Therya_notes_NE6

THERYA NOTES 2024, Vol. 5 : 124-132 DOI: 10.12933/therya_notes-24-160 ISSN 2954-3614

New records of rodent hosts for hard ticks in tropical forests of Yucatán, México: Implications for tick-borne diseases in human-modified landscapes

Nuevos registros de roedores como hospederos de garrapatas en bosques tropicales de Yucatán, México: Implicaciones para las enfermedades transmitidas por garrapatas en paisajes modificados

Eduardo E. Palomo-Arjona1, César R. Rodríguez-Luna1, Martha P. Ibarra-López1,2, Mariel Aguilar-Domínguez3, Karla R. Dzul-Rosado4, and Carlos N. Ibarra-Cerdeña1*

1Departamento de Ecología Humana, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV) Unidad Mérida. Antigua carretera a Progreso km 6, C. P. 97310, Mérida. Yucatán, México. E-mail: eduardo.palomo@cinvestav.mx (EEP-A); cesar.rodriguez@cinvestav.mx (CRR-L); martha.ibarra@academicos.udg.mx (MPI-L); cibarra@cinvestav.mx (CNI-C).

2Departamento de Ecología y Recursos Naturales, Centro Universitario de la Costa Sur, Universidad de Guadalajara. Av. Independencia Nacional 151, C. P. 48900, Autlán. Jalisco, México.

3Laboratorio de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Veracruzana. Miguel Ángel de Quevedo s/n, C. P. 91710, Veracruz. Veracruz, México. E-mail: marieaguilar@uv.mx (MA-D).

4Laboratorio de Enfermedades Emergentes y Re Emergentes, Centro de Investigaciones Regionales Dr. Hideyo Noguchi, Universidad Autónoma de Yucatán. Avenida Itzáes 490 x 59, C. P. 97000, Mérida. Yucatán, México. E-mail: karla.dzul@correo.uady.mx (KRD-R).

*Corresponding author

Rodents serve as reservoirs for up to 85 zoonotic diseases, some of which can be transmitted by ticks. Ticks of the Amblyomma and Ixodes genera have been recognized to be associated with 4 rodent species in the Yucatán Peninsula, México. Here, we present new records of rodents acting as hosts for ticks of these genera in tropical forests of Yucatán. Between June 2021–March 2022, Sherman traps were used for rodent capture in the Biocultural State Reserve of Puuc, Yucatán, México. Twelve quadrants with 50 traps each were established in tropical forest sites with varying levels of anthropogenic intervention. Rodents were inspected for ectoparasites, and ticks were collected using entomological forceps and preserved in 70 % ethanol. We captured 160 individuals of 6 rodent species in 5,400 trap nights. The most captured species were Heteromys gaumeri (n = 60) and Sigmodon toltecus (n = 44), while the least represented were Handleyomys rostratus (n = 1). We retrieved 492 ticks, identifying Amblyomma mixtum, parasitizing H. rostratus, H. gaumeri, and S. toltecus; Ixodes cf. Ixodes affinis parasitizing H. gaumeri and Ixodes sp. parasitizing S. toltecus. We reported, for the first time in México, H. rostratus and S. toltecus as hosts for Amblyomma mixtum. Additionally, we present the first record of Ixodes affinis parasitizing H. gaumeri and Ixodes sp. parasitizing S. toltecus in the Yucatán Peninsula. The presence of tick vectors of zoonotic pathogens among rodent reservoirs reflects a latent risk to humans and domestic animals in the region.

Key words: Amblyomma mixtum; ectoparasite; Ixodes; Maya Forest; pathogens; small mammals; vectors; zoonoses.

Los roedores son reservorios de hasta 85 patógenos zoonóticos, algunos transmitidos por garrapatas. En la Península de Yucatán, México, garrapatas de los géneros Amblyomma e Ixodes están asociadas a 4 especies de roedores. Aquí presentamos nuevos registros de roedores hospederos para garrapatas de estos géneros en Yucatán. Entre junio 2021–marzo 2022, se utilizaron trampas Sherman para la captura de roedores en la Reserva Estatal Biocultural del Puuc, Yucatán, México. Se establecieron 12 cuadrantes de 50 trampas en sitios con diferente nivel de intervención antrópica. Los roedores fueron inspeccionados por ectoparásitos y las garrapatas fueron colectadas usando pinzas entomológicas y preservadas en etanol al 70 %. Capturamos 160 individuos de 6 especies de roedores en 5,400 noches/trampa. Las especies más capturadas fueron Heteromys gaumeri (n = 60) y Sigmodon toltecus (n = 44), y la menos representada fue Handleyomys rostratus (n = 1). Recuperamos 492 garrapatas identificando a Amblyomma mixtum, parasitando a H. rostratus, H. gaumeri y S. toltecus; Ixodes cf. Ixodes affinis, parasitando a H. gaumeri e Ixodes sp. parasitando a S. toltecus. Reportamos, por primera vez en México, a H. rostratus y S. toltecus como hospederos de garrapatas de Amblyomma mixtum, y el primer registro de Ixodes cf. Ixodes affinis en H. gaumeri e Ixodes sp. en S. toltecus en la Península de Yucatán. La presencia de garrapatas vectores de patógenos zoonóticos entre roedores reservorios refleja el riesgo latente de propagación de enfermedades hacia el ser humano y sus animales domésticos en la región.

