Five species of ticks belonging to the genera Amblyomma, Haemaphysalis and Rhipicephalus were recorded from endemic and exotic wild mammals in the Esteros del Iberá wetlands, Argentina. Adults and immature stages of Amblyomma dubitatum were found on Hydrochoerus hydrochaeris, Sus scrofa, Axis axis and Myrmecophaga tridactyla. Larvae and nymphs of A. dubitatum were collected on Bubalus bubalis, Lepus europaeus, Monodelphis dimidiata and on the rodents Cavia aperea, Scapteromys aquaticus, Oligoryzomys flavescens and Akodon azarae. One male of Amblyomma nodosum was associated with M. tridactyla; specimens of Haemaphysalis juxtakochi were found on A. axis, S. scrofa and Mazama gouazoubira; and Rhipicephalus (Boophilus) microplus was detected on Blastocerus dichotomus. Adults of Amblyomma triste were collected on B. dichotomus, S. scrofa and H. hydrochaeris, while immatures of this tick were recorded on M. dimidiata, A. azarae, S. aquaticus, O. flavescens and H. hydrochaeris. In addition to elucidating tick-host associations, the findings of this survey are biomedically important. Although the tick fauna of Esteros del Iberá is limited, some species, such as A. triste and R. (B.) microplus, are recognized vectors of pathogenic agents infecting humans and animals. Also, a large number of the Esteros del Iberá collection records were for ticks from exotic (S. scrofa, A. axis, B. bubalis, L. europaeus) or reintroduced (M. tridactyla) mammals, suggesting that the introduction of these mammals may result in the amplification of tick populations in the study area, with potential deleterious effects on the endemic fauna.
Taxonomic knowledge of the parasitic arthropods associated with a particular host community is fundamental to studies of the influence of these parasites on host ecology and to attempts to evaluate their potential as vectors of infectious diseases. From a biomedical standpoint, ticks are among the most important parasitic arthropods (Hoogstraal 1985; Jongejan & Uilenberg 2004)—they are hematophagous ectoparasites of terrestrial tetrapods whose role as vectors of animal and human pathogens is widely recognized (Sonenshine and Mather 1994; Jongejan and Uilenberg 2004). About 198 species of ticks belonging to the families Argasidae (soft ticks) and Ixodidae (hard ticks) occur in the Neotropical Zoogeographic Region (Guglielmone et al. 2003; Nava et al. 2009, 2010b), and many of these are potential vectors of pathogens to mammals (Guglielmone et al. 2003).
The Esteros del Iberá is a large wetland complex spanning over 13,000 km2 in the Argentinean province of Corrientes (Canziani et al. 2003). This macrosystem is one of the most important wetlands in South America, and it is a multiple-use protected area (Loiselle et al. 2002; Canziani et al. 2003). More than 40 endemic mammal species (some at risk of extinction) and nine exotic species of mammals have been recorded in the Esteros del Iberá (Fabri et al. 2003). However, studies of ticks associated with the mammals of the Esteros del Iberá have been few (Ivancovich & Luciani 1992; Nava et al. 2010a, 2011). Consequently, the objective of this research was to produce an inventory of the ticks that infest endemic and exotic wild mammals in the Esteros del Iberá wetlands, in order to provide baseline information on tick-host specificity and the potential risk of tick-borne diseases in this area.
Materials and methods
Esteros del Iberá is located in Corrientes Province, Argentina (Fig. 1). This area comprises a complex of ecosystems, chief among them swamps and marshlands that connect an extensive system of shallow lakes (Neiff & Poi de Neiff 2006). Water inputs to the Esteros del Iberá are primarily through rainfall, the historic mean total being 1500 mm, with summer rains somewhat greater (600–700 mm) than during the rest of the year (Neiff & Poi de Neiff 2006). Masses of floating vegetation, known locally as “embalsados,” are common throughout the lagoons, where Schoenoplectus californicus(C.A. Meyer) Soják, Thypha spp., Fuirena robusta Kunth and Cyperus giganteus Vahl are the dominant wetland plants (Neiff et al. 2011). Terrestrial habitats are principally characterized by shrubland forests and temporarily flooded grasslands.
