SciELO - Scientific Electronic Library Online

 
vol.91El género Cryptocanthon (Coleoptera: Scarabaeidae) en Colombia: descripción de especies nuevas, distribución geográfica y conservaciónRelaciones filogenéticas del subgénero Hypodictyon (Anura: Strabomantidae: Pristimantis) con la descripción de tres especies nuevas de la región del Chocó índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Revista mexicana de biodiversidad

versión On-line ISSN 2007-8706versión impresa ISSN 1870-3453

Rev. Mex. Biodiv. vol.91  México  2020  Epub 02-Dic-2020

https://doi.org/10.22201/ib.20078706e.2020.91.3161 

Taxonomy and systematics

Ectoparasites associated with rodents (Rodentia) and marsupials (Didelphimorphia) from northeastern Argentina: new host and locality records

Ectoparásitos asociados con roedores (Rodentia) y marsupiales (Didelphimorphia) del nordeste de Argentina: nuevos registros de huéspedes y localidad

Alicia Paola Benitez-Ibaloa  *  

Leonardo Dionel Aguiarb 

Ingrid María Desireé Di Benedettoa  c 

Atilio José Mangoldc  d 

Francisca Milanoa 

Valeria Natalia Debárboraa  c 

aLaboratorio Biología de los Parásitos, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Avenida Libertad 5470, Corrientes, Argentina

bLaboratorio de Herpetología, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Avenida Libertad 5470, Corrientes, Argentina

cConsejo Nacional de Investigaciones Científicas y Técnicas, Godoy Cruz 2290 (C1425FQB) Ciudad Autónoma de Buenos Aires, Argentina

dInstituto Nacional de Tecnología Agropecuaria, Estación Experimental Agropecuaria Rafaela, CC 22, CP 2300 Rafaela, Santa Fe, Argentina


Abstract

Taxonomically, ectoparasites represent a very diverse group, which includes: fleas, lice, mites, and ticks, among others. The aim of this work is to extend the knowledge about the ectoparasite fauna associated with rodents and marsupials from Corrientes Province. For this purpose, 2 suburban sites in Corrientes City were sampled: Santa Ana de los Guácaras and San Patricio. Fifty-four mammal hosts were examined. Among the marsupials, 2 species were collected: Lutreolina crassicaudata Desmarest, 1804 and Didelphis albiventris Lund, 1840. The analyzed rodents included 3 species: Cavia aperea Erxleber, 1777, Oxymycterus rufus Fischer, 1814 and Oligoryzomys sp. Bangs, 1900. In total, 469 ectoparasites were collected including 5 genera of mites: Androlaelaps Berlese, 1903, Gigantolaelaps Nesbitt, 1951, Laelaps Koch, 1836, Mysolaelaps Fonseca, 1935, and Ornithonyssus Sambon, 1928; 3 species of ticks, Amblyomma ovale Koch, 1844, A. dubitatum Neumann, 1899, and Ixodes loricatus Neumann, 1899; 2 species of fleas: Polygenis axius Jordan & Rothschild, 1923 and Polygenis bohlsi Wagner, 1901, and 3 different lice, Trimenopon hispidum Burmeister, 1838, Gliricola sp. Schrank, 1781, and Gyropus sp. Nitzsch, 1818. These results provide host and locality records and new parasite-host associations.

Keywords: Mites; Ticks; Lice; Fleas

Resumen

Los ectoparásitos representan un grupo muy diverso taxonómicamente, que incluye a las pulgas, piojos, ácaros y garrapatas, entre otros. El objetivo de este trabajo es ampliar el conocimiento sobre la fauna de ectoparásitos asociada a roedores y marsupiales de la provincia de Corrientes. Para este propósito, se tomaron muestras de 2 sitios suburbanos en la ciudad de Corrientes: Santa Ana de los Guácaras y San Patricio. Se examinaron 54 huéspedes mamíferos. Entre los marsupiales, se recolectaron 2 especies: Lutreolina crassicaudata y Didelphis albiventris. Los roedores analizados incluyen 3 especies: Cavia aperea, Oxymycterus rufus y Oligoryzomys sp. El número total de ectoparásitos recolectados fue de 469, que incluyen 5 géneros de ácaros: Androlaelaps Berlese, 1903, Gigantolaelaps Nesbitt, 1951, Laelaps Koch, 1836, Mysolaelaps Fonseca, 1935 y Ornithonyssus Sambon, 1928; 3 especies de garrapatas: Amblyomma ovale, A. dubitatum e Ixodes loricatus; 2 especies de pulgas: Polygenis axius y Polygenis bohlsi, y 3 piojos diferentes: Trimenopon hispidum, Gliricola sp. y Gyropus sp. Estos resultados proporcionan nuevos registros de huéspedes y localidad, así como, nuevas asociaciones parásito-huésped.

Palabras claves: Ácaros; Garrapatas; Piojos; Pulgas

Introduction

Taxonomically, ectoparasites, mostly arthropods, represent a very diverse group that include lice, fleas, mites, ticks, among others (Lareschi, 2017). They exploit food and habitat resources offered by their hosts. Likewise, they acquire health importance as vectors due to their capacity to transmit a wide variety of pathogens such as protozoa, viruses, bacteria and fungi (Mullen & Durden, 2002). Thus, fleas and ticks that feed on small mammals are important vectors of several species bacteria of the genera Bartonella and Rickettsia (Linardi & Guimaraes, 2000; Lipatova et al., 2015).

Specifically, rodents, which are frequent hosts of ectoparasites, assume a role in the transmission of pathogens, since they are natural reservoirs of different parasites, bacteria and viruses. Their high dispersal and reproduction ability favors the transmission (Gómez-Villafañe et al., 2005).