Palabras clave: Amblyomma; ectoparásito; Ixodes; patógenos; pequeños mamíferos; Selva Maya; vectores; zoonosis.

Rodents constitute the most diverse and abundant order of mammals globally, with at least 2,680 species grouped into 35 families and 535 genera (Burgin et al. 2018; ASM 2023). This group of organisms is involved in the highest number of zoonoses compared to any other order of terrestrial mammals, as approximately 10 % of rodent species can harbor and transmit various zoonotic pathogens of public health significance (Han et al. 2015; Rabiee et al. 2018). Worldwide, it is estimated that 244 rodent species can act as reservoirs or hosts for up to 85 zoonotic diseases. In the case of the Americas, specifically in the Neotropical region, 130 rodent species, from 56 genera and 12 families, have been identified as confirmed reservoirs or hosts for 31 zoonoses caused by viruses, bacteria, helminths, and protozoa (Han et al. 2016; Rabiee et al. 2018; Ibarra-Cerdeña et al. 2024).

The transmission of zoonotic diseases can occur through direct or indirect pathways. Direct transmission occurs through contact with the saliva, feces, or urine of rodents or by consuming contaminated water or food (Meerburg et al. 2009; Battersby 2015). On the other hand, indirect transmission occurs through the bite of arthropod ectoparasite vectors (i.e., mites, ticks, fleas), which previously fed on the blood of infected rodents (Meerburg et al. 2009; Himsworth et al. 2013; Selmi et al. 2021). Zoonotic diseases with the highest number of rodent hosts are precisely those transmitted indirectly by vectors (Ibarra-Cerdeña et al. 2024).

Ticks (Acari: Ixodidae) are hematophagous ectoparasites of terrestrial vertebrates that constitute the second most important group of vectors in the transmission of diseases to humans worldwide, second only to mosquitoes (de la Fuente et al. 2008). Diseases transmitted by ticks associated with rodents include Crimean-Congo hemorrhagic fever (Földes et al. 2019), caused by viruses; rickettsioses (Sosa-Gutiérrez et al. 2016; Helminiak et al. 2022), Lyme disease (Krawczyk et al. 2020), anaplasmosis (Clark 2012), bartonellosis (Silaghi et al. 2016; Schulte Fischedick et al. 2016), Q fever, and tularemia (Bártová et al. 2020), all bacterial infections; and babesiosis (Obiegala et al. 2015), caused by protozoa.

In México, on the Yucatán Peninsula, comprising the states of Campeche, Quintana Roo, and Yucatán, 2 genera of ticks have been recorded on 4 rodent species (Light et al. 2020). Amblyomma ticks (Koch, 1844) have been found parasitizing Gaumer's spiny pocket mouse (Heteromys gaumeri Allen and Chapman, 1897) in the state of Yucatán (Guzmán-Cornejo et al. 2011). On the other hand, Ixodes ticks (Latreille, 1795) have been found on the big-eared climbing rat (Ototylomys phyllotis Merriam, 1901) and the Yucatán deer mouse (Peromyscus yucatanicus Allen and Chapman, 1897) in the state of Yucatán (Hoffmann et al. 1989; Whitaker and Morales-Malacara 2005) and in Campeche on Gaumer's spiny pocket mouse and the Toltec cotton rat (Sigmodon toltecus Saussure, 1860; Ceballos 2014; Light et al. 2020). However, knowledge about the ectoparasites associated with the 15 species of small rodents distributed across different habitat types in the Yucatán Peninsula region (Zaragoza-Quintana et al. 2016) is still limited. Therefore, our objective in this study was to present new records of rodents acting as hosts for ticks in the tropical forests of Yucatán.

The study was conducted in the central part of the protected area known as the Biocultural State Reserve of Puuc, in the southwestern region of Yucatán, with coordinates ranging from 19° 51' 33.92” – 20° 23' 24.16” N, and 89° 10' 30.42” – 89° 52' 30.12” W (Figure 1). The reserve covers an area of 1,358.49 km² and includes portions of the municipalities of Muna, Santa Elena, Oxkutzcab, Tekax, and Ticul (DOF 2011; INEGI 2017). The main types of vegetation include deciduous lowland forest, deciduous midland forest, and semi-deciduous midland forest (Rzedowski 2006; Essens and Hernández-Stefanoni 2013). These vegetation types are characterized by 50–70 % of tree species losing their foliage during the dry season, from November to April (Flores-Guido and Espejel-Carvajal 1994). The landscape consists of a mosaic of patches of the main vegetation types in different successional stages (anthropogenic impact) following traditional agricultural use (Dupuy et al. 2012). The climate in the study area is tropical subhumid with summer rainfall (Aw1), with an average annual temperature of 26 °C and annual precipitation ranging between 900–1100 mm (Flores-Guido and Espejel-Carvajal 1994; Orellana et al. 2009).

Between June 2021 and March 2022, Sherman box traps (Tallahassee, Florida) baited with a mixture of oat flakes and vanilla (Krebs 2006) were used for rodent capture in the study area (Figure 1). Three habitat types with different levels of anthropogenic intervention were considered, including mature/conserved forest, secondary/regenerative forest (without human intervention for ≥ 30 years), and agricultural crop sites. In each habitat type, 4 quadrants of 5 x 10 traps were established, with a separation of 10 m between them. Each quadrant was active for 3 consecutive nights during 3 sampling seasons: humid (October-November), sub-humid (June-July) and dry (February-March).