Information on tick-host associations for Esteros del Iberá was obtained from the serial scientific literature, from unpublished records of ticks deposited in the tick collection of INTA Rafaela, and by sampling endemic and exotic mammals in the study area. Mammals belonging to the orders Artiodactyla, Cingulata, Didelphimorphia, Lagomorpha, Pilosa and Rodentia were examined for ticks. Rodents of the subfamilies Sigmodontinae (Cricetidae) and Caviinae (Caviidae) and small marsupials (Didelphimorphia: Didelphidae) were captured using four linear grids, each equipped with 50 Sherman live traps (24 cm long, 9 cm high, 8 cm wide) set at 5-m intervals baited with food pellets and seeds, and one linear trapping grid equipped with 50 Tomahawk live traps (32 cm long, 10 cm high, 10 cm wide) set at 5-m intervals baited with carrots. Rodents and marsupials were processed according to the methodology described by Nava et al. (2006), and sigmodontines were determined with the collaboration of U.F.J. Pardiñas (Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Puerto Madryn, Argentina). Large mammals, such as Hydrochoerus hydrochaeris (Linnaeus, 1766) (Rodentia: Caviidae), Axis axis (Erxleben, 1777) (Artiodactyla: Cervidae), Sus scrofa Linnaeus, 1758 (Artiodactyla: Suidae) and Lepus europaeus Pallas, 1778 (Lagomorpha: Leporidae), were taken by shotgun. Specimens of A. axis, S. scrofa and L. europaeus were sacrificed in the context of a control program for exotic species, while specimens of H. hydrochaeris were captured with permission of the Dirección de Recursos Naturales of Corrientes Province during a program to limit overpopulation. Ticks were collected on specimens of Myrmecophaga tridactyla Linnaeus, 1758 (Pilosa: Myrmecophagidae) and Blastocerus dichotomus (Illiger, 1815) (Artiodactyla: Cervidae) during health examination of these mammals. Specimens of Cingulata (Dasypodidae) were captured by hand, checked for ticks, and released. Ticks attached to road-killed animals were also included in the analysis. Tick determinations were based on Joan (1930), Guglielmone and Viñabal (1994), Estrada-Peña et al.(2005), Barros-Battesti et al. (2006) and Martins et al. (2010), and by comparison of field-collected ticks with known laboratory-reared material housed in the tick collection of INTA Rafaela.
Males (MM), females (FF), nymphs (NN) and larvae (LL) of five tick species belonging to the genera Amblyomma, Haemaphysalis and Rhipicephalus were found parasitizing wild mammals in Esteros del Iberá. Ticks were collected from specimens of the orders Artiodactyla, Didelphimorphia, Lagomorpha, Pilosa and Rodentia, but not from Cingulata (Dasypus novemcinctus Linnaeus, 1758and Euphractus sexcinctus (Linnaeus, 1758)). Results are as follows:
