, F.D.S., 2023. Detection of Rickettsia spp. in animals and ticks in midwestern Brazil, where human cases of rickettsiosis were reported. Animals, 13, pp. 1288. https://doi.org/10.3390/ani13081288

Nicholson, W.L., Allen, K.E., McQuiston, J.H., Breitschwerdt, E.B. and Little, S.E., 2010. The increasing recognition of rickettsial pathogens in dogs and people. Trends in Parasitology, 26, pp. 205–212. https://doi.org/10.1016/j.pt.2010.01.007

Ojeda-Chi, M.M., Rodriguez-Vivas, R.I., Esteve-Gasent, M.D., Pérez de León, A.A., Modarelli, J.J. and Villegas-Perez, SL., 2019. Ehrlichia canis in dogs of Mexico: Prevalence, incidence, co-infection and factors associated. Comparative Immunology, Microbiology and Infectious Diseases, 67, p. 101351. https://doi.org/10.1016/j.cimid.2019.101351

Palacios-Santana, R., Wei, L., Fernandez-Santos, N.A., Rodriguez-Perez, M.A., Uriegas-Camargo, S., Mendell, N.L., Bouyer, D.H. and Estrada-Franco, J.G., 2023. Spotted fever and typhus group Rickettsiae in dogs and humans, Mexico, 2022. Emerging Infectious Diseases, 29, p. 1443–1446. https://doi.org/10.3201/eid2907.230333

Panti-May, J.A., Torres-Castro, M., Hernández-Betancourt, S., Dzul-Rosado, K., Zavala-Castro, J., López-Ávila, K. and Tello-Martín, R., 2015. Detection of Rickettsia felis in wild mammals from three municipalities in Yucatan, Mexico. Ecohealth, 12, pp. 523–527. https://doi.org/10.1007/s10393-014-1003-2

Panti-May, J.A., Hernández-Betancourt, S.F., Torres-Castro, M.A., Machaín-Williams, C., Cigarroa-Toledo, N., Sodá, L., López-Manzanero, G., Meza-Sulú, J.R. and Vidal-Martínez, V., 2016. Population characteristics of human-commensal rodents present in households from Mérida, Yucatán, México. MANTER: Journal of Parasite Biodiversity, 5, pp. 1–6. https://doi.org/10.13014/K2VD6WCX

Panti-May, J.A., Hernández-Betancourt, S.F., Torres-Castro, M.A., Parada-López, J., López-Manzanero, S. and Herrera-Meza, M.C., 2018. A population study of the house mouse, Mus musculus (Rodentia: Muridae), in a rural community of Mérida, México. Caribbean Naturalist, 46, pp. 1–13.

Peniche-Lara, G., Dzul-Rosado, K., Pérez-Osorio, C. and Zavala-Castro, J., 2015. Rickettsia typhi in rodents and R. felis in fleas in Yucatán as a possible causal agent of undefined febrile cases. Revista do Instituto de Medicina Tropical de São Paulo, 57, pp. 129–132. https://doi.org/10.1590/S0036-46652015000200005

R Core Team., 2024. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. 2024. https://www.R-project.org/

Reiczigel, J., Marozzi, M., Fábián, I. and Rózsa, L., 2019. Biostatistics for parasitologists -A primer to quantitative parasitology. Trends in Parasitology, 35, pp. 277–281. https://doi.org/10.1016/j.pt.2019.01.003

Reid, F.A., 2009. A field guide to the mammals of central America and southeast Mexico, 2nd Ed, New York: Oxford University Press.

Rodríguez-Vivas, R.I., Apanaskevich, D.A., Ojeda-Chi, M.M., Trinidad-Martínez, I., Reyes-Novelo, E., Esteve-Gassent, M.D. and De León, A.P., 2016. Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico. Veterinary Parasitology, 215, pp. 106–113. https://doi.org/10.1016/j.vetpar.2015.11.010

Rodríguez-Vivas, R.I., Flota-Burgos, G.J., Bolio-González, M.E., Rosado-Aguilar, J.A., Gutiérrez-Ruiz, E.J., Torres-Castro, M., Panti-May, A. and Reyes-Novelo, E., 2023. La garrapata café del perro, Rhipicephalus sanguineus: Biología y control. Vanguardia Veterinaria, May-April, pp. 10–16.