Captured rodents were identified using specialized keys (Reid 2009; Álvarez-Castañeda et al. 2017). As part of an alternate study focused on detection of zoonotic pathogens (bacteria and viruses), captured rodents were anesthetized with isoflurane (Sofloran Vet©) and euthanized by either cervical dislocation or overdose of sodium pentobarbital (Pisabental©) via intracardiac injection (AVMA 2020).

During anesthesia, sex, age, reproductive condition, and conventional body measurements (weight, total length, length of tail, foot, and ear) were obtained for each captured individual (Panti-May et al. 2012). Additionally, captured rodents were inspected for ectoparasites. Ticks were removed and collected using fine-tipped entomological forceps and preserved in 70 % ethanol. In the laboratory, we classified the life stage of collected ticks and identified adult individuals following the specialized taxonomic keys of Dantas-Torres et al. (2019), Guzmán-Cornejo et al. (2019), and Nava et al. (2019). Subsequently, we calculated the mean intensity of infection (MI) for each rodent species, defined as the total number of a tick species divided by the number of infected hosts, and the tick infestation prevalence as the proportion of infected hosts, with one or more individuals of a particular tick species, divided by the number of examined hosts and multiplied by 100 to express it as a percentage (Bush et al. 1997).

The rodent hosts specimens and their parasites were deposited in the Mammal (CINMMC 404–564) and Parasite collections (CINMPC 1404–1564), respectively, of the Departamento de Ecología Humana of the Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV) Unidad Mérida (Yucatán, México).

During the physical containment and manipulation of organisms, we followed the guidelines of the American Society of Mammalogists for the use of wild mammals in research and education (Sikes et al. 2016) and the procedure indicated by the American Veterinary Medical Association (Underwood et al. 2013; AVMA 2020). Specimen collections were done under collecting permit number SGPA/DGVS/3941/19, issued by the General Direction of Wildlife of México under the name of C. N. Ibarra-Cerdeña.

We achieved a sampling effort of 5,400 trap nights and captured 160 rodents, representing 3 families, 6 genera, and 6 species (Table 1). The most frequently captured rodent was Gaumer's spiny pocket mouse (H. gaumeri, n = 60), followed by the Toltec cotton rat (S. toltecus, n = 44), the big-eared climbing rat (O. phyllotis, n = 27), and the house mouse (Mus musculus, n = 26). The least represented species were the pygmy rice rat (Oligoryzomys fulvescens, n = 2) and the big-eared harvest mouse (Handleyomys rostratus, n = 1). Considering the habitat type, farmland sites accounted for 56.9 % (n = 91) of captures, followed by preserved forest sites (23.1 %, n = 37), and secondary forest (20.0 %, n = 32). The species H. rostratus was only present in preserved forest, while M. musculus was only captured in farmland sites. On the other hand, H. gaumeri and S. toltecus were present in all habitat categories, although the highest number of S. toltecus captures (n = 41) occurred in farmland sites (Table 1).

We collected 492 ticks from the 160 captured rodents. In 3 rodent species, we only recovered (n = 91) ticks in immature stages: M. musculus, O. fulvescens, and O. phyllotis. No nymph-stage ticks were found, and larvae represented 89 % (n = 438) of all the collections. The infestation by larvae was found in all 6 species of captured rodents and the prevalence of tick larvae infection in rodents was 58.8 % (Table 1). The highest prevalence values were for O. fulvescens and H. rostratus (100 %, both), followed for S. toltecus (84.1 %), H. gaumeri (56.7 %), and O. phyllotis (55.6 %). Meanwhile the lowest prevalence value was for M. musculus (19.2 %). The 3 species with the highest mean intensity of infection were S. toltecus (MI = 5.7), O. phyllotis (MI = 5.5), and H. gaumeri (MI = 4.0; Table 1).

On the other hand, the adult ticks, all females, represented 11 % (n = 54) of all the collections. Among adult ticks, we identified A. mixtum (n = 17), parasitizing H. rostratus, H. gaumeri, and S. toltecus; and Ixodes cf. Ixodes affinis (n = 37), parasitizing H. gaumeri and Ixodes sp. parasitizing S. toltecus (Figure 2). The infection prevalence for A. mixtum was 100 % for H. rostratus, 13.6 % for S. toltecus, and 8.3 % for H. gaumeri; for Ixodes ticks, the prevalence was 27.3 % for S. toltecus and 10.0 % for H. gaumeri (Table 1). The mean intensity of infection by ticks of A. mixtum was MI = 1.5 for S. toltecus, MI = 1.4 for H. gaumeri, and MI = 1.0 for H. rostratus. Meanwhile, the mean intensity by ticks of Ixodes sp. was MI = 2.6 for S. toltecus and Ixodes cf. Ixodes affinis MI = 1.0 for H. gaumeri (Table 1).

According to the habitat condition, no pattern was found regarding the prevalence of tick infestation in any of the stages (Table 2). However, the mean intensity of infection observed in A. mixtum for H. gaumeri (MI = 3.0) and Ixodes sp. for S. toltecus (MI = 2.6) were higher when compared with preserved and secondary forests. Mean intensity of infection, considering larval ticks, showed that the higher value occurred in regenerative forests for O. phyllotis (MI = 7.0) as well as in farmland for S. toltecus (MI = 6.0; Table 2). On the other hand, no apparent pattern was found that related tick infestation according to seasonal variation (Table 3).