1) Amblyomma dubitatum Neumann, 1899
Estancia “Ayuí” (28º37´S 57°32´W) 38MM 67FF 56NN ex H. hydrochaeris (Ivancovich & Luciani 1992)1; Estancia “Juan Ángel” (28°41′S 57°08′W) 20MM 8FF 1N ex H. hydrochaeris (Ivancovich & Luciani 1992); Estancia “Palmita” (28°46′S 57°48′W) 8MM 3FF 15NN ex H. hydrochaeris (Ivancovich & Luciani 1992); Laguna del Iberá (28°32′S 57°10′W) 20MM 37FF 5NN ex H. hydrochaeris (Ivancovich & Luciani 1992); 30 km SW of Colonia Carlos Pellegrini (28°40′S 57°26′W) MM FF NN LL (Number undetermined (NU)) ex H. hydrochaeris (Nava et al. 2010a); Estancia “Rincón del Socorro” (28°42′S 57°29′W) 4 NN ex S. scrofa, MM FF (NU) ex S. scrofa (Nava et al. 2010a). New records: Reserva Provincial Iberá (28°30′S 58°00′W) 1N ex Bubalus bubalis (Linnaeus, 1758); 37 km SW of Colonia Carlos Pellegrini (28°42′S 57°27′W) 37LL ex Scapteromys aquaticus Thomas, 1920, 3LL ex Cavia aperea Erxleben, 1777, 1N ex C. aperea, 28LL 4NN ex C. aperea, 1L 1N ex C. aperea, 30 LL 2NN ex C. aperea, 12 LL ex C. aperea, 54LL 2NN ex C. aperea, 21NN ex C. aperea, 10NN ex C. aperea, 2NN ex C. aperea, 9NN ex C. aperea, 1N ex C. aperea, 1N ex C. aperea, 6NN ex C. aperea, 7NN ex C. aperea; Estancia “Rincón del Socorro” (28°42′S 57°29′W) 1M 6NN 2LL ex A. axis, 37 NN ex S. scrofa, 14NN ex S. scrofa, 1M 2FF 18NN ex S. scrofa, 13 NN ex S. scrofa, 10NN 2LL ex S. scrofa, 5NN 1L ex S. scrofa, 8MM 7FF ex S. scrofa, 6NN ex S. scrofa, 3NN 1L ex S. scrofa, 1M 5FF ex S. scrofa, 20 NN 8LL ex M. tridactyla, 4NN 9LL ex M. tridactyla, 6NN ex M. tridactyla, 2MM 9NN ex M. tridactyla, 1M 10FF ex M. tridactyla, 12 NN 10 LL ex L. europaeus, 1M 16NN 71LL ex H. hydrochaeris, 7NN 9LL ex H. hydrochaeris, 1F 11NN 3LL ex H. hydrochaeris, 3MM 3FF 62NN 28LL ex H. hydrochaeris, 10MM 105NN 123LL ex H. hydrochaeris, 5MM 1F 5NN 212LL ex H. hydrochaeris, 24MM 18FF 59NN 61LL ex H. hydrochaeris, 48NN 83LL ex H. hydrochaeris, 5NN 30LL ex H. hydrochaeris, 50NN 126LL ex H. hydrochaeris, 23NN 6LL ex H. hydrochaeris, 38NN 15LL ex H. hydrochaeris, 2MM 2FF 80NN 2LL ex H. hydrochaeris, 1L ex Akodon azarae (J. Fischer, 1829), 1L ex A. azarae, 1L ex A. azarae, 3LL ex A. azarae, 7LL ex A. azarae, 99LL ex A. azarae, 9LL ex A. azarae, 5LL ex A. azarae, 5LL ex A. azarae, 1L ex A. azarae, 1N 13LL ex A. azarae, 3LL ex Oligoryzomys flavescens (Waterhouse, 1837), 1L ex O. flavescens,1L ex O. flavescens, 7LL ex O. flavescens, 19LL ex O. flavescens, 1N 9LL ex Monodelphis dimidiata (Wagner, 1847), 3NN 12LL ex M. dimidiata, 9LL ex M. dimidiata, 77LL ex M. dimidiata, 6LL ex M. dimidiata.
2) Amblyomma nodosum, Neumann 1899
New record: Estancia “Rincón del Socorro” (28°42′S 57°29′W) 1M ex M. tridactyla.
