INTRODUCTION

Fleas, mites, and ticks are common ectoparasites associated with wild rodents (Cricetidae) worldwide (Morand et al., 2006). Ectoparasites are an important component of biodiversity and hold significant sanitary relevance as they can cause diseases such as pulicosis and acariasis. Moreover, they may act as potential vectors of bacteria whose transmission cycles involve rodent hosts (Tsai et al., 2011; Gutiérrez et al., 2015; Tomassone et al., 2018). Worldwide, zoonotic research on ectoparasites has primarily focused on ticks (e.g. Nava et al., 2017), while studies on fleas and other Acari, such as Mesostigmata, remain scarce (Chaisiri et al., 2015; Moreno Salas et al., 2019, 2020). A similar trend is seen in Argentina, where substantial knowledge has been gained about ticks, encompassing numerous species and geographic regions (Nava et al., 2017). In contrast, researches on fleas are still preliminary (e.g. Urdapilleta et al., 2020, 2021; Melis et al., 2020a), and studies on Mesostigmata mites remain unexplored.

Ticks and fleas were reported to be associated with bacteria of the genus Rickettsia, among others. Rickettsias present a complex cycle that includes the participation of mammals (domestic and wild) as hosts and arthropods as vectors. These bacteria produce diseases considered emerging and collectively called rickettsiosis, which can affect humans and are characterized by high fever, headaches, skin rashes, and muscle pain (Moreno Salas et al., 2020; Moraga-Fernandez et al., 2023).

Northeastern Buenos Aires Province is one of the areas with the greatest biodiversity in Argentina, where cricetid rodents are an important ecosystem component (Burkart et al., 1999; Patton et al., 2015). Several ectoparasites associated with cricetids in the area have been studied, leading to the description of new species (e.g.Lareschi & Gettinger, 2009; Lareschi, 2020; Savchenko & Lareschi, 2022), thereby increasing the known diversity for the region and enhancing its contribution to the overall diversity of the country. Additionally, ticks and fleas parasitizing cricetids in the area have been recorded in association with Rickettsia (Nava et al., 2017; Melis et al., 2020a, 2020b), underscoring the importance of continuing these studies.

Pereyra Iraola Park (PPI) harbors the greatest biodiversity in the province of Buenos Aires. Located in the northeast of the province, the PPI spans the territory of four municipalities (La Plata, Berazategui, Ensenada, and Florencio Varela), though its jurisdiction is mainly provincial. In 2007, the United Nations Educational, Scientific and Cultural Organization (UNESCO) designated the PPI as a World Biosphere Reserve. The PPI forms the Pereyra Iraola Biosphere Reserve with the Punta Lara Nature Reserve (Paolocá, 2023). Prior to the founding of the PPI in 1949, over 10,000 hectares of the park were owned by two large families and were expropriated to protect their rich biodiversity (Morosi et al., 1992). Due to its origin as a family estate, the park features more than 132 introduced forest species, along with important native flora (Vitalone & Delgado, 1994). Currently, the PPI offers a recreational space for the inhabitants of the province while also serving as a buffer between the two major metropolitan areas: Great La Plata to the south and Great Buenos Aires to the north, where one-third of the population of Argentina lives, and the most important industrial and economic hub of the country is located (Del Rio et al., 2007). Due to its diverse uses, the PPI is included in the Man and Biosphere Program (MAB-UNESCO). The park has schools, scientific institutes, experimental nurseries, state agencies, park ranger bases, police training institutions, and numerous agroecological production farms. Among these farms, the Ecological Santa Elena Farm is noteworthy, as it also hosts the headquarters of the Community Centre for University Extension (CCEU) N°10 of the National University of La Plata (UNLP). In addition, the PPI is a popular destination for visitors from across the Metropolitan Area of Buenos Aires (AMBA), particularly on weekends (Domínguez, 2008)

For these reasons, the PPI is of significant interest for conducting various studies. Our research focuses on characterizing the ectoparasite communities associated with cricetid rodents in the area and analysing the presence of Rickettsia in these arthropods. The results will contribute to our understanding of the biodiversity of the region and the zoonotic significance of its fauna.