Regarding the knowledge in Argentina, most of the studies on ectoparasites associated with rodents and marsupials are derived from the province of Buenos Aires and provinces of the northwest and south of the country (Autino & Lareschi, 1998; Beldoménico et al., 2005; Castro & Cicchino, 1999; Cicchino & Castro, 1984; Colombetti et al., 2008; Colombo et al., 2013; Guglielmone & Nava, 2014; Lareschi & Linardi, 2005; Lareschi, Autino et al., 2003; Lareschi, Linardi et al., 2003; Lareschi, Buffevant et al., 2007; Lareschi, Nortarnicola et al., 2007; Lareschi et al., 2004, 2010; Nava & Lareschi, 2012; Nava et al., 2003, 2017; Navone et al., 2009; Sánchez & Lareschi, 2013, 2014, among others).

In Corrientes Province, the knowledge is scarce. Some of the studies include findings of mites and fleas that parasitize sigmodontine rodents in the Iberá Wetlands (Lareschi et al., 2006), ticks associated with the marsupial Didelphis albiventris (Di Benedetto et al., 2013; Gómez et al., 2000) and rodents of families Cricetidae and Caviidae in the Iberá Reserve (Debárbora et al., 2014). The aim of this work is to extend the knowledge about the ectoparasite fauna associated with rodents and marsupials from Corrientes Province, Argentina.

Materials and methods

During 2017, 2 suburban sites in Corrientes City were sampled: Santa Ana de los Guácaras and San Patricio. Test samples were made using different traps (Sherman and Tomahawk live-traps-type) and baits such as carrot with apple and vanilla essence, chicken and canned fish with cornmeal. It was determined that the most successful trap and bait was the Tomahawk type with the carrot and apple bait with vanilla essence. For this reason, 52 Tomahawk traps were used to capture rodents and marsupials. Four samplings were carried out at each site during 3 consecutive nights. Rodents and marsupials were processed according to the methodology described by Nava et al. (2006) and Tarragona et al. (2011) , and following biosecurity protocols proposed by Mills et al. (1995). Rodent captures were handled with thick rubber gloves and immediately placed inside a double plastic bag that closed perfectly. The bags were opened at Laboratorio de Biología de los Parásitos, Facultad de Ciencias Exactas y Naturales y Agrimensura (Universidad Nacional del Nordeste), with protective clothing and biosafety masks. We examined the specimens under a hood with extractor where the ectoparasites were checked and extracted. For caved rodents, they were checked and combed in the field and then released. Marsupials (Didelphidae) were anesthetized according to Tarragona et al. (2011) with the help of a veterinarian. Specimens were combed and the ectoparasites collected with tweezers. Once recovered from anesthesia, the marsupials were returned to their habitat. Sigmodontines (Rodentia: Cricetidae) were taxonomically identified by Carlos Galliari (Centro de Estudios Parasitológicos y de Vectores, Universidad Nacional de La Plata, Argentina). Hosts were captured under permission of the Dirección de Recursos Naturales of Corrientes Province, Argentina.

Ectoparasites were recovered by examining the fur with a magnifying lens, then preserved in 96º ethanol, and / or mounted on slides according to the routine methodology of each taxon. Mites were identified following Furman (1972) and Saunders (1975), ticks were identified following Martins et al. (2014) and Nava et al. (2017), fleas according to Smit (1987) and Linardi and Guimaraes, (2000) and lice according to Cicchino and Castro, (1998). The collected specimens are listed below, indicating the number of ectoparasite specimens of each sex, except for mites that were only determined to the genus level. Also adults were indicated, as well as host species and locality, in parentheses is mentioned the number of parasitized individuals over the number of hosts analyzed. A brief report that includes comments on previous records in the province of Corrientes and other known host species for each ectoparasite species is presented. Abbreviation NA (not available) is used when the information is undetermined. Abbreviation INTA means Instituto Nacional de Tecnología Agropecuaria.

Results

Fifty-four mammal hosts were examined, 20 belonging to the order Didelphimorphia and 34 to Rodentia. Among the marsupials, 2 species were assessed: Lutreolina crassicaudata Desmarest, 1804 and Didelphis albiventris Lund, 1840. The rodents analyzed included 3 species: Cavia aperea Erxleben, 1777, Oxymycterus rufus Fischer, 1814 and Oligoryzomys sp., Bangs, 1900. The total number of ectoparasites collected was 469 specimens, 130 specimens of these belong to the order Phthiraptera, 39 to Siphonaptera, 244 to Mesostigmata and 11 to Ixodida. Below, we present the ectoparasite species list associated with the mammals collected in this study.

Order Ixodida Leach, 1815

Family Ixodidae Koch, 1844

Amblyomma ovale, Koch, 1844: 1 nymph on O. rufus (1/1), Santa Ana de los Guácaras.

Previous records: females on Canis lupus familiaris Linnaeus, 1758, Santa Ana de los Guácaras (Debárbora et al., 2011); female and nymphs on D. albiventris, San Cayetano (Di Benedetto et al., 2013).

Amblyomma dubitatum, Neumann, 1899: 2 nymphs on L. crassicaudata (2/1), Santa Ana de los Guácaras.

