Mastozoología Neotropical ISSN: 0327-9383 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Navone, Graciela T.; Notarnicola, Juliana; Nava, Santiago; Robles, M. del Rosario; Galliari, Carlos; Lareschi, Marcela AND HELMINTHS ASSEMBLAGE IN SIGMODONTINE FROM WETLANDS OF THE RIO DE LA PLATA, ARGENTINA Mastozoología Neotropical, vol. 16, núm. 1, enero-junio, 2009, pp. 121-133 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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ARTHROPODS AND HELMINTHS ASSEMBLAGE IN SIGMODONTINE RODENTS FROM WETLANDS OF THE RIO DE LA PLATA, ARGENTINA

Graciela T. Navone1*, Juliana Notarnicola1, Santiago Nava2, M. del Rosario Robles1, Carlos Galliari1, and Marcela Lareschi1

1 Centro de Estudios Parasitológicos y de Vectores, Calle 2 N° 584, 1900 La Plata, Buenos Aires, Argentina. CEPAVE (CCT- CONICET- La Plata; UNLP) *[Correspondencia: ] 2 Instituto Nacional de Tecnología Agropecuaria INTA, Rafaela, Santa Fé, Argentina.

ABSTRACT: The assemblage of arthropods and helminths, present in sigmodontine ro- dents () from a broad wetland area of the Río de la Plata, Argentina, was studied. A total of 250 sigmodontines were captured during a two-year sampling period: Scapteromys aquaticus and Oxymycterus rufus were the most abundant hosts, followed by nigripes, Akodon azarae, , and Deltamys kempi. There were 33102 parasites collected, corresponding with Rhopalopsyllidae fleas (Siphonaptera), Hoplopleuridae lice (Phtiraptera), and Macronyssidae , , and Trombiculidae chiggers (), the trematodes Echinostomidae, , and Dicrocoelidae, the Ciclophyllidea, the nematods Trichuridae, Spiruridae, Onchocercidae, Physalopteridae, Aspidoderidae, Oxyuridae, and Nippostrongylinae, and the thorny-headed worm Acanthocephala. A list of arthropods and helminths species associated with each species was given, as well as the prevalence and mean abundance. New host and geographic records were provided. The phenogram of the relationships of the parasite assemblages showed a high value of similarity between both species of Oligoryzomys, and between S. aquaticus and O. rufus. Variation of the values observed in the prevalence and the mean abundance of the host-parasite association suggests that there could be environ- mental barriers between the rodent populations, or that differential behavior of the host species (i.e. use of microhabitats, tropics behaviors) may influence these indexes. This knowledge may be used to determine targets for biological conservation and ecological impact of in the area.

RESUMEN: Ensamble de artrópodos y helmintos parásitos en roedores sigmodontinos de los humedales del Río de la Plata, Argentina. Se estudió el ensamble parasitario de artrópodos y helmintos en roedores sigmodontinos (Cricetidae) en una franja de los humedales del Río de la Plata, Argentina. Se capturaron un total de 250 roedores sigmodontinos durante dos años consecutivos. Scapteromys aquaticus y Oxymycterus rufus fueron los más abundantes, seguidos por , Akodon azarae, Oligoryzomys flavescens, y Deltamys kempi. Se colectaron 33102 parásitos correspondientes a pulgas Rhopalopsyllidae (Siphonaptera), piojos Hoplopleuridae (Phtiraptera), ácaros Laelapidae y Macronyssidae, garrapatas Ixodidae, y bichos colorados Trombiculidae (Ac- ari), trematodes Echinostomidae, Microphallidae y Dicrocoelidae, cestodes Ciclophyllidea, nematodes Trichuridae, Spiruridae, Onchocercidae, Physalopteridae, Aspidoderidae, Oxyuridae y Nippostrongylinae, y los gusanos espinosos Acanthocephala. Se detalla una lista de las asociaciones de artrópodos y helmintos con cada especie hospedadora y se dan las prevalencias y abundancias medias. Además, se mencionan nuevos registros geográficos y hospedatorios. Los fenogramas de similitud de los ensambles parasitarios mostraron altos valores entre ambas especies de Oligoryzomys y entre S. aquaticus y O. rufus. Variaciones en los valores de prevalencia y abundancia media observados en las asociaciones parásito-hospedador sugieren que podrían estar actuando barreras ambientales 122 Mastozoología Neotropical, 16(1):121-133, Mendoza, 2009 GT Navone et al. http://www.sarem.org.ar

entre las poblaciones hospedadoras, o que el comportamiento diferencial de las especies hospedadoras (i.e. uso de microhabitat, comportamiento trófico) puede estar influenciando dichos índices. Este conocimiento puede ser utilizado para identificar objetivos en la conservación y en el impacto ecológico del parasitismo en el área.

