Ectoparsites from Wild Animals Run Over on Brazilian Roads
Received Date: January 20, 2024 Accepted Date: February 20, 2024 Published Date: February 23, 2024
doi: 10.17303/javm.2024.3.102
Citation: Fernanda Cunha Boer, Dafner Alves de Araújo, Camylla Silva Pereira, Herbert Sousa Soares, Valeria Castilho Onofrio (2024) Ectoparsites from Wild Animals Run Over on Brazilian Roads. J Anim Biol Vet 3: 1-6
Abstract
Anthropization of natural habitats is one of the main causes of biodiversity loss, causing profound changes in these environments. Among these changes, one that generates an important environmental impact is the implementation of highways, which leads to deforestation and consequently an alteration of the natural landscape. The construction of highways generates direct impacts on wildlife, modifying the structure and dynamics of ecosystems. The running over of wild animals is the main cause of vertebrate mortality through human action. One of the reasons for the increase in demand for new roads is the growth of cities, resulting in severe ecological impacts and bringing wild animals closer to the man and domestic animals. The present study aimed to investigate the presence of ectoparasites in wild animals run over on highways in the State of São Paulo. Of 36 animal’s investigueted, 11 were infested with ectoparasites, ten were infested exclusively by ticks and one by ticks and lice. Almost all of the animals that presented ectoparasites were mammals, with the exception of one terrestrial bird. Ticks of the species Amblyomma dubitatum, Amblyomma nodosum, Amblyomma ovale, Amblyomma sculptum, Rhipicephalus microplus and a louse of the species Solenopotes binipilosus were collected
Keywords: Amblyomma; Rhipichephalus; Ticks; Lice; Wild Animals
Introduction
Human action in natural habitats is one of the main causes of biodiversity loss [1], significantly altering natural environments [2]. In tropical regions, there is a global loss of biodiversity due to human activities [3].
Among the activities that have a major impact on the natural environment, we have the implementation of highways as a major modifier, generating a change in the natural landscape due to deforestation. Approximately 85% of vegetation loss occurs within fifty kilometers of the highway limit [4].
Highways generate direct impacts on wildlife, modifying the structure and dynamics of these animals' ecosystems, such as, for example, an increase in collisions with vehicles during their natural movement processes [5]. The running over of wild animals is the main cause of vertebrate mortality through human action [6]. According to estimates by the Brazilian Center for Road Ecology, every year 475 million wild animals die on Brazilian roads.
Ectoparasites are arthropods belonging to the classes Arachnida and Insecta, and are represented by mites, ticks and some groups of insects. It has diverse eating habits and can parasitize mammals, birds, reptiles and amphibians. They can affect human and animal health by being vectors or intermediate hosts of several pathogens, in addition to causing dermatitis, damage to epithelial tissue, hypersensitivity and anemia due to their eating habits, such as hematophagy [7].
Currently, there are more than 950 species of ticks in the world, and in Brazil we have records of approximately 80 of them [8]. The Amblyomma genus is the one with the greatest diversity of species in the Neotropical Region and the one of greatest health concern, as it has species that are vectors of pathogenic agents, such as the bacterium Rickettsia rickettsii, which causes Brazilian Spotted Fever (SANGIONI et al, 2005).
Fleas are wingless insects belonging to the order Phthiraptera and are represented by around 5 thousand species worldwide. They are highly specific and obligate ectoparasites of birds and mammals. Some hematophagous species are capable of transmitting disease-causing pathogens [7].
Different studies related to the detection of pathogens transmitted by ectoparasites in wild animals, have already been carried out In Brazil. The objective of this study was to investigate the presence of ectoparasites in wild animals run over on Brazilian highways.
Materials and Methods
Samples of ectoparasites from 11 wild animals that were run over between 2021 and 2022 on the SP-225, SP-327 and SP-270 highways in the state of São Paulo, Brazil were investigated in this study. These samples were obtained through a donation by the company Via Fauna. All ticks were preserved in absolute ethanol until analyses.
The identification of ectoparasites was based on morphology using specific identification keys for each of the groups collected [9-12].
Results
Eleven wild animals were infested with ectoparasites, ten of these were infested exclusively by ticks and one by ticks and lice. Almost all of the animals that presented ectoparasites were mammals, with the exception of a terrestrial bird of the species Cariama cristata.