The presence of Amblyomma ticks on Heteromys gaumeri has been previously documented in the state of Yucatán at the genus level, but the species was not identified (Guzmán-Cornejo et al. 2011; Light et al. 2020). In this study, we identified the species Amblyomma mixtum on H. gaumeri, and for the first time, we report the genus Amblyomma for H. rostratus and S. toltecus, specifically identifying Amblyomma mixtum on these species as well. Amblyomma mixtum is a generalist tick species widely distributed throughout North América and northern South América (Aguilar-Domínguez et al. 2021). Other Amblyomma species collected from rodents in Yucatán include Amblyomma maculatum, previously documented on the agouti (Cuniculus paca; Arana-Guardia et al. 2015) and in Handleyomys in Tabasco (Light et al. 2020). These ticks are also known to feed on dogs, equines, opossum and bovines (Rodríguez-Vivas et al. 2016; Dzul-Rosado et al. 2021; García-Rejón et al. 2021). Additionally, Amblyomma inornatum has been reported on Sigmodon rodents in Durango and Guerrero (Light et al. 2020) and on various wildlife species in the state of Yucatán (Arana-Guardia et al. 2015; García-Rejón et al. 2021; López‐Pérez et al. 2022).

Amblyomma ticks are important vectors of pathogens of zoonotic diseases as carriers of bacteria of the genera Anaplasma, Ehrlichia, and Rickettsia (Trout-Fryxell et al. 2017; Rochlin and Toledo 2020; Lippi et al. 2021). In Yucatán, Rickettsia felis has been reported in 6 rodent species, including H. gaumeri and S. toltecus (Panti-May et al. 2015). The first reports of human cases of spotted fever attributed to R. felis were diagnosed in Yucatán (Zavala-Velazquez et al. 2000). Similarly, wildlife with tick infestations has been found to be infected with rickettsias in various municipalities of Yucatán (Ojeda-Chi et al. 2019; Canto-Osorio et al. 2020).

In the case of Ixodes ticks, our findings represent the first records of these ticks in Yucatán, identifying 2 species: Ixodes cf. Ixodes affinis on H. gaumeri and an unidentified species, Ixodes sp., on S. toltecus. Within the Yucatán Peninsula, the presence of the genera Ixodes has been previously recognized in both host species only in the state of Campeche (Ceballos 2014; Light et al. 2020). In México, Ixodes eadsi and Ixodes sinaloa have been reported parasitizing rodents of the family Heteromyidae (Guzmán-Cornejo et al. 2023), and Ixodes minor has been reported on rodents of the genus Sigmodon (Light et al. 2020).

Ixodes ticks are known to harbor pathogens of the genera Anaplasma, Borrelia, Ehrlichia, Coxiella, Babesia, and Rickettsia (Biggs et al. 2016; Rochlin and Toledo 2020; Moraga-Fernández et al. 2023). Notably, Ixodes cf. Ixodes affinis, the tick species we collected on H. gaumeri, has been found infected with Rickettsia sp. cf. Rickettsia monacensis on a white-tailed deer in Campeche, México. This bacterium is a member of the Spotted Fever Group described in the Old World and is considered pathogenic to humans (Sánchez-Montes et al. 2021). In another study, Ixodes affinis was found infected with a Rickettsia endosymbiont on a hunting dog (Dzul-Rosado et al. 2023). These 2 studies highlight the significance of Ixodes cf. Ixodes affinis as a vector of Rickettsia, with the potential to amplify the transmission of disease agents between different hosts at the wildlife-domestic interface in human-modified landscapes.

Additionally, rodents harbor several bacteria that use ticks as vectors. In the Yucatán Peninsula, Borrelia burgdorferi s.l., the etiological agent of Lyme disease, has been reported in several rodent species: in the state of Quintana Roo, it has been described in H. gaumeri (Rodríguez-Rojas et al. 2020), and in Yucatán, in synanthropic species M. musculus and the black rat (Rattus rattus; Solís-Hernández et al. 2016). In Yucatán, cases of babesiosis in children attributed to Babesia microti have been detected (Peniche-Lara et al. 2018), whose competent reservoir is the white-footed mouse (Peromyscus leucopus; Hersh et al. 2012), a species native to the Yucatán Peninsula (Zaragoza-Quintana et al. 2016).

In the present study, tick infestation in the larval stage was observed in all 6 host rodent species. Small mammals are considered an important group for feeding tick larvae (Lindsø et al. 2023), as larvae commonly feed on wild rodents, unlike adult ticks that tend to prefer larger mammals (Paziewska et al. 2010; Esser et al. 2016). Additionally, the contribution of pathogens from rodents to the infection of larvae has been documented. For instance, in Europe, it was found that 89.0 % of Ixodes ricinus larvae infected with Borrelia burgdorferi s.l. had fed on rodents (Hofmeester et al. 2016).

Land use change was related to a higher mean intensity of infection for A. mixtum and larvae. Ticks are susceptible to the climatic conditions of their habitat, although susceptibility to temperature and desiccation can vary according to species and stage (Needham and Teel 1991). Ticks of the genus Ixodes, such as Ixodes scapularis, have low tolerance to desiccation and tend to be more present in forested habitats and thickets with dense vegetation. In contrast, Amblyomma americanum has generalist habits that allow it to occupy grassland habitats and environments subject to human disturbance (Diuk-Wasser et al. 2021; Mathisson et al. 2021).

