Unusual parasitism site of Dermacentor nitens (Acari: Ixodidae) on a horse

Abstract

Dermacentor nitens Neumann is the most common tick species infesting horses in the main Brazilian biomes. It has a predilection to attach to horse the ears, the nasal diverticulum, perineal and perianal regions. The infestations can generate severe damage in the ears, anemia, and the tick also acts as vector of Babesia caballi (Nuttall and Strickland), the causative agent of equine babesiosis. Our study describes unusual parasitism site of D. nitens on a female cross breed horse, approximately ten years old that presented high parasitism by ticks on the perineal and perianal region, ears, and the left eye orbit region, where an enucleation process had been performed a few years earlier. To our knowledge this is the first report of D. nitens parasitism on a formerly enucleated eye orbit.

Dermacentor nitens Neumann is the most common tick found parasitizing horses in the main Brazilian biomes, such as Amazon, Atlantic Forest, Cerrado (savannah), semiarid Caatinga, Pantanal (wetlands) (LABRUNA & FACCINI, 2020). This ixodid species became widely distributed in South America during the 20^th century through the movement and distribution of domestic equids (NAVA et al., 2017) and D. nitens has never been reported from a site without the presence of equids (LABRUNA & FACCINI, 2020).

Dermacentor nitens is a one-host ixodid tick, its parasitic phase on horses has an average duration of 25 days, the pre-oviposition period an average of 5 days and the average incubation period near 26 days, totaling a mean of 56 days of life cycle (RODRIGUES et al., 2017). Also, it presents a predilection for attaching to the ears of the hosts; however, depending on the degree of infestation, it can be found anywhere on the body, including the nasal diverticulum, the mane, tail, groin, and perineum region (LABRUNA et al., 2001, LABRUNA et al., 2002, RODRIGUES et al., 2017). D. nitens parasitism can result in health issues such as drop in hematological values for packed cell volume, lesions in the ears, resulting in permanent damage to cartilage, irritation, lower productivity, predisposition to secondary bacterial infections and screw-worm [Cochliomyia hominivorax (Coquerel)] infestations (LABRUNA & AMAKU, 2006). In addition, it has been implicated in the transmission of pathogenic agents to horses, being the confirmed vector of Babesia caballi (Nuttall and Strickland), one of the causative agents of equine piroplasmosis (ROBY & ANTHONY, 1963). The present study reported the presence of infestation by D. nitens in the formerly enucleated eye orbit of a horse from Goiás state, midwestern Brazil.

During the management and clinical evaluation of horses in the herd of Veterinary Teaching Hospital of the School of Veterinary and Animal Science of the Federal University of Goiás (UFG), located in Goiânia city (16º 40’ S, 49º 15’ W), Goiás State, midwestern Brazil, high parasitism by ticks was identified in the perineal and perianal regions, ears, and the left eye orbit, of an adult female cross breed horse of approximately ten years old, where an enucleation process had been performed two years earlier (Figure 1).

Sixteen specimens of ticks from the previously enucleated site, the left eye orbit, were collected with the aid of toothless anatomical tweezers. The collected ticks were preserved in absolute alcohol until taxonomic identification in the Laboratory of Parasitic Diseases (LADOPAR). Adult ticks, four males and 10 engorged females of Dermacentor nitens were identified following Barros-Battesti et al. (2006). Two nymphs of the genus Dermacentor were also identified, which, despite not having an identification key available to date, is likely to be Dermacentor nitens as this is the only species of the genus in the country (DANTAS-TORRES et al., 2009). All these ticks were deposited in the tick collection ‘Coleção Nacional de Carrapatos do Cerrado’ (CNCC) at the Veterinary and Animal Science School at the Federal University of Goiás under accession number (CNCC 032).

In Brazil, one of the tick species to which horses are frequently exposed is D. nitens (LABRUNA et al., 2001). In the animal of the present study, a high parasitic load was verified, and the only identified species was D. nitens, which is considered as potential vector of pathogens to horses, such as B. caballi (ROBY & ANTHONY, 1963). Unfortunately, samples of this animal were not collected and tested for the presence of any pathogens.

Aiming to reduce the risks of health issues and other losses associated with D. nitens parasitism, as mentioned previously, control strategies are necessary. The use of acaricides is still the predominant method in tick control; however, the indiscriminate use of these products combined with improper technical criteria contributes to the selection of resistant tick strains. The administration of these chemicals can also result in human and animal intoxication, as well as soil and water contamination (CHAGAS, 2004, BORGES et al., 2011). Control strategies of D. nitens are often applied jointly with the control of Amblyomma sculptum (Berlese) [published as Amblyomma cajennense (F.) until 2014], with the latter usually being the main target. However, due to different preferential attachment sites of these two tick species, the control strategy is frequently ineffective for D. nitens (BELLO et al., 2008). Furthermore, host-seeking larvae of D. nitens can be found in the pasture all year round; although quantities vary according to each season’s climatic characteristics (LABRUNA & FACCINI, 2020). Additionally, D. nitens presented up to five peaks of infestations on horses per year (LABRUNA et al., 2002) with corresponding peaks of host-seeking larvae in the pastures (LABRUNA & FACCINI, 2020). Thus, the knowledge about this species seasonal dynamics and behavior characteristics, in particular its preference for specific attachments sites is essential information supporting the formulation of an effective control strategy. The host reported in this study was part of a group of horses that had no pre-determined tick control strategies and was only subjected to acaracide application when infestations were notably high. Also, there were no recorded data on which acaricides were used nor the frequency and how they were applied. These factors present as potential contributors to the high load of D. nitens parasitism on the animal.