MATERIALS AND METHODS

Study area

Sampling was conducted at the Ecological Santa Elena Farm (34º50’S, 58º5’W) (Fig. 1), an agroecological production farm located in the southern part of the PPI, a few meters from the Pereyra Train Station next to the General Roca Railway Train Stations and adjacent to the María Teresa School. This farm is the headquarters of the CCEU N° 10 of the UNLP. For this reason, in addition to marketing pesticide-free vegetables through home deliveries, different teams carry out extension practices there and receive numerous visits from national and international schools, universities and research centers. The CCEU itself is inhabited by two caretakers living in a 60 m² house at the entrance of the property. Additionally, agricultural workers, as well as school and university students and researchers, regularly visit the premises to carry out extension and research tasks. Besides, the farm is home to numerous pigs, chickens in pens, and free-roaming horses, cows, a pony, dogs, and cats.

Samples

Rodent traps were placed in an area characterized by three greenhouses where corn, tomato, and legumes are grown, surrounded by a Celtis sp. forest. Rodents were captured alive using Sherman-like traps baited with oats. The traps were placed in the vicinity of the greenhouses and the house. Sampling occurred in 2017 (October) and 2018 (January, February, March, August and October). The sampling effort involved 80 traps per night spaced five meters apart and left in the field for 24 hours. Captured rodents were anesthetized with sulphuric ether and euthanized by cervical dislocation. All procedures were conducted following the ethical guidelines established by the American Society of Mammalogists (Sikes, 2016).

Ectoparasites were collected in the field by examining the fur of the hosts using brushes and forceps, and then stored in alcohol 96 % at -18 °C. A subsample of the ectoparasites was prepared for identification using conventional optical microscopic techniques. Other specimens were subjected to molecular analysis using the PCR technique to detect Rickettsia spp., as described below.

Taxonomic identifications

After DNA extraction, the exoskeletons of the fleas were prepared for their identification under an optical microscope. They were washed with distilled water, cleared in 10 % KOH, dehydrated in a series of ethanol concentrations (80 % to 100 %), diaphanized in eugenol, and mounted in Canada balsam and identified following descriptions and keys provided by Smit (1987) and Linardi & Guimarães (2000). Mites were cleared in lactophenol and mounted in Hoyer’s medium and identified following Furman (1972), Savchenko & Lareschi (2019, 2022), Lareschi (2020), and Radovsky (2010). Ticks were identified under a stereoscopic binocular microscope and identified following Nava et al. (2017). Moreover, voucher specimens of every species fleas were deposited at the Colección de Entomología, and mites at the Colección de Invertebrados, both of the Museo de la Plata, Argentina. Rodents were identified following Patton et al. (2015) and deposited at the Colección de Mamíferos del Centro Nacional Patagónico (CENPAT), Puerto Madryn, Argentina.

Ecological analyses

For ectoparasites collected from each host species indices and parameters were calculated as follows: Ectoparasite specific richness (S= number of species), Shannon specific diversity index [H= -Σ (pi ln pi)], equitability index (J= H/ln S), mean abundance (MA= total number of individuals of a particular parasite species in a sample of a particular host species/total number of hosts of that species, including both infected and non-infected hosts), mean intensity (MI= total number of individuals of a particular parasite species in a sample of a particular host species/total number of infected hosts of that species); and prevalence [P= (number of hosts infected with one or more individuals of a particular parasite species/the number of hosts examined for that parasite species) x 100] (Begon et al., 1988; Bush et al., 1997). The significance (p) of differences between mean abundances and prevalences was tested by using Fisher’s exact test and Bootstrap test (20000 replications), respectively. The software Quantitative Parasitology 3.0 (Reiczigel et al., 2019) was used for the analyses. Only host species with 10 or more individuals captured were considered for the analyses.