A total of 106 ticks were collected, 21 (19.8%) nymphs and 85 (80.2%) adults [46 (54.1%) males and 39 (45.9%) females]. Of these, 105 belong to the genus Amblyomma, of the species Amblyomma dubitatum (12), Amblyomma nodosum (26), Amblyomma ovale (1), Amblyomma sculptum (65), Amblyomma sp. (2) and a single specimen of the species Rhipicephalus microplus. Three specimens of lice of the species Solenopotes binipilosus were collected from Mazama sp. (Table 1).
The tick species A. sculptum was found parasitizing three Hidrochoerus hydrochaeris and a Myrmecophaga tridactyla. Mixed infestation by ticks of the species A. dubitatum and A. sculptum were recorded in two H. hydrochaeris, and infestation by A. nodosum and A. sculptum in a M. tridactyla.
Specimens of A. nodosum were collected in four Myrmecophaga tridactyla and one Tamandua tetradactyla, and only one female of A. ovale was collected on Procyon cancrivorus. A specimen of Mazama sp. was parasitized by ticks of the species R. microplus and by lice S. binipilosus. And in the only bird infested with ectoparasites, two tick nymphs of the genus Amblyomma were found (Table 1).
Discussion
In the present study, a total of five tick and a lice species were collected from roadkill wild animals. The ticks speceis A. sculptum was far the most abundant species, with 65 specimens (61.3 % of all ticks collected) collected from four individuals of two mammalian species.
Two of the three specimens of H. hydrochaeris examined were infested with A. dubitatum and A. sculptum and the third one only with A. sculptum. Although the capybara is considered the main host of A. dubitatum [13], in southeastern Brazil, infestation of these rodents with both tick species is relatively common [14,15]. Also in this region, high environmental infestations by A. sculptum are associated with the presence of horses and capybaras that are hosts of the adults of this tick [16,17].
One of the four specimens of M. tridactyla examined was parasitized by adults of A. nodosum and A. sculptum, and the number of specimens of the latter tick species exceeding more than seven times that of the former.
The finding of A. ovale in carnivores such as P. cancrivorus is not an unusual record, since the species has this group of mammals, mainly canids, as its preferred hosts [18]. The same for M. tridactyla and T. tetradactyla, from which specimens of A. nodosum were collected, and whose adult stage parasitizes almost exclusively this group of mammals [19-28].
A specimen of Mazama sp. was infested by R. microplus, a species of tick that parasitizes cattle [29], recorded the occurrence of the tick species R. microplus, D. nitens and A. sculptum parasitizing free-living M. gouazoubira in the state of Minas Gerais, Brazil.
In the same specimen of Mazama sp. which was parasitized by R. microplus, lice of the species S. binipilosus were found. Cervids are its usual hosts and its distribution is restricted to the American continent, occurring in North, Central and South America [30]. In South America, it was recorded in Argentina parasitizing M. gouazoubira and M. americana [31], in Chile on Pudu puda and Hippocamelus bisulcus [32,33] and in Peru on Odocoileus virginianus peruvianus [34].
In the same specimen of Mazama sp. which was parasitized by R. microplus, lice of the species S. binipilosus were found. Cervids are its usual hosts and its distribution is restricted to the American continent, occurring in North, Central and South America [30]. In South America, it was recorded in Argentina parasitizing M. gouazoubira and M. americana [31], in Chile on Pudu puda and Hippocamelus bisulcus [32,33] and in Peru on Odocoileus virginianus peruvianus [34].
Conclusions
Parasitism of ticks from domestic animals to wild animals was observed in this sudy, indicating that the latter are probably moving through areas where domestic animals are. Thus increasing the risk of transmission of agents between wild and domestic animals.
The results of this study reinforce the relevance of research into arthropod parasites of wild animals, and may even serve as an alert to the presence of ectoparasites that vector pathogenic agents, such as A. sculptum, found parasitizing capybaras and anteaters. In the ectoparasite samples analyzed, it was possible to observe the low specificity of A. sculptum in relation to its hosts.
Acknowledgments
We are grateful to the company Via Fauna for donating the ectoparasites samples investigated in this study.
- Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM et al. (2015) Accelerated human-induced losses of modern species: Entering the sixth mass extinction. Science Advances, 1: e1400253.
- Ficetola GF, Mazel F, Thuiller W (2017) Global determinants of zoogeographical boundaries. Nat Ecol Evol 1: 89.