Key words. Ectoparasites. Endoparasites. Río de La Plata. Rodents. Wetlands.

Palabras clave. Ectoparásitos. Endoparásitos. Humedales. Río de La Plata. Roedores.

INTRODUCTION ever, most of these surveys in the wetland area deal with descriptions of new species and/or Colonization of a host species by a parasite records of new hosts. Lareschi (2000) de- species is a process that may take several scribed some parasite associations between generations. Its success depends on different arthropods and hosts (i. e. sigmodontine ro- factors, such as environmental conditions, age dents) from the Selva Marginal de Punta Lara, and sex of the host, or more complex ones, near the Río de la Plata. Moreover, Lareschi for example, the behavior and immune status et al. (2004, 2007) showed the association of the hosts (Poulin and Morand, 2004). Once between the arthropods Hoplopleura travassosi the host-parasite association is known, varia- Werneck, Gigantolaelaps wolffsohni tions of them can be detected as the presence- (Oudemans), and bacoti (Hirst) absence of the above mentioned association with the filarioid worms Litomosoides or variation in the indexes—prevalence, mean bonaerensis Notarnicola, Bain and Navone and abundance. Using the variability of these fea- L. oxymycteri Notarnicola, Bain and Navone, tures, it is possible to predict what host har- and suggested their potential role as natural bors what parasite (Poulin and Morand, 2004). vectors of the filarioids. In terrestrial habitats, environmental factors can The aim of this research is to study the also cause variation in parasite species rich- parasite assemblage (arthropods and helminths) ness among populations of the same host spe- present in the most representative sigmodontine cies (Krasnov et al., 1997). rodent species from a wetland area of the Río The wetlands of the Río de la Plata, Argen- de la Plata, Buenos Aires Province, to provide tina, comprise a forest of complex structure the prevalence and mean abundance of the with numerous species and strata (Menalled host-parasite associations, and to analyze the and Adamoli, 1995). This area is included in similarity of the parasite communities. New the Ecoregion of Delta and Paraná Island host-parasite associations are mentioned. (Burkart et al., 1999). Wild rodents are the most representative in the area, and MATERIALS AND METHODS at least 10 species are mentioned for the wet- lands living in different microhabitats ranging Studied area.—Samples were carried out on an from flooded to grassland habitats (Massoia, area besides the Río de la Plata, from Reserva 1961; Ringuelet, 1962; 1981; Gomez Villafañe Natural de Hudson (34° 45’ S, 58° 06’ W) to La et al., 2005). Several host-parasites associa- Balandra (34° 56’ S, 57° 42’ W). The area is char- acterized by lowlands throughout the margin of tions were reported from these rodents in the the Río de la Plata intercalated with coastal strips area. Among them, ticks, mites, fleas, nema- emerging from water. It displays periods of floods todes, and are mentioned (Sutton, originated mainly by the local rain, the dripping 1974; Castro et al., 1987; Sutton and Lunaschi, water from temporal creeks, and periodical south- 1994; Lareschi, 1996; Suriano and Navone, east winds, plus the freshet of the Río de la Plata 1996; Lareschi and Mauri, 1998; Notarnicola (Dascanio et al., 1994). A succession of vegetal et al., 2000; Robles and Navone, 2006). How- communities are disposed from the margin to in- PARASITES ASSEMBLAGE IN SIGMODONTINES 123