Prospecting for Rickettsia

From the only tick collected and from a subsample of mites organized in pools (each pool consisting of three to five specimens collected from the same individual host), genomic DNA extraction was performed by a destructive method through proteolytic digestion with the enzyme proteinase K, placing each specimen in a solution consisting of 340 μl of a solution (10 mM TRIS at pH 8; 100 mM EDTA; 100 mM NaCl), 40 μl of 20 % SDS (sodium dodecyl sulfate) and 20 μl of proteinase K, 500 μg/ml (InvitrogenTM). DNA purification was performed with phenol and chloroform-isoamyl alcohol to denature and precipitate proteins, and precipitation was done with absolute ethanol. Finally, the extracted DNA was reconstituted in a TE buffer solution (10 mM Tris at pH 7.6; 0.1 mM EDTA) (Mangold et al., 1998).

In the case of fleas, it was necessary to preserve the exoskeleton for later preparation and identification under a microscope. Thus, individual DNA extraction was performed with Chelex®-100 (Bio-Rad Laboratories, CA, US) after an incision at the abdominal level to preserve the exoskeleton for further identification under an optical microscope. All collected fleas were analyzed. Genomic DNA extraction was adapted from the procedure described by Miura et al. (2017)as follows: a 5 % solution of Chelex®-100 resin in sterile distilled water was prepared, 100 μL of the homogenized mixture was placed in a microcentrifuge tube together with the individual flea sample, and 5 μL of proteinase K were added; it was left incubating for 18 h at 56 °C, then the enzyme was inactivated at 95 °C for 10 min, and once cooled it was centrifuged for 5 min at 14000 rpm.

In the first instance, a conventional PCR targeting a ca. 800-bp gltA fragment (citrate synthase) was performed to detect the presence of Rickettsia genus by using primers: CS-239 5’-CTCTTCTCATCCTATGGCTATTAT-3’ and CS-1069 5’-CAGGGTCTTCGTGCATTTCTT-3’ (Labruna et al., 2004). To identify Rickettsia to a specific level, samples shown to be positive to gltA were used to amplify: a ca. 800-bp fragment of the outer membrane protein B (OmpB) with the primers 120-M59: 5’-CCGCAGGGTTGGTAACTGC-3’ and 120-807 5’-CCTTTTAGATTACCGCCTAA-3’ (Regnery et al., 1991; Roux & Raoult, 2000). A negative control with ultrapure water and positive control consisting of DNA from Rickettsia vini was included for each reaction. The PCR conditions were: for gltA, 95 ºC for 3 min, 40 cycles of: denaturation at 95 ºC for 15 s, annealing at 52 ºC of 30 s, extension at 72 ºC for 30 s; and a final extension at 72 ºC for 7 min; for ompB, an initial denaturation at 95 ºC for 5 min, 40 cycles of: denaturation at 95 ºC for 30 s, annealing at 50 ºC of 30 s, extension at 72 ºC for 50 s; and a final extension at 72 ºC for 5 min. Afterward, PCR products of positive samples were purified with Wizard® Genomic DNA Purification kit (Promega®) and sequenced using ABI 3730XLs genetic analyzer, Macrogen Inc. (Korea).

The sequences were edited and aligned using CodonCode Aligner (CodonCode Corporation). The DNA sequences obtained were subjected to an analysis of comparison of sequences by using the Basic Local Alignment Search Tool (BLAST; https://blast.ncbi.nlm.nih.gov/Blast.cgi) to determine similarities with species of the genus Rickettsia. A phylogenetic tree was constructed with MrBayes 3.2.6 after 10 million generations, using a GTR+G model of substitution and including other sequences of Rickettsia spp. available in Genbank to determine their phylogenetic relationships. Only sequences where Rickettsia and host were identified at the species level were considered. The tree was visualized with FigTree v.1.4.4. The Bayesian posterior probabilities were transformed into percentages and indicated on the nodes of phylogenetic trees. GenBank accession numbers were indicated on the label of the tree, and samples obtained in this study were in bold (OL961553, OL961554).