Rodríguez-Vivas, R.I., Flota-Burgos, G.J., Torres-Castro, M., Reyes-Novelo, E., Sánchez-Montes, S. and Colunga-Salas, P., 2024. Monthly fluctuation of parasitism by adult Ixodes keiransi ticks in dogs from Yucatán, Mexico. Veterinary Parasitology: Regional Studies and Reports, 53, p. 101077. https://doi.org/10.1016/j.vprsr.2024.101077

Rymaszewska, A. and Piotrowski, M., 2024. Rickettsia species: genetic variability, vectors, and Rickettsiosis-A review. Pathogens, 13, p. 661. https://doi.org/10.3390/pathogens13080661

Sánchez-Montes, S., Colunga-Salas, P., Lozano-Sardaneta, Y.N., Zazueta-Islas, H.M., Ballados-González, G.G., Salceda-Sánchez, B., Huerta-Jiménez, H., Torres-Castro, M., Panti-May, J.A., Peniche-Lara, G., Muñoz-García, C.I., Rendón-Franco, E., Ojeda-Chi, M.M., Rodríguez-Vivas, R.I., Zavala-Castro, J., Dzul-Rosado, K., Lugo-Caballero, C., Alcántara-Rodríguez, V.E., Delgado-de la Mora, J., Licona-Enríquez, J.D., Delgado-de la Mora, D., López-Pérez, A.M., Álvarez-Hernández, G., Tinoco-Gracia, L., Rodríguez-Lomelí, M., Ulloa-García, A., Blum-Domínguez, S., Tamay-Segovia, P., Aguilar-Tipacamú, G., Cruz-Romero, A., Romero-Salas, D., Martínez-Medina, M.A. and Becker I., 2021a. The genus Rickettsia in Mexico: Current knowledge and perspectives. Ticks and Tick-borne Diseases, 12, p. 101633. https://doi.org/10.1016/j.ttbdis.2020.101633

Sánchez-Montes, S., Salceda-Sánchez, B., Bermúdez, S.E., Aguilar-Tipacamú, G., Ballados-González, G.G., Huerta, H., Aguilar-Domínguez, M., Mora, J.D., Licona-Enríquez, J.D., Mora, D.D., López-Pérez, A.M., Torres-Castro, M.A., Alcántara-Rodríguez, V., Becker, I. and Colunga-Salas, P., 2021b. Rhipicephalus sanguineus complex in the Americas: systematic, genetic diversity, and geographic insights. Pathogens, 10, p. 1118. https://doi.org/10.3390/pathogens10091118

Santoyo-Colín, V., Sánchez-Montes, S., Salceda-Sánchez, B., Huerta-Jiménez, H., Alcántara-Rodríguez, V., Becker, I., Gual-Sill, F. and López-Pérez, A.M., 2021. Urban foci of murine typhus involving cat fleas (Ctenocephalides felis felis) collected from opossums in Mexico City. Zoonoses and Public Health, 68, pp. 1–7. https://doi.org/10.1111/zph.12770

Sosa-Gutiérrez, C.G., Vargas, M., Torres, J. and Gordillo-Pérez, G., 2014. Tick-borne rickettsial pathogens in rodents from Mexico. Journal of Biomedical Science and Engineering, 7, pp. 884–889. https://doi.org/10.4236/jbise.2014.711087

Suárez-Galaz, A., Reyes-Novelo, E., Cruz-Romero, A., Ramos-Vázquez, R., Panti-May, J.A., Ruiz-Piña, H., Sánchez-Montes, S. and Torres-Castro M., 2024. The relationship between the spatial occurrence of Leptospira exposed animals and the characteristics of the peridomiciles they inhabit in a locality if southeastern Mexico. Pathogens, 13, p. 1037. https://doi.org/10.3390/pathogens13121037

Szabó, M.P., Pinter, A. and Labruna, M.B., 2013. Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Frontiers in Cellular Infection Microbiology, 3, pp. 27. https://doi.org/10.3389/fcimb.2013.00027

Thrusfield, M., 2007. Veterinary epidemiology, 3rd. Ed, Oxford: Blackwell.