ner lands as follows; rushes, riverside grasslands, on the basis of the values of P and MA of 45 riverside scrubland, «sauzales», wetland forest, species or parasite species group (MVSP software). straw grassland, and grass pseudo-steppe, produc- ing heterogeneous microhabitats in the coast RESULTS (Cabrera and Dawson, 1944; Barrios and Moschione, 1993). A total of 250 rodents belonging to six spe- Hosts.—Rodents were trapped from April 1995 cies of were trapped in the area: to October 1996 during 30 trapping session. Cap- Scapteromys aquaticus Thomas (n = 130), tures were carried out by two of the authors (GN Oxymycterus rufus (Fischer) (n = 58), and ML) in accordance with regulations and poli- Oligoryzomys flavescens (Waterhouse) (n = cies of the Dirección de Administración y Difusión 27), Akodon azarae (Fischer) (n = 23), Conservacionista del Ministerio de Asuntos Oligoryzomys nigripes (Olfers) (n = 8), and Agrarios, Buenos Aires. Live-traps were distrib- Deltamys kempi Thomas (n = 4). Nineteen uted along two transects; 30 to 40 traps stations traps captured other mammals such as marsu- were set three meters apart from each other. Traps were bait-loaded with oiled bread and activated pials and rats. The total RAI in the area was for one night at each trapping session. A total of 11.7%. Scapteromys aquaticus and O. rufus 2303 night traps were used. In positive captures, were the most abundant hosts (RAI = 5.6%, the rodents inside their traps were placed in indi- and 2.5% respectively), followed by O. vidual plastic bags to avoid contamination with flavescens (RAI = 1.2), A. azarae (RAI = 1), ectoparasites from another host species. Then, they O. nigripes (RAI = 0.3), and D. kempi (RAI were sacrificed with sulfuric ether and frozen. After = 0.2). About 33 102 parasites (9603 collecting parasites, they were deposited at the arthropods and 23 499 helminths) were recov- Colección de Mastozoología, Museo de La Plata ered from these hosts and grouped in the taxa (CMMLP), and the Instituto de Limnología ILPLA, Buenos Aires, Argentina (see Appendix). U.F.J Siphonaptera, Phthiraptera, Acari, , Pardiñas from the Centro Nacional Patagónico, Cestoda, Nematoda, and Acanthocephala. Puerto Madryn, Argentina and CG identified the Table 1 details a list of the collected para- rodents. We followed Barquez et al. (2006) for the sites species (arthropods and helminths) from systematic of the species. six sigmodontine rodent species. Table 2 sum- Parasites.—Arthropods were recovered by ex- marizes P and MA of the collected parasites amining the furs under magnifying lens, preserved from the Río de la Plata’s wetlands. in 70º ethanol, and mounted on permanent slides. The body cavity and the viscera of hosts were Scapteromys aquaticus Thomas examined for parasites. Helminths were fixed in 10% formalin, and preserved in 70% ethanol. This host species was the most frequently Arthropods and helminths were identified follow- trapped in the area (RAI = 5.6%). Specimens ing the conventional techniques and bibliography were commonly captured in flooded trap-sta- of the genera and species level, except the tions, where rushes were dominant. The para- Acantocephala and nematode cysts. Voucher speci- site richness was 22 (10 arthropods species, mens were deposited in the Colección de 11 helminths species, and one helminth larva) Entomología (CEMLP), Colección de Helmintología (CHMLP) from Museo de La Plata, (Tables 1, 2). Argentina (see Appendix), and CEPAVE authors Among mites, Laelaps manguinhosi Fonseca collection. showed the highest P and MA (Table 2). The Data Analysis.—The relative abundance index lice Hoplopleura scapteromydis Ronderos, is (RAI) was estimated as follows: (number of trapped specifically associated with S. aquaticus, and rodent / number of nights x number of traps) x 100 showed high value of P and MA. On the other (Jones et al., 1996). Prevalence (P) and Mean hand, because ticks molt as well as eggs and Abundance (MA) with the standard deviation were immature stages of fleas occur out of the host’s calculated following Bush et al. (1997). Phenogram bodies, flooded soils constitute a barrier for of the relationships of parasite assemblages among six host species was constructed using WPGMA the development of these arthropods. Thus, on a similarity matrix (Morisita index) computed with the exception of Polygenis (Neopolygenis) 124 Mastozoología Neotropical, 16(1):121-133, Mendoza, 2009 GT Navone et al. http://www.sarem.org.ar

Table 1 List of the species of parasites (arthropods and helminths; * = presence) collected from six species of sigmodontine rodents. Abbreviations: SA, Scapteromys aquaticus; OR, Oxymycterus rufus; OF, Oligoryzomys flavescens; ON, Oligoryzomys nigripes; AA, Akodon azarae; DK, Deltamys kempi.