RESULTS

A total of 106 cricetid rodents were trapped and identified as Oxymycterus rufus (Fischer) (n= 44), Akodon azarae (Fischer) (n= 41), Oligoryzomys flavescens (Waterhouse) (n= 19), Calomys laucha (Fischer) (n= 1) and Holochilus brasiliensis (Desmarest) (n= 1). Ectoparasites associated only with the three most abundant rodent species were studied, and a total of 859 ectoparasites were collected from them. Out of these, 826 specimens were mites (Acari, Mesostigmata), 32 were fleas (Hexapoda, Siphonaptera), and only one was a tick (Acari, Ixodida). The collected ectoparasites were identified as: Acari, Mesostigmata, Laelapidae: Androlaelaps azarae Lareschi (n= 376), Androlaelaps fahrenholzi (Berlese) (n= 185), Mysolaelaps microspinosus Fonseca (n= 118), Gigantolaelaps wolffsohni Oudemans (n= 39), Laelaps schatzi Savchenko & Lareschi (n= 27), Laelaps galliarii Savchenko & Lareschi (n=17); Acari, Macronyssidae: Ornithonyssus bacoti (Hirst) (n= 64); Acari, Ixodida, Ixodidae: Amblyomma triste Koch (n= 1) (Fig. 2); Hexapoda, Siphonaptera, Rhopalopsyllidae: Polygenis (Neopolygenis) atopus (Jordan & Rothschild) (n= 10), Polygenis (Neopolygenis) massoiai Del Ponte (n= 1), Polygenis (Polygenis) axius axius (Jordan & Rothschild) (n= 13), Polygenis (Polygenis) platensis (Jordan & Rothschild) (n= 8) (Fig. 3).

Total species richness was S= 12, diversity was H= 1.65, and equitability was J= 0.66. In comparison, mites included more species and were more prevalent and abundant (S= 7; P= 83.6%; MA= 7.95) than fleas (S= 4; P= 22%, p< 0.0001; MA= 0.31, p< 0.0001) and ticks (S= 1; P= 1%, p< 0.0001; MA= 0.01, p< 0.0001). Also, fleas were more prevalent and abundant than ticks (P, p< 0.0001; MA, p<0.0005). When comparing among host species, O. rufus showed the highest diversity (H= 1.18), specific richness (S= 7) and equitability (J= 0.61) of ectoparasites, while Ak. azarae showed the lowest diversity (H= 0.58) and equitability (J= 0.32) (Table I).

When comparing total ectoparasites associated with every host species, the mean abundances were higher for O. flavescens (MA= 11.16) and Ak. azarae (MA= 11.39) compared to O. rufus (MA= 4.11, p= 0.004, p= 0.007). There were no differences between O. flavescens and Ak. azarae (p= 0.93). Also, there were no differences between the prevalences of O. flavescens (P= 94.7) and Ak. azarae (P= 92.7, p=0.9), O. flavescens and O. rufus (P= 81.8, p= 0.25), and Ak. azarae and O. rufus (p= 0.19).

Considering only the fleas, O. rufus showed the highest P (38.6%) and MA (0.5), compared to Ak. azarae (P= 12%, p= 0.007; MA= 0.2, p= 0.045) and O. flavescens (P= 5%, p= 0.007; MA= 0.05, p= 0.0008). There were no differences between Ak. azarae and O. flavescens for P (p= 0.65) and MA (p=0.16). Concerning mites, O. flavescens (P= 95%; MA= 11.1) and Ak. azarae (P= 92%; MA= 11.2) showed prevalences and mean abundances higher than O. rufus (P= 70%, p= 0.047, p= 0.012; MA= 3.6, p= 0.002, p= 0.004). There were no differences between Ak. azarae and O. flavescens for P (p= 0.99) and MA (p= 0.98).