The specificity patterns of each tick species could explain the higher intensity of infection by A. mixtum in disturbed habitats and the lower infestation by Ixodes. Immature stage ticks, like larvae, feed opportunistically (Esser et al. 2016). Therefore, we attribute the high mean intensity of infection found in this host to the high dominance and competitiveness of Sigmodon rats in farmlands (Cruz et al. 2010), as well as their higher capture rate in these conditions.

The variability in tick infestation according to seasonality appears to be influenced by the specificity of each species and the stage of the ticks. We recognize that an annual sampling design, coupled with more detailed identification of individuals (Randolph 1975; Kollars et al. 2000), could provide more robust results and clarify the specific patterns of each group, as well as the relationships between hosts.

Our results represent the first record of H. rostratus and S. toltecus as hosts of any Amblyomma species in México, and the first report of any Ixodes species on H. gaumeri and S. toltecus in the Yucatán Peninsula. The presence of vector ticks and the circulation of zoonotic pathogens among reservoir rodents reflect a latent risk of disease spread to humans and domestic animals in the region, making it a significant public and animal health concern. This risk may be exacerbated by the fact that both H. gaumeri and S. toltecus are predominantly found in human-modified landscapes, inhabiting agricultural areas and even rural households and backyards associated with secondary forests, where contact between rodent ectoparasites and humans is possible (Cimé-Pool et al. 2007; López-Cancino et al. 2015; Peniche-Lara et al. 2015; Panti-May et al. 2015, 2018; Canché-Pool et al. 2022).

Acknowledgements

This work was partially funded by the SEP-CINVESTAV project (FIDSC2018/160) "Análisis de los efectos de la deforestación y la defaunación selectiva en la transmisión de parásitos en ambientes tropicales". The first authors (EEP-A and CRR-L) thank CONAHCYT for the graduate and postdoctoral scholarships (777072 and I1200/320/2022, respectively). Special thanks to R. Espinal for help with the illustrative material, to J. Callaghan, director of the Kaxil Kiuic Biocultural Reserve, for facilitating access to the study sites, and to A. Uc-Santos for his help during the monitoring of rodents. We are grateful to S. E. Bermúdez C. from Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Ciudad de Panamá, Panamá, for help with tick species identification. Two anonymous reviewers helped to improve earlier versions of this note.

Literature cited

Aguilar-Domínguez, M., et al. 2021. Potential distribution of Amblyomma mixtum (Koch, 1844) in climate change scenarios in the Americas. Ticks and Tick-borne Diseases 12:101812.

Álvarez-Castañeda, S. T., T. Álvarez, and N. González-Ruiz. 2017. Keys for identifying Mexican mammals. Pandora Impresores. Jalisco, México.

American Society of Mammalogists (ASM). 2023. Mammal Diversity Database (Version 1.12.1) [Data set]. Zenodo. https://doi.org/10.5281/zenodo.10595931. Accessed on May 12, 2024.

American Veterinary Medical Association (AVMA). 2020. Guidelines for the euthanasia of animals: 2020 Edition. https://www.avma.org/sites/default/files/2020-02/Guidelines-on-Euthanasia-2020.pdf. Accessed on September 20, 2021.

Arana-Guardia, R., et al. 2015. Ticks (Acari: Ixodidae) from wild mammals in fragmented environments in the south of Yucatán Peninsula, México. Southwestern Entomologist 40:657–660.

Bártová, E., et al. 2020. Coxiella burnetii and Francisella tularensis in wild small mammals from the Czech Republic. Ticks and Tick-borne Diseases 11:101350.

Battersby, S. A. 2015. Rodents as carriers of disease. Pp. 81–100 in Rodent pests and their control (Buckle, A., and R. Smith, eds.). CABI International. Wallingford, United Kingdom.

Biggs, H. M., et al. 2016. Diagnosis and management of tickborne rickettsial diseases: Rocky Mountain spotted fever and other spotted fever group rickettsioses, ehrlichioses, and anaplasmosis—United States. Morbidity and Mortality Weekly Report: Recommendations and Reports 65:1–44.

Burgin, C. J., et al. 2018. How many species of mammals are there? Journal of Mammalogy 99:1–14.

Bush, A. O., et al. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83:575–583.

Canché-Pool, E. B., et al. 2022. Cutaneous leishmaniasis emergence in southeastern Mexico: The case of the state of Yucatan. Tropical Medicine and Infectious Disease 7:444.

Canto-Osorio, J. M., et al. 2020. Ectoparasites of Didelphis virginiana from Yucatan, Mexico. Journal of Medical Entomology 57:1821-1829.

Ceballos, G. 2014. Mammals of México. Johns Hopkins University Press. Baltimore, U.S.A.

Cimé-Pool, J., et al. 2007. Comunidad de pequeños roedores en una milpa tradicional del centro de Yucatán, México. Revista Mexicana de Mastozoología (Nueva Época) 11:57–68.

Clark, K. L. 2012. Anaplasma phagocytophilum in small mammals and ticks in northeast Florida. Journal of Vector Ecology 37:262–268.

Cruz, L. E., et al. 2010. Interspecific variability in the abundance of small rodents in the highlands of Chiapas, Mexico. Therya 1:129–135.