Previous records: females, males and nymphs on Hydrochoerus hydrochaeris Linnaeus, 1766, Estancia "Ayuí", Estancia "Juan Ángel", Estancia "Palmita", Laguna del Iberá, Estancia “La Armonía” (Ivancovich & Luciani, 1992). Nymphs on cattle, Monte Caseros (Guglielmone et al., 2002). Nymphs on cattle, Goya; females, males, and nymphs on H. hydrochaeris, Mercedes (INTA Collection). Males, nymphs, and larvae on man, Iberá II Provincial Reserve (Oscherov et al., 2006). Male and female on Sus scrofa Linnaeus 1758, “Rincón del Socorro” (INTA Collection). Females, males, nymphs, and larvae on H. hydrochaeris, 30 km SW of Colonia Carlos Pellegrini (Nava et al., 2010). Females, males, and nymphs on S. scrofa, Estancia "Rincón del Socorro” (Debárbora et al., 2012; Nava et al., 2010). Nymph on Bubalus bubalis Linnaeus, 1758, Iberá Provincial Reserve (Debárbora et al., 2012). Larvae on Scapteromys aquaticus, Thomas, 1920; larvae and nymphs on C. aperea, 37 km SW of Colonia Carlos Pellegrini (Debárbora et al., 2012). Larvae and nymphs on Axis axis Erxleben, 1777 and S. scrofa; males and larvae on Myrmecophaga tridactyla Linnaeus, 1758, and Lepus europaeus Pallas, 1778; females, males, nymphs, and larvae on H. hydrochaeris; nymphs and larvae on Akodon azarae Fischer, 1829; larvae on Oligoryzomys flavescens Waterhouse, 1837; larvae and nymphs on Monodelphis dimidiata Wagner, 1847, Estancia "Rincón del Socorro" (Debárbora et al., 2012). Females, males, nymphs, and larvae on vegetation, Mburucuya. Larvae and nymphs on vegetation, Mercedes. Females, males, and nymphs on vegetation, Provincial Route 40, km 60. Male, nymph, and larvae on vegetation, Santa Barbara (Monje et al., 2015).

Ixodes loricatus, Neumann, 1899: 2 females and one male on L. crassicaudata (3/2), Santa Ana de los Guácaras. Previous records: females on D. albiventris, Corrientes (Gómez et al., 2000).

Order Siphonaptera Latreille, 1825 Family Rhopalopsyllidae Oudemans, 1909

Polygenis axius, Jordan & Rothschild, 1923: 12 females and 10 males on L. crassicaudata (22/7), 1 female and 1 male on Oligoryzomys sp. (2/1), Santa Ana de los Guácaras. One female and 1 male on L. crassicaudata (2/2); 2 males on D. albiventris (2/2); 1 female and 1 male on C. aperea (2/2); 1 female on O. rufus (1/1), San Patricio.

Previous records: females and males on O. rufus, Department of San Miguel (Lareschi et al., 2006).

Polygenis bohlsi, Wagner, 1901: 5 males on L. crassicaudata (5/5), Santa Ana de los Guácaras. One male on L. crassicaudata (1/1), 1 female and 1 male on D. albiventris (2/1), one male on C. aperea (1/1), San Patricio.

Previous records: There are no previous records for this flea in Corrientes Province.

Order Phthiraptera Haeckel, 1896

Family Trimenoponidae Harrison, 1915

Trimenopon hispidum Burmeister, 1838: 30 nymphs, 15 females and 9 males on C. aperea (54/13), Santa Ana de los Guácaras. Eighteen nymphs, 26 females, and 13 males on C. aperea (57/12), San Patricio.

Previous records: there are no previous records for this lice in Corrientes Province.

Family Gyropidae Kellog, 1896

Gyropus sp. Nitzch, 1818: 1 female on C. aperea (1/1), San Patricio.

Previous records: there are no previous records for this lice in Corrientes Province.

Gliricola sp. Schrank, 1781: 13 females and 3 males on C.

aperea (16/1), San Patricio.

Previous records: there are no previous records for this lice species for Corrientes Province.

Order: Mesostigmata Canestrini, 1891

Family: Lealepidae Berlese, 1892

Androlaelaps sp. Berlese, 1903: 20 adults on O. rufus (20/1), Santa Ana de los Guácaras.

Previous records: females on A. azarae, Department of San Miguel (Lareschi et al., 2006).

Gigantolaelaps sp. Nesbitt, 1951: 6 adults on Oligoryzomys sp. (6/2), Santa Ana de los Guácaras.

Previous records: female on Ol. flavescens, Department of San Miguel (Lareschi et al., 2006).

Laelaps sp. Koch, 1836: 4 adults on Oligoryzomys sp. (4/1), Santa Ana de los Guácaras.

Previous records: females on Holochilus brasiliensis Desmarest, 1819, Loreto (Lareschi et al., 2001). Females on Oligoryzomys delticola Thomas, 1917, Calomys callidus Thomas, 1916, O. rufus, Department of San Miguel (Lareschi, et al., 2006).

Mysolaelaps sp. Fonseca, 1935: 13 adults on Oligoryzomys sp. (13/2), Santa Ana de los Guácaras.

Previous records: female on O. flavescens, Department of San Miguel (Lareschi et al., 2006).

Family: Macronyssidae Oudemans, 1936

Ornithonyssus sp. Sambon, 1928: one specimen on L. crassicaudata (1/1); 10 specimens on Oligoryzomys sp. (10/1); 4 specimens on O. rufus (4/1); 17 specimens on C. aperea (17/2), Santa Ana de los Guácaras; 169 specimens on C. aperea (169/10), San Patricio.

Previous records: there are no previous records for this mite in Corrientes Province.

Discussion

Currently, 409 species of native mammals to Argentina are recognized, of which approximately 85 species are registered for the Corrientes Province (Barquez et al., 2006; Parera, 2018). In this work, we report 10 taxa of ectoparasites associated with 3 species of rodents and 5 associated with 2 species of marsupials from Corrientes.

Rodents of the families Cricetidae and Echimyidae are the main hosts for larvae and nymphs of A. ovale (Guglielmone & Nava, 2014). They present a wide distribution, records of this species are found from the central-northern area of Argentina throughout the Neotropics to the Nearctic region up to USA. While in Argentina there are records associated with other hosts such as canids reported as the main hosts for adults in Chaco, Misiones, Formosa, Entre Ríos, Salta, Jujuy, Mendoza, La Rioja (Guglielmone & Mangold, 1986; Guglielmone & Nava, 2014; Ivancovich & Luciani, 1992; Sinkoc et al., 1998). In the province of Corrientes, records for A. ovale have been found on C. familiaris and D. albiventris (Debárbora et al., 2011; Di Benedetto et al., 2013). In this research, a new association of nymphs of A. ovale with the cricetid O. rufus is recorded, being the first parasite-host association for the country and South America.