Some ectoparasite species were associated with only one host species, such as An. azarae, which was specific to Ak. azarae; G. wolffsohni, L. schatzi, L. galliarii and M. microspinosus only to O. flavescens; P. massoiai to O. rufus; and A. triste to O. rufus (Table II). On the other hand, some ectoparasite species were shared by two or the three cricetid species; A. fahrenholzi was significantly different among host species, with higher mean abundance on O. rufus and Ak. azarae compared to O. flavescens (p= 0.002; p= 0.004), while there were no significant differences between Ak. azarae and O. rufus (p= 0.74). Neither were there differences in prevalences between Ak. azarae–O. flavescens (p= 0.1), Ak. azarae–O. rufus (p= 0.9), and O. flavescens–O. rufus (p= 0.2) (Table II). For O. bacoti, the prevalence was higher in O. rufus compared to Ak. azarae (p= 0.0001), but there was no difference for MA (p= 0.28). For P. (P.) a. axius the prevalence and mean abundance were higher in O. rufus then in Ak. azarae (P, p= 0.03; MA, p= 0.03). The prevalences and mean abundances for P. (N.) atopus and P. platensis were no different between cricetid rodents (Table II).

Concerning prospection of Rickettsia spp., only two fleas were positive, while mites and ticks were negative. Of the two positive fleas, one was identified as P. (P.) atopus from O. rufus and the other one, as P. (P.) a. axius from A. azarae. The sequence analysis indicated that the two positive findings corresponded to Rickettsia felis (Table III; Fig. 4).

The phylogenetic tree showed a clade including all ompB sequences of R. felis and separated from the other Rickettsia species. These clades were structured independently of the arthropod, host, or site of sampling. The clade of R. felis was a sister clade of R. prowazekii, R. rickettsii, and R. typhi, and both clades were sisters of the clade including to R. aeschlimanni, R. massiliae, R. parkeri, and R. raoultii (Fig. 4).

DISCUSSION

While 12 species of ectoparasites were identified, none of the host species reached this specific richness because several of the ectoparasites were host-specific. Although studies on the ectoparasites of the rodents herein considered were carried out in close localities years ago, comparisons are difficult to make because those researches do not consider all the ectoparasites identified at a specific level, such as fleas (Polygenis spp.) (e.g. Lareschi, 1996), or they include the Phthiraptera species, not considered in the present study (e.g. Liljesthröm & Lareschi, 2002). In addition, in recent years the systematics of some ectoparasite species has been revised and these changes make comparisons difficult, so it would be necessary to review those specimens. In this sense, the taxonomic review of Mesostigmata mites associated with cricetids from the PPI and its surroundings allowed the identification of cryptic species and, in some cases, they were described as new species for science. Such is the case of L. schatzi, which was previously considered included in the complex Laelaps paulistanensis Fonseca, An. azarae in Androalelaps rotundus (Fonseca) complex, and L. galliarii and Laelaps scapteromyos (Savchenko & Lareschi) in Laelaps manguinhosi Fonseca (Savchenko & Lareschi, 2019, 2022; Lareschi, 2020). These studies not only expanded the number of known species of the Laelapidae family, but also increased the known biodiversity for the area. Moreover, some of these species previously considered generalists (e.g. An. rotundus and L. manguinhosi), were then considered specific to their hosts based on these studies. These findings not only highlight the importance of the area in biodiversity studies but also suggest the need for its protection, given that being host-specific, the extinction of the rodent hosts would, in turn, lead to the extinction of their parasites.