Dantas-Torres, F., et al. 2019. Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: Updated species checklist and taxonomic keys. Ticks and Tick-borne Diseases 10:101252.

de la Fuente, J., et al. 2008. Overview: ticks as vectors of pathogens that cause disease in humans and animals. Frontiers in Bioscience 13:6938–6946.

Diario Oficial del Gobierno del Estado de Yucatán. (DOF). 2011. Decreto Número 455. Gobierno del Estado. Poder Ejecutivo. https://www.Yucatán.gob.mx/docs/diario_oficial/diarios/2011/2011-11-01.pdf. Accessed on February 11, 2023.

Diuk-Wasser, M. A., et al. 2021. Impact of land use changes and habitat fragmentation on the eco-epidemiology of tick-borne diseases. Journal of Medical Entomology 58:1546–1564.

Dupuy, J. M., et al. 2012. Patterns and correlates of tropical dry forest structure and composition in a highly replicated chronosequence in Yucatán, México. Biotropica 44:151–162.

Dzul-Rosado, K. R., et al. 2021. Urban ecology of hosts and vectors of Rickettsia in a rickettsiosis-endemic city of the Yucatan peninsula, Mexico. Acta Tropica 216:105832.

Dzul-Rosado, K. R., et al. 2023. Tick-associated diseases identified from hunting dogs during the COVID-19 pandemic in a Mayan community in Yucatan, Mexico. Open Veterinary Journal 13:794–800.

Essens, T., and J. L. Hernández-Stefanoni. 2013. Mapping Lepidoptera and plant alpha-diversity across a heterogeneous tropical dry forest using field and remotely sensed data with spatial interpolation. Journal of Insect Conservation 17:725–736.

Esser, H. J., et al. 2016. Host body size and the diversity of tick assemblages on neotropical vertebrates. International Journal for Parasitology: Parasites and wildlife 5:295–304.

Flores-Guido, J. S., and I. Espejel-Carvajal. 1994. Tipos de vegetación de la Península de Yucatán. Etnoflora Yucatánense, Fascículo 3. Universidad Autónoma de Yucatán. Mérida, México.

Földes, F., et al. 2019. Serologic survey of the Crimean-Congo haemorrhagic fever virus infection among wild rodents in Hungary. Ticks and Tick-borne Diseases 10:101258.

García-Rejón, J. E., et al. 2021. Identification of parasitic arthropods collected from domestic and wild animals in Yucatán, México. Annals of Parasitology 67:647–658.

Guzmán-Cornejo, C., et al. 2011. The Amblyomma (Acari: Ixodida: Ixodidae) of México: identification keys, distribution and hosts. Zootaxa 2998:16–38.

Guzmán-Cornejo, C., et al. 2019. The soft ticks (Parasitiformes: Ixodida: Argasidae) of Mexico: Species, hosts, and geographical distribution. Zootaxa 4623:485–525.

Guzmán-Cornejo, C., et al. 2023. Actualización de la riqueza de garrapatas de los géneros Ixodes y Amblyomma (Ixodida: Ixodidae) en México. Dugesiana 30:163–176.

Han, B. A., et al. 2015. Rodent reservoirs of future zoonotic diseases. Proceedings of the National Academy of Sciences 112:7039–7044.

Han, B. A., A. M. Kramer, and J. M. Drake. 2016. Global patterns of zoonotic disease in mammals. Trends in Parasitology 32:565–577.

Helminiak, L., et al. 2022. Pathogenicity and virulence of Rickettsia. Virulence 13:1752–1771.

Hersh, M. H., et al. 2012. Reservoir competence of wildlife host species for Babesia microti. Emerging Infectious Diseases 18:1951–1957.

Himsworth, C. G., et al. 2013. Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector-Borne and Zoonotic Diseases 13:349–359.

Hoffmann, A., M. Ojeda, and G. López. 1989. Los ectosimbiontes de Peromyscus difficilis (J. A. Allen, 1891) (Rodentia: Cricetidae). Revista de la Sociedad Mexicana de Historia Natural 40:49–58.

Hofmeester, T. R., et al. 2016. Few vertebrate species dominate the Borrelia burgdorferi sl life cycle. Environmental Research Letters 11:043001.

Ibarra-Cerdeña, C. N., et al. 2024. Rodents as key hosts of zoonotic pathogens and parasites in the Neotropics. Pp. 143–184 in Ecology of wildlife diseases in the Neotropics (Acosta-Jamett, G., and A. Chaves, eds.). Springer Nature. Cham, Swiss.

Instituto Nacional de Estadística y Geografía (INEGI). 2017. Anuario estadístico y geográfico de Yucatán 2017. https://www.inegi.org.mx/app/biblioteca/ficha.html?upc=702825095116. Accessed on February 12, 2023.

Kollars, Jr, T. M., et al. 2000. Host associations and seasonal activity of Amblyomma americanum (Acari: Ixodidae) in Missouri. Journal of Parasitology 86:1156–1159.

Krawczyk, A. I., et al. 2020. Effect of rodent density on tick and tick-borne pathogen populations: consequences for infectious disease risk. Parasites and Vectors 13:34.

Krebs, C. J. 2006. Mammals. Pp. 351–369 in Ecological census techniques. A handbook. (Sutherland, W. J. ed.). Cambridge University Press. New York, U.S.A.