On the other hand, A. dubitatum a tick that feeds on a wide range of mammals, and also immature stages have even been found on birds (Flores et al., 2014; Nava et al., 2010). However, in this work we collected nymphs of this species associated with the marsupial L. Crassicaudata, which had been previously registered as a host of this tick species in Brazil (Blanco et al., 2017; Saraiva et al., 2012). Therefore, this represents a new host association in Argentina. Considering that this marsupial is commonly found near bodies of water, and in the study area, there are lagoons with populations of H. hydrochaeris, which is one of its primary host, it is not common to find this association.

Regarding I. loricatus, a Neotropical parasite of marsupials and rodents (Nava et al., 2004), was reported in central and northern Argentina (Guglielmone et al., 2011; Tarragona et al., 2018). For Corrientes, Gómez et al. (2000) mention I. loricatus infecting D. albiventris, although in this research the species was found on L. crassicaudata.

In northwestern Argentina, Lareschi, Autino et al. (2003) provided records of hosts and distribution areas of mites associated with wild rodents; the families Laelapidae and Macronyssidae are mentioned. Presence of Laelapidae mites of the genera Gigantolaelaps, Androlaelaps, Mysolaelaps and Laelaps were found in association with cricetid rodents, coinciding with those reported by Lareschi et al. (2001, 2006) for the province of Corrientes. On the other hand, Ornithonyssus sp. were reported in association with A. azarae, O. rufus, S. Aquaticus, and O. flavescens in Buenos Aires, Salta and Tucumán (Capri & Mauri, 1971; Colombo et al., 2013; Lareschi, 1996; Lareschi, Autino et al., 2003; Liljeström & Lareschi, 2002). The records presented in this work are new for the province of Corrientes, expanding the distribution range of the species in the country.

In reference to parasitic insects, some groups show a high level of specificity for their hosts such as lice (Pérez, 2015). In this study, the findings of Gliricola sp., Gyropus sp. and T. hispidum associated with rodents of the family Caviidae, reaffirm the above mentioned, as well as the works of Werneck (1948), Emerson and Price (1975). In discrepancy with Ronald and Wagner (1976) and Valim et al. (2004), they mention a lower abundance while in this work the opposite occurs being T. hispidum, the most abundant of all the analyzed ectoparasites.

In Argentina, there are studies of T. hispidum and Gliricola porcelli found on C. aperea for the provinces of Buenos Aires and Entre Ríos, while Gyropus ovalis was found in the mentioned provinces and in Chaco province as well (Castro & Cicchino, 1987; Castro et al., 1996; Werneck, 1948). Since there are no studies on these parasite-host associations in the province of Corrientes, this work would be the first contribution on the subject. Although these lice are chewers, they can cause damage to their hosts when infestations are high, producing alopecia or secondary infections due to excessive scratching (Owen, 1968; Paterson, 1967).

In the Neotropical region, the fleas parasitize mainly small mammals, as caviomorph rodents and sigmodontine, as well as marsupials of the order Didelphimorphia (Krasnov, 2008). In Argentina, P. axius has been mentioned infecting rodents and marsupials (Linardi & Guimaraes, 2000; Nava & Lareschi, 2012). Lareschi, Nortarnicola et al. (2007) report the first records of fleas of the genus Polygenis parasitizing cavid rodents in the province of Cordoba. In Corrientes, Lareschi et al. (2006) recorded specimens of this genus on O. rufus for San Miguel, coinciding with what was found in this research. Additionally, we report L. crassicaudata as a new host for P. axius. On the other hand, P. bolhsi has been mentioned in Argentina infecting Didelphis sp., C. aperea, A. azarae, Akodon dolores Thomas, 1916, Calomys laucha Fischer, 1814, Deltamys kempi Thomas, 1917, Graomys griseoflavus Waterhouse, 1837, S. aquaticus and Mus musculus Linnaeus, 1758 (Autino & Lareschi, 1998; Lareschi et al., 2004; Lareschi et al., 2016), in accordance with what was found in this work, it can be considered a generalist species and has already been registered in other countries of South America (Smit, 1987). The distribution of this genus is expanded to the province of Corrientes due to the results of this work. Although Lareschi et al. (2016) mention P. bohlsi for the province of Corrientes, this corresponds to a study conducted in the province of Mendoza, since the previous reports were for Entre Ríos, Buenos Aires, Córdoba and Chaco provinces (Autino & Lareschi, 1998).

The first records for the province of Corrientes are: P. bohlsi, T. hispidum, Gyropus sp., Gliricola sp., and Ornithinyssus sp. Furthermore, from an epidemiological perspective, the finding of ticks and fleas in wildland-urban interface sites constitutes a warning about the possibility of contact between these ectoparasites and people, and their consequent potential for pathogen transmission. In this sense, there are records in the Corrientes Province of A. dubitatum carrying pathogens Rickettsia bellii, Rickettsia sp. strain cooperi and Rickettsia sp. strain Atlantic rainforest. The latter is pathogenic for humans (Monje et al., 2015), and of A. ovale with Hepatozoon canis and Rickettsia sp. strain Atlantic rainforest in Brazil (Forlano et al., 2005; Nieri-Bastos et al., 2016). Similarly, fleas of the genus Polygenis are vectors of a variety of bacteria such as Bartonella sp. and Salmonella sp. (de Sousa et al., 2018; Linardi & Guimaraes, 2000). Thus, the need to carry out studies aimed to clarify the role of these ectoparasites in the transmission of pathogens to humans becomes evident.