Parasite species Host species

SA OR OF ON AA DK

Arthropods Insecta Siphonaptera, Rhopalopsyllidae Polygenis (Neopolygenis) atopus (Jordan and Rothschild, 1922) * * * * * Polygenis (Neopolygenis) massoiai Del Ponte, 1967 * * Polygenis (Neopolygenis) frustratus Johnson, 1957 * * Polygenis (Polygenis) rimatus (Jordan, 1932) * Polygenis (Polygenis) axius axius (Jordan and Rothschild, 1923) * * Polygenis (Polygenis) bohlsi bohlsi (Wagner, 1901) * * Polygenis sp. * Phthiraptera, Anoplura, Hoplopleuridae Hoplopleura scapteromydis Ronderos, 1965 * Hoplopleura fonsecai Werneck, 1934 * Hoplopleura travassosi Werneck, 1932 * * Hoplopleura aitkeni Jonson, 1972 * Acari Laelapidae Androlaelaps fahrenholzi (Berlese, 1911) * * * * Androlaelaps rotundus (Fonseca, 1936) * Androlaelaps sp. 1 * Laelaps manguinhosi Fonseca, 1936 * * * * Laelaps paulistanensis Fonseca, 1936 * * * Gigantolaelaps wolffsohni (Oudemans, 1910) * * Mysolaelaps microspinosus Fonseca 1936 * * Macronyssidae (Hirst, 1913) * * * Ixodidae Ixodes loricatus Neumann, 1899 * * * * * Trombiculidae Eutrombicula alfreddugesi (Oudemans, 1920) * * * * Helminths Digenea Echinostomatidae Echinostoma platensis Sutton and Lunaschi, 1994 * Echinoparyphium scapteromae (Sutton, 1983) * * * * * Microphallidae Levinseniella (Monarrhenos) cruzi Travassos, 1920 * * * Dicrocoelidae Zoonorchis oxymycterae Sutton, 1983 * * Cestoda Ciclophyllidea, Hymenolepididae Rodentolepis sp. * * * Nematoda Trichuridae Trichuris laevitestis Suriano and Navone, 1994 * * Echinocoleus sp. * Pseudocapillaria sp. * PARASITES ASSEMBLAGE IN SIGMODONTINES 125

(Table 1 cont.)