Torres-Castro, M., Martínez-Ortiz, D., Panti-May, A., Koyoc-Cardeña, E., López-Ávila, K., Dzul-Rosado, K., Zavala-Castro, J., Chablé-Santos, J. and Manrique-Saide, P., 2018. Rickettsia typhi in rodents from a community with history of murine typhus from Yucatan, Mexico. Revista MVZ Córdoba, 23, pp. 6974–6980. https://doi.org/10.21897/rmvz.1420

Torres-Castro, M., Reyes-Novelo, E., Noh-Pech, H., Tello-Martín, R., Lugo-Caballero, C., Dzul-Rosado, K., Puerto-Manzano, F. and Rodríguez-Vivas R.I., 2020. Personal and household factors involved in recent Rickettsia exposure in a rural population from Yucatán, Mexico. Zoonoses and Public Health, 67, pp. 506–515. https://doi.org/10.1111/zph.12714

Torres-Castro, M., Sánchez-Montes, S., Colunga-Salas, P., Noh-Pech, H., Reyes-Novelo, E. and Rodríguez-Vivas, R.I., 2022a. Molecular confirmation of Rickettsia parkeri in humans from Southern Mexico. Zoonoses and Public Health, 69, pp. 382–386. https://doi.org/10.1111/zph.12927

Torres-Castro, M., Reyes-Novelo, E., Noh-Pech, H., Sánchez-Montes, S., Colunga-Salas, P., Lugo-Caballero, C. and Rodríguez-Vivas, R.R., 2022b. Rickettsia rickettsii and Rickettsia typhi in inhabitants from a rural community of southeast Mexico. Revista Peruana de Medicina Experimental y Salud Pública, 39, pp. 124–125. https://doi.org/10.17843/rpmesp.2022.391.10519

Torres-Castro, M., Reyes-Novelo, E., Bolio-González, M., Lugo-Caballero, C., Dzul-Rosado, K., Colunga-Salas, P., Sánchez-Montes, S., Noh-Pech, H., Puerto, F.I. and Rodríguez-Vivas RI., 2022c. Epidemiological study of the occurrence of typhus group Rickettsia natural infection in domiciliated dogs from a rural community in south-eastern Mexico. Animals, 12, p. 2885. https://doi.org/10.3390/ani12202885

Torres-Castro, M., Reyes-Novelo, E., Arroyo-Ramírez, A., Lugo-Caballero, C., Panti-May, J.A. and Rodríguez-Vivas, R.I., 2024. Actualización sobre aspectos epidemiológicos de la rickettsiosis en el trópico de México. Tropical and Subtropical Agroecosystems, 27, pp. 048. https://dx.doi.org/10.56369/tsaes.4942

Vázquez-Guerrero, E., Reyes-Solís, G.C., Cano-Ravell, A.E., Machain-Williams, C., Leyva-Gastélum, M., Estrada-de Los Santos, P., Álvarez-Hernández, G. and Ibarra JA., 2023. Detection of Rickettsia amblyommatis and Rickettsia bellii in ticks collected from pet dogs in peri-urban and rural areas in Yucatan, Mexico. Experimental and Applied Acarology, 90, pp. 441–453. https://doi.org/10.1007/s10493-023-00825-z




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v28i3.63546

DOI: http://dx.doi.org/10.56369/tsaes.6354

Bookmark and Share


Copyright (c) 2025 Abigail Arroyo-Ramírez, César Lugo-Caballero, Enrique Reyes-Novelo, Marco Torres-Castro, Henry Noh-Pech, Alejandro Rafael Suárez-Galaz, Jesús Alonso Panti-May, Roger Iván Rodríguez-Vivas, Tana Osorio-Primo, Hugo Ruiz-Piña

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.