- Gibbs HK et al. (2010) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. PNAS 107: 16732-7.
- Domingues MS, Bermann C, Sidneide MA (2014) Soy production in Brazil and its relationship with deforestation in the Amazon. Geographical Presence Magazine,1: 1.
- Peña AP, Drumond ME (1999) Survey of vertebrates killed by being run over on the GO-244 highway – Area of influence of the “Luiz Alves do Araguaia” irrigation project. Relatório.
- Costa AS (2014) Effect of temporal scales in defining highway impact mitigation measures. 74 f. Dissertation (Master's) - Postgraduate Course in Applied Ecology, Federal University of Lavras, Lavras.
- Guimarães JH, Tucci EC, Barros-Battesti DM (2001) Ectoparasites of Veterinary Importance. São Paulo: Plêiade/- FAPESP. 213: 218.
- Onofrio VC (2021) Ticks: should we worry about them? In.: Camila Lorenz, Flávia Virgínio, Gabriel C. Lima (Org.). Does Living In The Future Still Have The Climate For That? Global warming, its impacts and the arthropod revolution 66-70.
- Kim KC, Weisser CF (1974) Taxonomy of Solenopotes Enderlein, 1904, with redescription of Linognathus panamensis Ewing (Linognathidae: Anoplura). Parasitology, 69: 107-35.
- Barros-Battesti DM, Arzua M, Bechara HG (2006) Ticks of medical and veterinary importance in the Neotropics: an illustrated guide for species identification. São Paulo/BR: Vox /ICTTD-3/ Butantan, 223.
- Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key, Ticks and Tick-borne Diseases 1: 75-99.
- Dantas-Torres F, Martins TF, Muñoz-Leal S, Onofrio VC, Barros-Battesti DM (2019) Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: Updated species checklist and taxonomic keys. Ticks Tick Borne Diseases, 10: 101252.
- Nava S, Venzal JM, Labruna MB, Mastropaolo M, Gonzáles EM, Mangold AJ et al. (2010) Hosts, distribution and genetic divergence (16S rDNA) of Amblyomma dubitatum (Acari: Ixodidae). Experimental and Applied Acarology, 51: 2010.
- Heijden KM, Szabó MPJ, Egami MI, Campos Pereira M, Matushima ER (2005) Histopathology of tick-bite lesions in naturally infested capybaras (Hydrochoerus hydrochoeris) in Brazil. Experimental and Applied Acarology, 37: 245-55.
- Perez CA, Almeida AF, Almeida A, Carvalho VHB, Balestrin DC, Guimarães MS et al. (2008) Ticks of the genus Amblyomma (Acari: Ixodidae) and their relationships with hosts in an endemic area for Spotted Fever in the State of São Paulo. Brazilian Journal of Veterinary Parasitology, 17: 210-7.
- Labruna MB, Kerber CE, Ferreira F, Faccini JLH, De Waal DT et al. (2001) Risk factors to tick infestations and their occurrence on horses in the state of São Paulo, Brazil. Veterinary Parasitology, 97: 1-14.
- Pacheco RE, Horta MC, Moraesfilho J, Ataliba AC, Pinter A, Labruna MB (2007) Rickettsial infection in capybaras (Hydrochoerus hydrochaeris) from São Paulo, Brazil: serological evidence for infection by Rickettsia bellii and Rickettsia parkeri. Biomedica, 27: 364-71.
- Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK (2005) Ticks (Acari: Ixodida) on wild carnivores in Brazil. Experimental and Applied Acarology, 36: 149-63.
- Bechara GH, Szabó MPJ, Almeida WVFO, Bechara JN, Pereira RJG, Garcia JE et al. (2002) Ticks associated with armadillo (Euphractus sexcinctus) and anteater (Myrmecophaga tridactyla) of Emas National Park, State of Goias, Brazil. Ann N Y Acad Sci; 969: 290-3.
- Martins JR, Medri IM, Oliveira CM, Guglielmone AA (2004) Occurrence of ticks on giant anteater (Myrmecophaga tridactyla) and collared anteater (Tamandua tetradactyla) in the Pantanal region of Mato Grosso do Sul State, Brazil. Ciência Rural, 34: 293-5.
- Quadros RM, Benedet R, Mazzolli M, Marques SMT (2009) Amblyomma nodosum (Acari: Ixodidae) infesting collared anteater (Tamandua tetradactyla, Linnaeus, 1758) in Urupema, Santa Catarina. BIOCIÊNCIAS, Porto Alegre 17: 109-10.