Light, J. E., et al. 2020. Checklist of ectoparasites of cricetid and heteromyid rodents in México. Therya 11:79–136.

Lindsø, L. K., et al. 2023. Individual heterogeneity in ixodid tick infestation and prevalence of Borrelia burgdorferi sensu lato in a northern community of small mammalian hosts. Oecologia 203:421–433.

Lippi, C. A., et al. 2021. Scoping review of distribution models for selected Amblyomma ticks and rickettsial group pathogens. PeerJ 9:e10596.

López-Cancino, S. A., et al. 2015. Landscape ecology of Trypanosoma cruzi in the southern Yucatan Peninsula. Acta Tropica 151:58-72.

López‐Pérez, A. M., et al. 2022. Spatial distribution patterns of tick community structure in sympatric jaguars (Panthera onca) and pumas (Puma concolor) from three ecoregions in México. Medical and Veterinary Entomology 36:371–380.

Mathisson, D. C., et al. 2021. Effect of vegetation on the abundance of tick vectors in the northeastern United States: a review of the literature. Journal of Medical Entomology 58:2030–2037.

Meerburg, B. G., G. R. Singleton, and A. Kijlstra. 2009. Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35:221–270.

Moraga-Fernández, A., et al. 2023. Exploring the diversity of tick-borne pathogens: The case of bacteria (Anaplasma, Rickettsia, Coxiella and Borrelia) protozoa (Babesia and Theileria) and viruses (Orthonairovirus, tick-borne encephalitis virus and louping ill virus) in the European continent. Veterinary Microbiology 286:109892.

Nava, S., et al. 2019. Guía para la identificación de las principales especies de garrapatas que parasitan a los bovinos en la provincia de Entre Ríos, Argentina. Ediciones INTA. Buenos Aires, Argentina.

Needham, G. R., and P. D. Teel. 1991. Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36:659–681.

Obiegala, A., et al. 2015. Molecular examinations of Babesia microti in rodents and rodent-attached ticks from urban and sylvatic habitats in Germany. Ticks and Tick-borne Diseases 6:445–449.

Ojeda-Chi, M. M., et al. 2019. Molecular detection of rickettsial tick-borne agents in white-tailed deer (Odocoileus virginianus yucatanensis), mazama deer (Mazama temama), and the ticks they host in Yucatán, México. Ticks and Tick-borne Diseases 10:365–370.

Orellana, R., et al. 2009. Atlas: Escenarios de cambio climático en la Península de Yucatán. Centro de Investigación Científica de Yucatán. Mérida, México.

Panti-May, J. A., et al. 2012. Abundance and population parameters of commensal rodents present in rural households in Yucatan, Mexico. International Biodeterioration and Biodegradation 66:77–81.

Panti-May, J. A., et al. 2015. Detection of Rickettsia felis in wild mammals from three municipalities in Yucatán, México. Ecohealth 12:523–527.

Panti-May, J. A., et al. 2018. Características poblaciones de Rattus rattus y Mus musculus presentes en comunidades rurales de Yucatán, México. Tropical and Subtropical Agroecosystems 21:345–356.

Paziewska, A., et al. 2010. Utilization of rodent species by larvae and nymphs of hard ticks (Ixodidae) in two habitats in NE Poland. Experimental and Applied Acarology 50:79–91.

Peniche-Lara, G., et al. 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 57:129–132.

Peniche-Lara, G., et al. 2018. Human Babesiosis, Yucatán State, México, 2015. Emerging Infectious Diseases 24:2061–2062.

Rabiee, M. H., et al. 2018. Rodent-borne diseases and their public health importance in Iran. PLoS Neglected Tropical Diseases 12:e0006256.

Randolph, S. E. 1975. Seasonal dynamics of a host-parasite system: Ixodes trianguliceps (Acarina: Ixodidae) and its small mammal hosts. The Journal of Animal Ecology 44:425–449.

Reid, F. A. 2009. A field guide to the mammals of Central America and Southeast Mexico. Oxford University Press. New York, U.S.A.

Rochlin, I., and A. Toledo. 2020. Emerging tick-borne pathogens of public health importance: a mini-review. Journal of Medical Microbiology 69:781–791.

Rodríguez-Rojas, J. J., et al. 2020. Molecular detection of Leptospira interrogans and Borrelia burgdorferi in wild rodents from México. Vector-Borne and Zoonotic Diseases 20:860–863.

Rodríguez-Vivas, R. I., et al. 2016. Ticks collected from humans, domestic animals, and wildlife in Yucatán, México. Veterinary Parasitology 215:106–113.

Rzedowski, J. 2006. Vegetación de México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. México City, México.

Sánchez-Montes, S., et al. 2021. Molecular detection of Rickettsia sp. cf. Rickettsia monacensis in Ixodes sp. cf. Ixodes affinis collected from white-tailed deer in Campeche, Mexico. Parasitology Research 120:1891-1895.

Selmi, R., et al. 2021. Zoonotic vector-borne bacteria in wild rodents and associated ectoparasites from Tunisia. Infection, Genetics and Evolution 95:105039.

Schulte Fischedick, F. B., et al. 2016. Identification of Bartonella species isolated from rodents from Yucatan, Mexico, and isolation of Bartonella vinsonii subsp. yucatanensis subsp. nov. Vector-Borne and Zoonotic Diseases 16:636-642.

Sikes, R. S., and Animal Care and Use Committee of the American Society of Mammalogists. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688.