Acknowledgements

We especially want to express our sincere appreciation of Santiago Nava for his help in the identification of samples; Irina Martínez for her support in the field work handling animals; Carlos Galliari for his help in the identification of sigmodontine rodents, Ana Arias for the English revision, the team of the Laboratorio Biología de los Parásitos for their support in the field work and finally, we thank the anonymous reviewers for their enriching contributions with the manuscript. In addition, we thank Facultad de Ciencias Exactas y Naturales y Agrimensura for providing the official vehicle. Financial support was provided by Secretaría General de Ciencia y Técnica (PI 16F/007).

References

Autino, A. G., & Lareschi, M. (1998). Siphonaptera. In J. J. Morrone, & S. Coscarón (Eds.), Biodiversidad de artrópodos argentinos: una perspectiva biotaxonómica (pp. 279-290). La Plata, Argentina: Ediciones Sur. [ Links ]

Barquez, R. M., Díaz, M. M., & Ojeda, R. A. (2006). Mamíferos de Argentina. Sistemática y distribución. Mendoza, Argentina: Editorial SAREM. [ Links ]

Beldoménico, P. M., Lareschi, M., Nava S., Mangold, A. J., & Guglielmone, A. A. (2005). The parasitism of immature stages of Ixodes loricatus (Acari: Ixodidae) on wild rodents in Argentina. Experimental and Applied Acarology, 36, 139- 148. https://doi.org/10.1007/s10493-005-1272-0 [ Links ]

Blanco, C. M., Teixeira, B. R., da Silva, A. G., de Oliveira, R. C., Strecht, L., Ogrzewalska, M. et al. (2017). Microorganisms in ticks (Acari: Ixodidae) collected on marsupials and rodents from Santa Catarina, Paraná and Mato Grosso do Sul states, Brazil. Ticks and Tick-borne Diseases, 8, 90-98. https://doi.org/10.1016/j.ttbdis.2016.10.003 [ Links ]

Capri, J. J., & Mauri, R. A. (1971). Ectoparásitos (Suctoria and Acarina) de roedores de la familia Caviidae en Argentina. Revista de la Sociedad Entomológica Argentina, 33, 1-4. [ Links ]

Castro, D. D. C., & Cicchino, A. (1987). Lista referencial de los Anoplura y Mallophaga (Insecta) conocidos como parásitos de mamíferos en la Argentina. Revista de la Sociedad Entomológica Argentina , 44, 357-369. [ Links ]

Castro, D. D. С., & Cicchino, A. C. (1999). Adultos y estados preimaginales de dos especies de Phthiraptera (Gyropidae, Hoplopleuridae) parásitos de Microcavia australis (Rodentia, Caviidae). Iheringia, Serie Zoológica, 86, 61-70. [ Links ]

Castro, D. D. C., Cicchino, A. C., & Lareschi, M. (1996). Morfología coriónica de los huevos de Phthiraptera (Psocodea) parásitos de Cavia pamparum Thomas, 1917 (Rodentia, Caviidae). Revista Brasilera de Entomología, 40, 211-220. [ Links ]

Cicchino, A. C. , & Castro, D. D. C. (1984). Contribución al conocimiento de los malófagos argentinos XV. Una nueva especie del género Philandesia, Kellogg and Nakayama, 1914 (Mallophaga-Trimenoponidae). Historia Natural, 4, 25-32. [ Links ]

Cicchino, A. C. , & Castro, D. D. C. (1998). Amblycera. In J. J. Morrone, & S. Coscaron (Eds.), Biodiversidad de artrópodos argentinos: una perspectiva biotaxonómica (pp. 84-103). La Plata, Argentina: Ediciones Sur . [ Links ]

Colombetti, P. L., Autino, A. G., Claps, G. L., Carma, M. I., & Lareschi, M. (2008). Primera cita de Cleopsylla townsendi (Siphonaptera: Stephanocircidae: Craneopsyllinae) en la Argentina. Revista de la Sociedad Entomológica Argentina , 67, 179-182. [ Links ]

Colombo, V. C., Lareschi, M. , Monje, L. D., Nava, S., Antoniazzi, L. R., Beldoménico, P. M. et al. (2013). Garrapatas (Ixodida) y ácaros (Mesostigmata) parásitos de roedores sigmodontinos del delta del Paraná, Argentina. Revista FAVE, Sección Ciencias Veterinarias, 12, 39-50. https://doi.org/10.14409/favecv.v12i1/2.4544 [ Links ]

Debárbora, V. N., Mangold, A., Oscherov, E. B., Guglielmone, A. A. , & Nava, S. (2014). Study of the life cycle of Amblyomma dubitatum (Acari: Ixodidae) based on field and laboratory data. Experimental and Applied Acarology , 63, 93-105. https://doi.org/10.1007/s10493-014-9767-1 [ Links ]

Debárbora, V. N. , Nava, S. , Cirignoli, S., Guglielmone, A. A. , & Poi, A. S. (2012). Ticks (Acari: Ixodidae) parasitizing endemic and exotic wild mammals in the Esteros del Iberá wetlands, Argentina. Systematic and Applied Acarology, 17, 243-251. https://doi.org/10.11158/saa.17.3.3 [ Links ]

Debárbora, V. N. , Oscherov, E. B. , Guglielmone, A. A. , & Nava, S. (2011). Garrapatas (Acari: Ixodidae) asociadas a perros en diferentes ambientes de la provincia de Corrientes, Argentina. Investigación Veterinaria, 13, 45-51. [ Links ]

de Sousa, K. C. M., do Amaral, R. B., Herrera, H. M., Santos, F. M., Macedo, G. C., de Andrade-Pinto, P. C. E. et al. (2018). Genetic diversity of Bartonella spp. in wild mammals and ectoparasites in Brazilian Pantanal. Microbial Ecology, 76, 544-554. https://doi.org/10.1007/s00248-017-1138-0 [ Links ]