- Garcia MV, Silva DC, Almeida RFC, Cunha RC, Matias J, Barros JC et al. (2013) Environmentally associated ticks (Acari: Ixodidae) in Campo Grande, Mato Grosso do Sul, Brazil. Revista Brasileira de Parasitologia Veterinária 22: 124-8.
- Martins TF, Venzal JM, Terassini FA, Costa FB, Marcili A, Camargo LMA et al. (2014) New tick records from the state of Rondônia, western Amazon, Brazil. Experimental and Applied Acarology, v. 62: 121-8.
- Soares HS, Barbieri AR, Martins TF, Minervino AH, De Lima JT (2015) Ticks and rickettsial infection in the wildlife of two regions of the Brazilian Amazon. Exp. Appl. Acarol. 65: 125e140.
- Witter R, Martins TF, Campos AK, Melo ALT, Correa SHR, Morgado TO et al. (2016) Rickettsial infection in ticks (Acari: Ixodidae) of wild animals in midwestern Brazil. Ticks and Tick-borne Diseases, 7: 415-23.
- Nascimento KKG, Veríssimo SMM, Raia VA, Guimarães RCS, Seade GCC, Azevedo ACP et al. (2017) Tick fauna of wild animals received and attended at the Santarém Zoological Park, western Pará State, Brazil. Ciencia Rural, 47: 20170159.
- Luz HR, Martins TF, Muñoz-Leal S, Costa FB, Gianizella SL, Faccini JL, Labruna MB (2020) Ticks from the Brazilian Amazon: Species, Distribution and Host-Relations. 34 p. In: Mikkola H. J. (Edt.). Ecosystem and Biodiversity of Amazonia. London: IntechOpen, 256: 2020.
- Martins TF, Reis JL, Viana EB, Luz HR, Oda FH,Dantas SP et al. (2020) Ticks (Acari: Ixodidae) on captive and free-ranging wild animals in Tocantins State, a Cerrado-Amazon transition region of northern Brazil. International Journal of Acarology 46: 254-7.
- Silveira JAG, Rabelo EML, Ribeiro MFB (2011) Detection of Theileria and Babesia in brown brocket deer (Mazama gouazoubira) and marsh deer (Blastocerus dichotomus) in the State of Minas Gerais, Brazil. Veterinary Parasitology 177: 61-6
- Durden LA, Musser GG (1994) The sucking lice (Insecta: Anoplura) of the world: A taxonomic checklist with records of mammalian hosts and geographical distributions. Bulletin of the American Museum of Natural History, 218: 1-90.
- Castro DC, Cicchino CA (1998) Anoplura. In: Biodiversity of Argentine arthropods, A biotaxonomic perspective, J. Morrone, S. Coscarón (eds.). Sur Editions: La Plata, Argentina, 125-43.
- González-Acuña D, DC Del Castro, L Moreno, E Mey (2004) First records of lice (Insecta: Phthiraptera) from wild southern pudu, Pudu puda (Mammalia: Artiodactyla: Cervidae). European Journal of Wildlife Research 50: 216-7.
- González-Acuña D, Saucedo GC, Corti P, Casanueva ME, Cicchino A (2009) First records of the louse Solenopotes binipilosus (Insecta: Phthiraptera) and the mite Psoroptes ovis (Arachnida: Acari) from wild southern huemul (Hippocamelus bisulcus). Journal of wildlife diseases, 45: 1235-8.
- Murga-Moreno CA, Ruiz-Pérez D, Rojas-Moncada J, Ortiz P, Sánchez L et al. (2023) Parasites in a wild white-- tailed deer in Cajamarca, Peru. Peruvian journal of biology 30: e26580-010.
- Silveira JAGEM, Rabelo L, Ribeiro MFB (2012) Molecular Detection of Tick-Borne Pathogens of the Family Anaplasmataceae in Brazilian Brown Brocket Deer (Mazama gouazoubira, Fischer, 1814) and Marsh Deer (Blastocerus dichotomus, Illiger, 1815). Transboundary and Emerging Diseases, 59: 353-60.
- Ficetola GF, Mazel F, Thuiller W (2017) Global determinants of zoogeographical boundaries. Nat Ecol Evol 1: 89.
