Introduction

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.

FIGURE 1.

Location of Esteros del Iberá, Corrientes Province, Argentina.

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.

Results

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:

Discussion

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.