3) Amblyomma triste Koch, 1844
Laguna del Iberá (28º32′S 57º10′W) 2 FF ex B. dichotomus (Nava et al. 2011), 1M 1N ex H. hydrochaeris (Nava et al. 2011); Loreto (27º46′S 57º16′W) 1N 2LL ex A. azarae (Nava et al. 2011), 2NN 4LL ex Calomys callosus (Rengger, 1830) (Nava et al. 2011), 2NN 16LL ex Oxymycterus rufus (G. Fischer, 1814) (Nava et al. 2011), 1N ex Oligoryzomys nigripes (Olfers, 1818) (Nava et al.2011). New records: 30 km SW of Colonia Carlos Pellegrini (28º40′S 57º26′W) 1M ex H. hydrochaeris; 37 km SW of Colonia Carlos Pellegrini (28°42′S 57°27′W) 1N ex S. aquaticus, 1N ex C. aperea; Estancia “Rincón del Socorro” (28º42′S 57º29′W) 1M 7FF ex S. scrofa, 1M 1 F ex S. scrofa, 1F ex S. scrofa, 2NN ex A. azarae, 3NN ex A. azarae, 4LL ex A. azarae, 10LL ex A. azarae, 3NN 9LL ex A. azarae, 2NN ex O. flavescens, 2LL ex M. dimidiata, 64LL 2NN ex M. dimidiata, 17LL ex A. azarae, 7LL ex A. azarae, 58LL 2NN ex A. azarae, 5LL ex A. azarae, 1L ex O. flavescens, 118LL 5NN ex A. azarae, 19LL 1N ex O. flavescens, 1L ex A. azarae, 46LL ex O. flavescens, 19LL ex A. azarae, 3LL ex M. dimidiata, 1N 57LL ex A. azarae, 42LL ex A. azarae, 1N 13LL ex A. azarae, 2LL ex M. dimidiata, 8LL ex A. azarae.
4) Haemaphysalis juxtakochi Cooley, 1946
New records: Estancia “Rincón del Socorro” (28°42′S 57°29′W) 2FF 1N ex A. axis, 1F ex S. scrofa; 100 km NW of Mercedes (28º36′S 57º16′W) 5MM 2FF ex Mazama gouazoubira (G. Fischer, 1814).
5) Rhipicephalus (Boophilus) microplus (Canestrini, 1888)
New records: Laguna del Iberá (28º32′S 57º10′W) 25FF ex B. dichotomus, 9 MM 11FF ex B. dichotomus; 100 km NW of Mercedes (28º36′S 57º16′W) 4MM 2FF 1N ex B. dichotomus.
This is the first systematic study of ticks associated with wild mammals in the Esteros del Iberá wetlands. The apparently limited tick fauna—only five species—may be related to the unique ecological characteristics of the study area, which possibly preclude the establishment of other tick species, or it may be an artifact of sampling, since hosts belonging to the orders Carnivora and Chiroptera were not examined. Future studies should focus on ticks associated with mammalian orders that were not sampled during this investigation.
Two of the five tick species collected in Esteros del Iberá are of known medical and veterinary importance. Amblyomma triste has been found infected by Rickettsia parkeri in Argentina, Brazil and Uruguay (Venzal et al. 2004; Silveira et al. 2007; Nava et al. 2008), where cases of human disease attributed to this rickettsia have been diagnosed (Conti-Díaz et al. 2009; Moraes-Filho et al.2009; Romer et al. 2011). In our study, adults of A. triste were found on B. dichotomus, H. hydrochaeris and S. scrofa. These results are not unexpected because Nava et al. (2011) determined that adult A. triste feed on large mammals belonging to different orders. Additionally, both B. dichotomus and H. hydrochaeris had already been recorded as key hosts for adults of A. triste in Argentina (Nava et al. 2011). Therefore, our record of A. triste adults on S. scrofa, although new, is not surprising. Similarly, most of the larvae and nymphs of this tick species collected at Esteros del Iberá were from rodents of the subfamilies Sigmodontinae and Caviinae, confirming the results of Nava et al. (2011) in Argentina and Venzal et al. (2008) in Uruguay, who established that these rodents are principal hosts for the immature stages of A. triste. Although Venzal et al. (2008) also found larvae and nymphs of A. triste on the marsupial M. dimidiata, the collection of larvae and nymphs of A. triste on this host in Esteros del Iberá represents the first record of this parasite-host association for Argentina and suggests that M. dimidiata is a suitable host for the immature stages of this tick.