Parasite species Host species

SA OR OF ON AA DK

Spiruridae Protospirura numidica criceticola Quentin et al., 1968 * * Onchocercidae (filarioids) Litomosoides oxymycteri Notarnicola et al., 2000 * Litomosoides bonaerensis Notarnicola et al., 2000 * * Physalopteridae Cysts located on intestinal external walls and mesenteries * Aspidoderidae Nematomystes rodentiphilus Sutton et al., 1980 * * Oxyuridae Syphacia sp. 1 * Syphacia carlitosi Robles and Navone, 2007 * Trichostrongylina, Nippostrongylinae Stilestrongylus sp. 1 * Stilestrongylus sp. 2 * * Stilestrongylus sp. 3 * Stilestrongylus flavescens Sutton and Durette-Desset, 1991 * * Stilestrongylus azarai Durette-Desset and Sutton, 1985 * Malvinema spp. * Suttonema sp. * Acanthocephala Specimens undetermined * atopus (Jordan and Rothschild), low values of Physalopteridae were recovered either from the P and MA of these last groups of arthropods external intestine walls of the specimen or may be related to environmental conditions. attached to mesenteries. The presence of these Concerning the helminths of S. aquaticus larval stages indicates that rodents are inter- (Table 1), six of 12 species found (three trema- mediate hosts. Adults Physalopteridae from todes, one cestode, one nematode, and one Turgida turgida Rudolphi were found by acanthocephala) have indirect life cycles, Navone (unpublished data) in Didelphis which include an intermediate host acquired albiventris Lund and Lutreolina crassicaudata through the food-web. Among the remaining (Desmarest) from this wetland area. This find- worms, the nippostrongylines nematodes and ing suggests that marsupials could possibly be Nematomystes rodentiphilus Sutton, Chabaud the final hosts. Besides, S. aquaticus is a new and Durette-Desset have direct life cycles. Both host record for Rodentolepis sp., Echinocoleus nematodes displayed the highest P and MA sp., and the Physalopterinae cysts. (69 to75%, and 36.9-47.2 respectively) (Table 2). These nematodes are small worms, para- Oxymycterus rufus (Fischer) sitizing the small intestine and the caecum, respectively. In contrast, Trichuris laevitestis Oxymycterus rufus was the second species in Suriano and Navone is a larger nematode and abundance captured in the wetland area (RAI they frequently occurred with low P and MA = 2.5). The parasite species richness reached (8.5% and 0.3, respectively). Cysts of nema- 19 (11 species of arthropods and eight of todes containing larval stages of helminths) (Tables 1, 2). 126 Mastozoología Neotropical, 16(1):121-133, Mendoza, 2009 GT Navone et al. http://www.sarem.org.ar ents from the wetlands of 3.9 ± 1 - - 0.4 ± 6.1 - - 0.6 ± 0.7 - - 0.2 ± 7.4 - - 21.7 43.5 13.0 1.7 ± - - 25 0.25 ± 0.5 4.1 ± 2.60.1 ± 0.3 -0.1 ± 0.3 ------19.8 ± (19.8) - - - - 62.5 87.5 12.5 Host species 2.1 ± 2 75 2.7 ± 2.6 - - - - 3.1 ± 30 0.3 ± 0.5 0.3 ± 0.5 50 0.8 ± 1.3 - - - - 0.7 ± 1.6 100 12.1 ± 4.5 - - - - 0.3 ± 0.6 25 0.8 ± 1.8 4.3 0.1 ± 0.4 - - 23.1 26.9 11.1 Table 2 6.4 ± 29 ------252 ± 1 0.5 ± 1.8 ------1.9 ± 3.6 7.7 0.1 ± 0.3 - - 0.4 ± 1.5 -0.5 ± 1.8 ------50 - 0.5 ± 0.6 - - 14.8 ± 68.8 3.80.2± 0 - - 46.5 41.4 8.4 ± 3 - - 12.5 18.9 15.5 10.3 0.4 ± 1 3.4 0.1 ± 0.4 0.5 ± 2 1.2 ± 3.6 0.3 ± 1.4 ------18.3 ± 25.6 1.70.1 ± 0 19.2 ± 62.3 17.8 ± 52.2 S. aquaticusrufus O. flavescens O. nigripes O. azarae A. kempi D. ------6.9 - 0.1 ± 0.3 - - 3.8 -0.2± 0 1.7 - - 0 ± 0.1 3.8 0 ± 0.2- - - - - 61.5 1 ------47.8 0.2 ± 3 ------56.5 ------1.7 - 0.1 ± 0 - 23.1 - - 76.9 65.4 2 ± 2 100 - - 8.6 1.6 ± 6.8 - - - - 4.3 0.3 ± 0.9 - - 3 ± 1.2 0 8.6 0.2 ± 0.6 ------20 2.8 ± 10.8 5.21.3 ± 0.2 6.1 0.2 ± 1.4 - - 7.4 0.3 ± 1.3 - - - - 0.7 0 ± 0.1 ------50 0.25 ± 0.5 0.7 0.1 ± 0 17.2 3.1 0 ± 0.2 3.4 0 ± 0.3 7.7 0.1 ± 0.3 8.5 0.3 ± 1.7 ------13 0.3 ± 0.4 - - 21.5 50.7 41 ± 19 ------28.5 75.3 16.9 42.3 13.1 21.5 P (%) MA P (%) MA P (%) MA P (%) MA P (%) MA P (%) MA sp. - - 13.8 sp. 14.6 1.6 ± 0.56 ------sp. 1 ------50 1.75 ± 2.9 sp. 13 0.3 1.1 sp. ------4.3 0 ± 10.5 - - Parasites species Protospirura n. criceticola Hoplopleura scapteromydis Polygenis (N.) frustratus Polygenis Hoplopleura fonsecai Polygenis (N.) atopus Polygenis (P.) rimatus Polygenis (P.) a. axius Polygenis (P.) b. bohlsi Hoplopleura travassosi Polygenis (N.) massoiai Androlaelaps fahrenholzi Hoplopleura aitkeni Androlaelaps rotundus Androlaelaps Laelaps manguinhosi Laelaps paulistanensis Ornithonyssus bacoti Gigantolaelaps wolffsohni Mysolaelaps microspinosus Ixodes loricatus Eutrombicula alfreddugesi Echinostoma platensis Echinoparyphium scapteromae Trichuris laevitestis Echinocoleus Pseudocapillaria Rodentolepis Levinseniella (M.) cruzi Zoonorchis oxymycterae the Río de la Plata, Buenos Aires. Prevalence (P) and Mean Abudance (MA) ± the standard deviation of parasites collected from six species sigmodontines rod PARASITES ASSEMBLAGE IN SIGMODONTINES 127