Silaghi, C., et al. 2016. Bartonella, rodents, fleas and ticks: a molecular field study on host-vector-pathogen associations in Saxony, Eastern Germany. Microbial Ecology 72:965–974.

Solís-Hernández, A., et al. 2016. Prevalence of Borrelia burgdorferi sensu lato in synanthropic rodents in two rural communities of Yucatán, México. Biomédica 36:109–117.

Sosa-Gutiérrez, C. G. et al. 2016. Tick-borne rickettsial pathogens in questing ticks, removed from humans and animals in México. Journal of Veterinary Science 17:353–360.

Trout-Fryxell, R. T., et al. 2017. Investigating the adult ixodid tick populations and their associated Anaplasma, Ehrlichia, and Rickettsia bacteria at a Rocky Mountain spotted fever hotspot in Western Tennessee. Vector-Borne and Zoonotic Diseases 17:527–538.

Underwood, W., et al. 2013. AVMA guidelines for the euthanasia of animals: 2013 edition. American Veterinary Medical Association. Illinois, U.S.A.

Whitaker, J. O., and J. B. Morales-Malacara. 2005. Ectoparasites and other associates (ectodytes) of mammals of México. Pp. 535–666 in Contribuciones mastozoológicas en homenaje a Bernardo Villa (Sánchez-Cordero, V., and R. A. Medellín, eds.). Instituto de Biología, UNAM/Instituto de Ecología, UNAM/CONABIO. México City, México.

Zaragoza-Quintana, E. P., et al. 2016. Los pequeños roedores de la Península de Yucatán: conocimiento y perspectivas en 114 años de investigación. Therya 7:299–314.

Zavala-Velázquez, J. E., et al. 2000. Rickettsia felis rickettsiosis in Yucatán. The Lancet 356:1079-1080.

Associated editor: Gloria Tapia Ramírez.

Submitted: March 7, 2024; Reviewed: May 26, 2024.

Accepted: May 28, 2024; Published on line: June 7, 2024.

Table 3. Prevalence and mean intensity of tick (Acari: Ixodidae) infestation in rodents according to habitat seasonality in tropical forests of southern Yucatán, México. The prevalence value, calculated as prevalence = (n/N) * 100, is expressed as a percentage and denoted in parentheses.

Season	Species	Captured (N)	Number of individuals infested (n) by ticks (prevalence %)			Mean intensity of infection (MI)
Season	Species	Captured (N)	Larvae	Amblyomma mixtum	Ixodes	Larvae	Amblyomma mixtum	Ixodes
Humid (Oct–Nov)	Heteromys gaumeri	17	14 (82.4)	1 (5.8)	2 (11.7)	2.2	1.0	1.0
	Handleyomys rostratus	-	-	-	-	-	-	-
	Oligoryzomys fulvescens	2	2 (100)	-	-	1.5	-	-
	Sigmodon toltecus	10	8 (80.0)	4 (40.0)	1 (10.0)	6.0	1.3	1.0
	Ototylomys phyllotis	8	4 (50.0)	-	-	1.5	-	-
	Mus musculus	4	1 (25.0)	-	-	1.0	-	-
Sub-humid (Jun–Jul)	Heteromys gaumeri	20	5 (25.0)	1 (5.0)	2 (10.0)	8.8	1.0	1.0
	Handleyomys rostratus	-	-	-	-	-	-	-
	Oligoryzomys fulvescens	-	-	-	-	-	-	-
	Sigmodon toltecus	17	15 (88.2)	-	9 (52.9)	4.4	-	3.0
	Ototylomys phyllotis	6	5 (83.3)	-	-	10.2	-	-
	Mus musculus	18	5 (27.8)	-	-	1.0	-	-
Dry (Feb–Mar)	Heteromys gaumeri	23	15 (65.2)	3 (13.0)	2 (8.7)	4.1	1.7	1.0
	Handleyomys rostratus	1	1 (100)	1 (100)	-	2.0	1.0	-
	Oligoryzomys fulvescens	-	-	-	-	-	-	-
	Sigmodon toltecus	17	14 (82.4)	2 (11.7)	2 (11.7)	6.8	2.0	1.5
	Ototylomys phyllotis	13	6 (46.2)	-	-	4.3	-	-
	Mus musculus	4	2 (50.0)	-	-	1.0	-	-

Family	Species	Tropical forest condition			Total (N)	Number of individuals infested (n) by ticks (prevalence %)			Mean intensity of infection (MI)
Family	Species	Preserved	Regenerative	Farmland	Total (N)	Larvae	Amblyomma mixtum	Ixodes	Larvae	Amblyomma mixtum	Ixodes
Heteromyidae	Heteromys gaumeri	23	14	23	60	34 (56.7)	5 (8.3)	6 (10.0)+	4.0	1.4	1.0
Cricetidae	Handleyomys rostratus	1	-	-	1	1 (100)	1 (100)*	-	2.0	1.0	-
	Oligoryzomys fulvescens	-	1	1	2	2 (100)	-	-	1.5	-	-
	Sigmodon toltecus	1	2	41	44	37 (84.1)	6 (13.6)*	13 (29.5)+	5.7	1.5	2.6
	Ototylomys phyllotis	12	15	-	27	15 (55.6)	-	-	5.5	-	-
Muridae	Mus musculus	-	-	26	26	5 (19.2)	-	-	1.0	-	-