The second tick species of economic relevance collected on wild mammals in Esteros del Iberá is R. (B.) microplus, which was found on the marsh deer, B. dichotomus. This tick is a major pest of cattle and the vector of Babesia bovis and Babesia bigemina, the causative agents of bovine babesiosis (Guglielmone 1992). The ability of B. dichotomus to serve as an alternative host for R. (B.) microplus is not well known. In a study of ticks associated with B. dichotomus in Brazil, carried out in a marsh environment with ecological characteristics similar to Esteros del Iberá, Szabó et al.(2003) determined that R. (B.) microplus was the most prevalent tick on this deer. However, these authors were not convinced that B. dichotomus was able to exclusively maintain populations of R. (B.) microplus. Additional studies should be conducted to determine the suitability of B. dichotomus as a host for R. (B.) microplus and the deleterious effects that this tick may have on marsh deer.
Amblyomma dubitatum is a South American tick associated with H. hydrochaeris (Nava et al.2010a), and the results of our study confirm this observation, because most collections of A. dubitatum were made on H. hydrochaeris. Small marsupials and rodents of the subfamilies Caviinae and Sigmodontinae appear to be alternative hosts for larvae and nymphs, while S. scrofa and A. axis can support the entire life cycle of this tick because immature and adult stages were found feeding on these two exotic mammals. Although the numbers of A. dubitatum collected on L. europaeus, B. bubalis and M. tridactyla were lower, they were sufficient to suggest that these three species of mammals may serve as alternative hosts for A. dubitatum. Similarly, H. juxtakochi may maintain a surrogate life cycle independent of its native host (Mazama spp. (Szabó et al. 2006)) in Esteros del Iberá, because it was also found parasitizing S. scrofa and A. axis.
Although the principal hosts for A. nodosum are mammals of the family Myrmecophagidae(Jones et al. 1972; Guglielmone et al. 2003), the finding of a male of A. nodosum parasitizing M. tridactyla in Esteros del Iberá is not easy to interpret. Myrmecophaga tridactyla became extinct there 30 years ago (Chebez 1999) but was successfully reintroduced recently. The previous records of A. nodosum in Argentina consist of two males collected on Tamandua tetradactyla (Linnaeus, 1758) in Chaco Province, and two males and one female collected on the same host in Formosa Province (Ivancovich 1987). It is unlikely that A. nodosum could have sustained itself in Esteros del Iberá prior to the reintroduction of M. tridactyla. We therefore speculate that the male of A. nodosum reported in this study was not detected on our individual of M. tridactyla prior to its release into the wild. If this hypothesis is valid, the entry into Esteros del Iberá of non-native ticks and their associated pathogens with mammals introduced from other ecological areas constitutes a potential threat to wildlife.
In Brazil, A. dubitatum has been found infected with Rickettsia bellii and R. parkeri (strain COOPERI) (Labruna et al. 2004), Rickettsia rhipicephali and R. bellii have been detected in H. juxtakochi (Labruna et al. 2007), and R. bellii (strain Pontal) and R. parkeri (strain NOD) have been found in A. nodosum (Ogrzewalska et al. 2009). However, the precise role of A. dubitatum, H. juxtakochi and A. nodosum in the transmission of pathogenic microorganisms to both humans and animals is as yet unknown.
A high proportion of the records presented in this work are associations between ticks and exotic (S. scrofa, A. axis, B. bubalis, L. europaeus) or reintroduced (M. tridactyla) mammals. Non-indigenous species may act as new hosts for native parasites, and this interrelationship can have a negative effect on native fauna due to acquisition and amplification of the native parasite by an introduced host (Kelly et al. 2009; Mastitsky & Veres 2010; Tompkins et al. 2011). Both A. axis and S. scrofa are exotic large mammals that occur throughout Esteros del Iberá. The considerable number of specimens of A. dubitatum and A. triste that were collected on A. axis and S. scrofa suggests that introduction of these mammals may result in an increase in tick populations, with potential eco-epidemiological implications. Further studies should determine whether a positive numerical response of tick populations to the presence of exotic hosts is occurring in the Esteros del Iberá wetlands.
We are grateful to INTA, Asociación Cooperadora INTA Rafaela, and CONICET for providing financial support to VND, SN and AAG. Fieldwork was conducted with the support of The Conservation Land Trust Argentina. We thank Dr. U.F.J. Pardiñas for identifying our sigmodontine rodents, and Oscar Warnke for assisting with fieldwork.