Di Benedetto, I. M. D., Nava, S. , & Oscherov, E. B. (2013). Primer registro de Didelphis albiventris Lund, 1841 (Didelphimorphia: Didelphidae) como hospedador para adultos y ninfas de Amblyomma ovale Koch, 1844 (Acari: Ixodidae) en Argentina. Revista Argentina de Parasitología, 1, 45-48. [ Links ]

Emerson, K. C., & Price, R. D. (1975). Mallophaga of Venezuelan mammals. Brigham Young University Science Bulletin, Biological Series, 20, 1. [ Links ]

Flores, F. S., Nava, S. , Batallán, G., Tauro, L. B., Contigiani, M. S., Diaz, L. A. et al. (2014). Ticks (Acari: Ixodidae) on wild birds in north-central Argentina. Ticks and Tick-borne Diseases , 5, 715-721. https://doi.org/10.1016/j.ttbdis.2014.05.004 [ Links ]

Forlano, M., Scofield, A., Elisei, C., Fernandes, K. R., Ewingy, S. A., & Massard, C. L. (2005). Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Veterinary Parasitology, 134, 1-7. https://doi.org/10.1016/j.vetpar.2005.05.066 [ Links ]

Furman, D. P. (1972). Mites of the family Laelapidae in Venezuela (Acarina: Laelapidae). Brigham Young University Science Bulletin , Biological Series, 17, 1-65. [ Links ]

Gómez, L., Santa Cruz, A. M., Borda, J., & Lombardero, O. J. (2000). Nueva localización en Argentina de Ixodes loricatus Neumann, 1899 (Acari: Ixodidae) parasitando a Didelphis albiventris. Revista de Medicina Veterinaria, 81, 340-341. [ Links ]

Gómez-Villafañe, I. E., Miño, M., Cavia, R., Hodara, K., Courtalón, P., Suárez, O. et al. (2005). Roedores: guía de la provincia de Buenos Aires. Buenos Aires: LOLA. [ Links ]

Guglielmone, A. A. , & Mangold, A. J. (1986). Hallazgo de Amblyomma ovale Koch, 1844 (Amblyomma fossum Neumann, 1899) en las provincias de Salta y Jujuy, Argentina. Veterinaria Argentina, 3, 167-168. [ Links ]

Guglielmone, A. A. , Mangold, A. J. , Boero, C., Piccinini, A., & Keirans, J. E. (2002). Hallazgo de Amblyomma cooperi Nuttall and Warburton, 1907 en bovinos de corrientes, Argentina. Veterinaria Argentina, 19, 124-125. [ Links ]

Guglielmone, A. A. , & Nava, S. (2014). Distribución geográfica, hospedadores y variabilidad genética de Amblyomma ovale y Amblyomma aureolatum (Acari: Ixodidae), dos vectores potenciales de Rickettsias en la argentina. In J. Basualdo, D. Enria, P. Martina, M. Rosenzvit, & A. Seijo (Eds.), Temas de zoonosis VI (pp. 313-319). Buenos Aires: Asociación Argentina de Zoonosis. [ Links ]

Guglielmone, A. A. , Nava, S. , & Díaz, M. M. (2011). Relationships of South American marsupials (Didelphimorphia, Microbiotheria and Paucituberculata) and hard ticks (Acari: Ixodidae) with distribution of four species of Ixodes. Zootaxa, 3086, 1-30. https://doi.org/10.11646/zootaxa.3086.1.1 [ Links ]

Ivancovich, J. C., & Luciani, C. A. (1992). Las garrapatas de Argentina. Buenos Aires: Monografía de la Asociación Argentina de Parasitología Veterinaria, 95. [ Links ]

Krasnov, B. R. (2008). Funtional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge, UK: Cambridge University Press. https://doi.org/10.1017/CBO9780511542688 [ Links ]

Lareschi, M. (1996). Estudio preliminar de la comunidad de roedores (Rodentia: Muridae) y sus ectoparásitos (Acari, Phthiraptera y Siphonaptera) en Punta Lara (Buenos Aires). Revista de la Sociedad Entomológica Argentina , 55, 113-120. [ Links ]

Lareschi, M. (2017). Artrópodos ectoparásitos. In F.B. Draggo (Coord.), Macroparásitos: diversidad y ecología (pp.167- 183). La Plata, Argentina: Edulp. [ Links ]

Lareschi, M. , Abba, A. M., Sauthier, D. E. U., Bender, J. B., & Nava, S. (2001). New records of the mite Laelaps manguinhosi (Acari: Parasitiformes: Laelapidae) in Argentina. Revista de la Sociedad Entomológica Argentina , 60, 255-256. [ Links ]

Lareschi, M. , Autino, A., Díaz, M. M. , & Barquez, R. M. (2003). New host and locality records for mites and fleas associated with wild rodents from northwestern Argentina. Revista de la Sociedad Entomológica Argentina , 2, 60-64. [ Links ]

Lareschi, M. , Buffevant, M., & Nava, S. (2007). Ácaros and pulgas ectoparásitos de Galea musteloides Meyen, 1832 (Rodentia: Caviidae) en el Noroeste de la Provincia de Córdoba, Argentina. Revista FAVE, Sección Ciencias Veterinarias , 6, 11-17. https://doi.org/10.14409/favecv.v6i1/2.1438 [ Links ]

Lareschi, M. , Gettinger, D., Nava, S. , Abba, A., & Merino, M. L. (2006). First report of mites and fleas associated with sigmodontine rodents from Corrientes Province, Argentina. Mastozoología Neotropical, 13, 251-254. [ Links ]

Lareschi, M. , & Linardi, P. M. (2005). New data on the morphology of Polygenis (Polygenis) rimatus (Jordan) (Siphonaptera: Rhopalopsyllidae). Neotropical Entomology, 34, 121-125. https://doi.org/10.1590/s1519-566x2005000100017 [ Links ]