The main attachment sites of D. nitens on the horse head are the ears and the nasal diverticulum; although, high parasitism can also be found on the mane, perineal, perianal and groin regions (BORGES et al., 2000, LABRUNA et al., 2001, LABRUNA et al., 2002). Due to the predilection of D. nitens for feeding inside the ears, infestations at this location provide favorable conditions for infestations by C. hominivorax that commonly lead to permanent damage to the cartilage of the equine ears (LABRUNA et al., 2001, FRIEDHOFF et al., 1990, BORGES et al., 2000), and may also cause secondary infections (LABRUNA et al., 2001). The predilection of D. nitens to attach to shaded areas of the horse body have been reported (LABRUNA & AMAKU, 2006). This behavior might explain our usual finding of ticks attached to the left eye orbit of a horse, in which an enucleation process had been carried out, leaving the surface of the eye orbit irregular and concave. This further demonstrates the importance of the correct use of acaricide products, given the opportune presence of D. nitens on unusual anatomical areas of the horse body.

In the present study, the high degree of parasitism by D. nitens on a body site where the enucleation process had occurred indicates the need for further studies of the behavior of this species, to better understand its adaptability to the place where it was found. Additionally, this tick ability to adapt to regions of the host body with little to no exposure to sunlight demonstrates the importance of this behavior being considered while formulating and applying control strategies, thus ensuring the correct contact between acaracide and ticks. To our knowledge this is the first record of the presence of D. nitens on the eye orbit of a horse previously submitted to an enucleation process.

ACKNOWLEDGEMENTS

This Project was financed by the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) (202110267000287) and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and also was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil - Finance code 001.

References

BARROS-BATTESTI, D. M. et al. Carrapatos de importância médico-veterinária da Região Neotropical: um guia ilustrado para identificação de espécies. Vox/ICTTD-3/Butantan, São Paulo, 2006. Available from: <Available from: https://repositorio.butantan.gov.br/handle/butantan/3153 > Accessed: Oct. 27, 2022.

BELLO, A. C. P. P. et al. Controle de Anocentor nitens (Neumann, 1897) (Acari: Ixodidae) em equinos. Revista Brasileira de Parasitologia Veterinária, v.17, p.59-63, 2008. Available from: <Available from: http://www.redalyc.org/articulo.oa?id=397841469012 >. Accessed: Oct. 24, 2022.

BORGES, L. M. F. et al. Seasonal dynamics of Anocentor nitens on horses in Brazil. Veterinary Parasitology, v.89, p.165-171, 2000. Available from: <Available from: https://doi.org/10.1016/S0304-4017(00)00204-1 >. Accessed: Oct. 26, 2022.

BORGES, L. M. F. et al. Perspectives for the use of plant extracts to control the cattle tick Rhipicephalus (Boophilus) microplus Revista Brasileira de Parasitologia Veterinária, v.20, p.89-96, 2011. Available from: <Available from: https://doi.org/ 10.1590/S1984-29612011000200001 >. Accessed: Oct. 24, 2022.

CHAGAS, A. C. S. Controle de parasitas utilizando extratos vegetais. Revista Brasileira de Parasitologia Veterinária, v.13, p.156-160, 2004.

DANTAS-TORRES, F. et al. The ticks (Acari: Ixodida: Argasidae, Ixodidae) of Brazil. Systematic and Applied Acarology, v.14, p.30-46, 2009 Available from: <Available from: https://doi.org/10.11158/saa.14.1.4 >. Accessed: Oct. 25, 2022.

FRIEDHOFF, K. T. et al. Haemoparasites of equines: impact on international trade of horses. Revue Scientifique et Technique, v.9, p.1187-1194, 1990.

LABRUNA, M. B., AMAKU, M. Rhythm of engorgement and detachment of Anocentor nitens females feeding on horses. Veterinary Parasitology, v.137, p.316-332, 2006. Available from: <Available from: https://doi.org/10.1016/j.vetpar.2006.01.025 >. Accessed: Oct. 27, 2022.

LABRUNA, M. B., FACCINI, J. L. H. The nonparasitic phase of Dermacentor nitens under field conditions in southeastern Brazil. Revista Brasileira de Parasitologia Veterinária, v.29, p.1-12, 2020. Available from: <Available from: https://doi.org/10.1590/S1984-29612020090 >. Accessed: Oct. 25, 2022.

LABRUNA, M. B. et al. Risk factors to tick infestations and their occurrence on horses in the state of São Paulo, Brazil. Veterinary Parasitology, v.97, p.1-14, 2001. Available from: <Available from: https://doi.org/10.1016/s0304-4017(01)00387-9 >. Accessed: Oct. 24, 2022.

LABRUNA, M. B. et al. Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of São Paulo, Brazil. Veterinary Parasitology, v.105, p.65-77, 2002. Available from: <Available from: https://doi.org/10.1016/s0304-4017(01)00649-5 >. Accessed: Oct. 24, 2022.

NAVA, S. et al. Ticks of the Southern Cone of America: Diagnosis, Distribution, and Hosts with Taxonomy, Ecology and Sanitary Importance (Genera and Species of Ixodidae). Academic Press, London, 2017.

ROBY, T. O., ANTHONY, D. W. Transmission of equine piroplasmosis by Dermacentor nitens Neumann. Journal of the American Veterinary Medical Association, v.142, p.768-769, 1963.

RODRIGUES, V. S. et al. Life cycle and parasitic competence of Dermacentor nitens Neumann, 1897 (Acari: Ixodidae) on different animal species. Ticks and Tick Borne Diseases, v.8, p.379-384, 2017. Available from: <Available from: https://doi.org/10.1016/j.ttbdis.2016.12.014 >. Accessed: Oct. 25, 2022