Although, as stated, comparisons between different studies are not exact, in general terms, within the ectoparasites, the Mesostigmata mites presented the greatest richness and diversity of species and were the most abundant and prevalent. In turn, fleas presented higher values in all these parameters and indices than ticks. These results agree with similar studies in nearby areas such as Punta Lara Nature Reserve (Lareschi, 1996). Likewise, they also agree with studies in other locations in the Argentinean provinces of Buenos Aires (e.g. Navone et al., 2009; Colombo et al., 2014), Entre Ríos (Abba et al., 2001) and Misiones (Lareschi et al., 2019), as well as in southern Brazil (e.g. Barros et al., 1993; Sponchiado et al., 2015). Similarly, high species richness and diversity (e.g. in O. rufus) were not associated with high abundance and prevalence (which were higher in O. flavescens and A. azarae). Comparing the higher taxa of ectoparasites, in O. rufus fleas had the highest abundance and prevalence values, while in the remaining host species, Mesostigmata mites presented the highest ones. Although these values for the communities associated with each host species in some cases agree with results from nearby areas and in others disagree (e.g. Lareschi, 1996), the dominance of Mesostigmata mites remains constant.

Concerning molecular results, they indicate that the sequences of this study have high similarity with R. felis isolated from the flea Ctenocephalides felis (Bouché) from America and Asia. Previously, in Argentina, R. felis was reported for P. (P.) a. axius from Arana, a semiurbanized area located 14 km south of the city of La Plata (northeast of Buenos Aires Province) (Melis et al., 2020a), and C. felis from Rafaela city in Santa Fe Province, Argentina (Nava et al., 2008).

Our study reported the association of R. felis with the flea P. (P.) atopus for the first time and extended the association with P. (P.) a. axius to a nearby locality. Since these fleas have a wide distribution and are also host generalists (Lareschi et al., 2016), the results obtained are epidemiologically important. Rickettsia felis is associated with the spotted fever group rickettsiae (SFG). This bacterium is an emergent and widely distributed flea-borne human pathogenic species, associated with domestic and peridomestic animals and ectoparasites (Stevenson et al., 2005; Merhej & Raoult, 2011; Panti-May et al., 2015). Its main vector is the flea C. felis, but mosquitoes, Mesostigmata mites and ticks may also be associated with this bacterium (Shpynov et al., 2018). Although in this study, Mesostigmata mites were negative for Rickettsia presence, this bacterium was reported in the families Laelapidae and Macronyssidae from Brazil, Lithuania, and China (e.g. Nieri-Bastos et al., 2011; Kuo et al., 2020; Yin et al., 2021; Radzijevskaja et al., 2018). Thus, the epidemiologic relevance of Mesostigmata in the cycle of Rickettsia should not be discarded.

The only tick collected was negative to Rickettsia. However, the association of A. triste with Rickettsia parkeri was reported in nearby localities (Venzal et al., 2012; Nava et al., 2017; Romer et al., 2020). Thus, more samples are needed to evaluate the presence of Rickettsia in this tick in PPI area.

The results obtained present a scenario where it is necessary to continue the research on the ectoparasites of cricetid rodents in the PPI in order to elucidate the taxonomic status of the different species and their host affinity, and consequently, the biodiversity in the area. Likewise, it is necessary to increase research on the Rickettsia-ectoparasite association in order to elucidate the possible role of fleas, mites and ticks in the enzootic cycle of rickettsiae with potential risk for humans mainly in environments where human activities are frequent.

Acknowledgments

We are especially grateful to Elena Senattori (Santa Elena Farm) and Fernando Glenza (Cátedra Libre de Soberanía Alimentaria, Universidad Nacional de La Plata) for providing the guidance and logistics necessary to carry out the sampling at the Farm; to Graciela Minardi (CEPAVE) for her collaboration with the statistical analyses; and to Ulyses Pardiñas (IDEAus, CONICET, Argentina) for his collaboration in the identification of the rodents. The study was supported by Agencia Nacional de Promoción Científica y Tecnológica (PICT 2015-1564), Universidad Nacional de La Plata, Argentina (N992) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (PIP 628) (all to M. Lareschi). Collecting permits were provided by the Dirección de Flora y Fauna del Ministerio de Desarrollo Agrario de la Provincia de Buenos Aires. This study is part of the doctoral dissertation of M. Melis at the Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina.

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Notas de autor

mlareschi@cepave.edu.ar

Información adicional

redalyc-journal-id: 3220