Lareschi, M. , Linardi, P. M. , Autino, A. G. , Barquez, R. M. , & Díaz, M. M. (2003). First report of Polygenis (Polygenis) roberti beebei (Fox, 1947) (Siphonaptera: Rhopalopsyllidae) in Argentina, with a new host record and morphological data. Systematic Parasitology, 56, 183-187. https://doi. org/10.1023/b:sypa.0000003804.37547.9b [ Links ]

Lareschi, M. , Nortarnicola, J., Nava, S. , & Navone, G. (2007). Parasite community (Arthropods and Filarioids) associated with wild rodents from the marshes of La Plata River, Argentina. Comparative Parasitology, 74, 141-147. https://doi.org/10.1654/4208.1 [ Links ]

Lareschi, M. , Ojeda, R., & Linardi, P. M. (2004). Flea parasites of small mammals in the Monte Desert biome in Argentina with new host and locality records. Acta Parasitologica, 49, 63-66. [ Links ]

Lareschi, M. , Sánchez, J. P., & Autino, A. (2016). A review of the fleas (Insecta: Siphonaptera) from Argentina. Zootaxa , 4103, 239-258. https://doi.org/10.11646/zootaxa.4103.3.3 [ Links ]

Lareschi, M. , Sánchez, J. P. , Ezquiaga, M. C., Autino, A. G. , Díaz, M. M. , & Barquez, R. M. (2010). Fleas associated with mammals from Northwestern Argentina, with new distributional reports. Comparative Parasitology , 77, 207- 213. https://doi.org/10.1654/4448.1 [ Links ]

Liljeström, G., & Lareschi, M. (2002). Estudio preliminar de la comunidad de ectoparásitos de roedores sigmondontinos en el partido de Berisso, provincia de Buenos Aires. In D. Salomón (Ed.), Actualizaciones en artropodología sanitaria argentina (pp. 257-260). Buenos Aires: Fundación Mundo Sano. [ Links ]

Linardi, P. M. , &, Guimaraes, L. R. (2000). Sifonápteros do Brasil. Museu de Zoologia, São Paulo, Brasil: Universidade de São Paulo. [ Links ]

Lipatova, I., Paulauskas, A., Puraite, I., Radzijevskaja, J., Balciauskas, L., & Gedminas, V. (2015). Bartonella infection in small mammals and their ectoparasites in Lithuania. Microbes and infection, 17, 884-888. https://doi.org/10.1016/j.micinf.2015.08.013 [ Links ]

Martins, T. F., Labruna, M. B., Mangold, A. J. , Cafrune, M. M., Guglielmone, A. A. , & Nava, S. (2014). Taxonomic key to nymphs of the genus Amblyomma (Acari: Ixodidae) in Argentina, with description and redescription of the nymphal stage of four Amblyomma species. Ticks and Tick-borne Diseases , 5, 753-770. https://doi.org/10.1016/j.ttbdis.2014.05.007 [ Links ]

Mills, J. N., Yates, T. L., Childs, J. E., Parmenter, R. R., Ksiazek, T. G., Rolliny, P. E. et al. (1995). Guidelines for working with rodents potentially infected with Hantavirus. Journal of Mammalogy, 76, 716-722. https://doi.org/10.2307/1382742 [ Links ]

Monje, L. D., Nava, S., Eberhardt, A. T., Correa, A. I., Guglielmone, A. A., & Beldoménico, P. M. (2015). Molecular detection of the human pathogenic Rickettsia sp. strain Atlantic rainforest in Amblyomma dubitatum ticks from Argentina. Vector-borne and Zoonotic Diseases, 15, 167-169. https://doi.org/10.1089/vbz.2014.1741 [ Links ]

Mullen, G. R., & Durden, L. A. (2002). Medical and veterinary entomology. San Diego: Elsevier. https://doi.org/10.1016/B978-0-12-510451-7.X5000-2 [ Links ]

Nava, S. , & Lareschi, M. (2012). Ecological characterization of a community of arthropods parasitic of Sigmodontine Rodents in the Argentinean Chaco. Journal of Medical Entomology, 49, 1276-1282. https://doi.org/10.1603/me12057 [ Links ]

Nava, S. , Lareschi, M. , Beldoménico, P. M. , Zerpa, C., Venzal, J. M., Mangold, A. J. et al. (2004). Sigmodontinae rodents as hosts for larvae and nymphs of Ixodes loricatus Neumann, 1899 (Acari: Ixodidae). Parasite, 11, 411-414. https://doi.org/10.1051/parasite/2004114411 [ Links ]

Nava, S. , Lareschi, M. , & Voglino, D. (2003). Interrelationship between ectoparasites and wild rodents from northeastern Buenos Aires Province, Argentina. Memórias do Instituto Oswaldo Cruz, 98, 45-49. https://doi.org/10.1590/s0074-02762003000100007 [ Links ]

Nava, S. , Mangold, A. J. , & Guglielmone, A. A. (2006). The natural hosts for larvae and nymphs of Amblyomma neumanni and Amblyomma parvum (Acari: Ixodidae). Experimental and Applied Acarology , 40, 123. https://doi.org/10.1007/s10493-006-9026-1 [ Links ]

Nava, S. , Venzal, J. M. , Acuña, D. G., Martins, T. F. , & Guglielmone, A. A. (2017). Ticks of the Southern cone of America: diagnosis, distribution, and hosts with taxonomy, ecology and sanitary importance. Cambridge, Massachusetts, USA: Academic Press. https://doi.org/10.1016/B978-0-12-811075-1.00010-8 [ Links ]

Nava, S. , Venzal, J. M. , Labruna, M. B. , Mastropaolo, M., González, E. M., Mangold, A. J. et al. (2010). Hosts, distribution and genetic divergence (16S rDNA) of Amblyomma dubitatum (Acari: Ixodidae). Experimental and Applied Acarology , 51, 335-351. https://doi.org/10.1007/s10493-009-9331-6 [ Links ]

Navone, G. T. , Notarnicola, J., Nava, S. , Robles, M. R., Galliari, C., & Lareschi, M. (2009). Arthropods and helminths assemblage in sigmodontine rodents from wetlands of the Rio de la Plata, Argentina. Mastozoología Neotropical , 16, 121-133. [ Links ]

Nieri-Bastos, F. A., Horta, M. C., Barros-Battesti, D. M., Moraes-Filho, J., Ramírez, D. G., Martins, T. F. et al. (2016). Isolation of the pathogen Rickettsia sp. strain Atlantic rainforest from its presumed tick vector, Amblyomma ovale (Acari: Ixodidae), from two areas of Brazil. Journal of Medical Entomology , 53, 977-981. https://doi.org/10.1093/jme/tjw062 [ Links ]

Oscherov, E. B. , Bar, M. E., Milano, A. M. F., & Damborsky, M. P. (2006). Presencia de garrapatas del género Amblyomma (Ixodidae) en áreas naturales protegidas. Acta Bioquímica Clínica Latinoamericana, 3, 185. [ Links ]

Owen, D. (1968). Investigations: B. Parasitological studies. Laboratory Animal Center News Letter, 35, 7-9. [ Links ]

Parera, A. F. (2018). Los mamíferos de la Argentina y la region austral de Sudámerica. Segunda Edición. Buenos Aires: AP Ediciones Naturales. [ Links ]

Paterson, J. S. (1967). The guinea pig or cavy (Cavia porcellus L.). In UFAW staff (Eds.), The UFAW handbook on the care and management of laboratory animals, 3 rd Ed. (pp. 241- 287). London: Livingston and the Universities Federation for Animal Welfare. [ Links ]

Pérez, J. M. (2015). Orden Phthiraptera. Revista Ibero Diversidad Entomológica-SEA, 51, 1-11. [ Links ]

Ronald, N. C., & Wagner, J. E. (1976). The arthropod parasites of the genus Cavia. In J. E. Wagner, & P. J. Manning (Eds.), The biology of the guinea pig (pp. 201-209). Orlando, Florida: Academic Press. [ Links ]

Sánchez, J. P. , &, Lareschi, M. (2013). The fleas (Insecta: Siphonaptera), parasites of Sigmodontine rodents (Cricetidae) from northern Patagonia, Argentina. Comparative Parasitology , 80, 110-117. https://doi.org/10.1654/4576.1 [ Links ]

Sánchez, J. P. , & Lareschi, M. (2014). New records of fleas (Siphonaptera: Ctenophthalmidae: Rhopalopsyllidae and Stephanocircidae) from Argentinean Patagonia, with remarks on the morphology of Agastopsylla boxi and Tiarapsylla argentina. Revista Mexicana de Biodiversidad, 85, 383-390. https://doi.org/10.7550/rmb.42071 [ Links ]

Saraiva, D. G., Fournier, G. F., Martins, T. F. , Leal, K. P., Vieira, F. N., Câmara, E. M. et al. (2012). Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Experimental and Applied Acarology , 58, 159-166. https://doi.org/10.1007/s10493-012-9570-9 [ Links ]

Saunders, R. C. (1975). Venezuelan Macronyssidae (Acarina: Mesostigmata). Brigham Young University Science Bulletin , Biological Series, 20, 2. [ Links ]

Sinkoc, A. L., Brum, I. G. W., Moraes, W., & Crawshaw, P. (1998). Ixodidae parasitos de animais silvestres na regiao de Foz de Iguaçú, Brasil e Argentina. Arquivos do Instituto Biologico, 65, 29-33. [ Links ]

Smit, F. G. A. M. (1987). An illustrated catalogue of the Rothschild collection of fleas (Siphonaptera) in the British Museum (Natural History): with keys and short descriptions for the identification of families, genera, species and subspecies of the Order. Malacopsylloidea and Rhopalopsyllidae. Oxford, USA: Oxford University Press. [ Links ]

Tarragona, E. L., Mastropaolo, M. , Zurvera, D., Beldoménico, P. M. , & Guglielmone, A. A. (2018). Host-parasite association between Didelphis albiventris (Didelphimorphia: Didelphidae) and Ixodes loricatus (Acari: Ixodidae) in their southern ranges. Experimental and Applied Acarology , 75, 129-134. https://doi.org/10.1007/s10493-018-0248-9 [ Links ]

Tarragona, E. L. , Zurvera, D. , Manzoli, D. E., Correa, A. I., Delgado, A. R., Magni, C. et al. (2011). Inmovilización química y evaluación fisiológica de comadreja overa, Didelphis albiventris (Lund, 1841) silvestres de la provincia de Santa Fe, Argentina. Investigación Veterinaria , 16, 79-85. [ Links ]

Valim, M. P., Amorim, M., & Serra-Freire, N. M. (2004). Parasitismo por Acari e Phthiraptera em cobaios [Cavia Porcellus (Linnaeus, 1758)] de ambientes rural e urbano nos municípios de Silva Jardim e Duque de Caxias, Rio de Janeiro, Brasil. Brazilian Journal of Veterinary Research and Animal Science, 41, 240-246. https://doi.org/10.1590/s1413-95962004000400004 [ Links ]

Werneck F. B. (1948). Os malófagos de mamíferos. Parte 1: Amblycera e Ischnocera (Philopteridae e parte de Trichodectidae). Revista Brasileira de Biologia, Volume Special, 1-243. [ Links ]

Received: August 06, 2019; Accepted: December 04, 2019

*Autor para correspondencia: paoben.26_@hotmail.com (A.P. Benitez-Ibalo)

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License