Only one specimen of O. rufus was parasit- ized with the lice Hoplopleura fonsecai Wernerck. Previous studies reported the ab- sence of these arthropods parasitizing O. rufus during a monthly study in Punta Lara (Lareschi, 1996). However, in a northern locality (i.e. Otamendi-Buenos Aires), also in a monthly study, it was registered a prevalence of 40% (Lareschi and Sánchez López, 1999). Lice are obligatory parasites and all the stages of their life cycle occur on the host, so the coloniza- tion of a new host takes place by frequent physical contact among them. The differences of the P observed in H. fonsecai may suggest the presence of environmental barriers between

6.2 ± 5 - - - - the northern populations of O. rufus 69.4 ± 23.5 - -(Otamendi) - - and the southern in the wetland localities. Larvae of Eutrombicula alfreddugesi 87.5 Oudemans are generalist parasites of amphib- ians, reptiles, birds, mammals, and also hu- mans (Daniel and Stekol’nikov, 2004). These Host species chiggers were collected from four out of the

3.8 ± 6.5 1.8 ± 7.8 - - -six host - species - trapped - in this study (Table 2). However, it was mainly associated with S.

11.1 aquaticus and O. rufus, the more abundant hosts in the area. The remarkable seasonality of this chigger, with a preference toward spring and summer and absence in winter (Lareschi, 2.6 ± 8 ------4.8 ± 27 - - - -2000), -may affect - values - of total - P and MA, which are lower when each season is indepen- dently considered. Among the mites, Androlaelaps fahrenholzi (Berlese) and O. bacoti showed the highest values of P and MA

2.4 -(Table -2). ------Regarding to helminths, O. rufus harbored

47.2 ± 77.5 1.70.3± 0.3 - -three - species - of trematodes - and - one - cestode - species with indirect life cycles. These para- S. aquaticusrufus O. flavescens O. nigripes O. azarae A. kempi D. ------95.6 1.5 ± 81.6 ------100 126.7±168.6 100 -- - -- 43.1 - - - -sites 34.6 - are acquired - with - the diet - indicating - that 4.3 0.1 ± 0.6 - - 36.9 63 ± 21.3 ------75.4 P (%) MA P (%) MA P (%) MA P (%) MAtheir main P (%) MA food P (%) consists MA in larval insects, mollusks, and small vertebrates, which are the usual intermediate hosts. Three of four spe- cies of nematodes collected from this host

S. flavescens displayed direct life cycles. The fourth, the filarioid L. oxymycteri, is transmitted by a azarai

vector, probably either the O. bacoti or sp. 3 ------7547.4 ± 28.7 sp. 1 sp. 2 +

spp.another 6.1arthropod 2.6 39.4 - ectoparasite - as -stated in ------sp. - - 18.9 sp. 1 -Lareschi - et al. - (2003, 2007). - Most helminths showed low P and MA with the exception of the filarioid (43.1% and 4.7 respectively) Parasites species Malvinema Suttonema Acanthocephala 6.9 0.2 ± Stilestrongylus Stilestrongylus Stilestrongylus Litomosoides oxymycteri Stilestrongylus Litomosoides bonaerensis Cysts of PhysalopteridaeNematomystes rodentiphilus Syphacia carlitosi 20 2.3 ± 11.3 ------Syphacia 128 Mastozoología Neotropical, 16(1):121-133, Mendoza, 2009 GT Navone et al. http://www.sarem.org.ar

(Table 2). Zoonorchis oxymycterae Sutton was Oligoryzomys nigripes (Olfers) originally described parasitizing O. rufus from Few specimens were trapped in the area (RAI Otamendi. In the present study, it was also = 0.3). The species richness was 11 (8 found widening its known geographical distri- arthropods species and three helminths) bution. Moreover, Echinoparyphium (Tables 1, 2). Concerning arthropods, O. scapteromae (Sutton), Levinseniella bacoti and Ixodes loricatus Neumann showed (Monarrhenos) cruzi Travassos, Rodentolepis low P and MA values (Table 2). On the other sp., and Pseudocapillaria sp. are new host hand, the lice H. travassosi as well as the flea records. P. (N.) atopus and the mites G. wolffsohni, Laelaps paulistanensis, and M. microspinosus, Oligoryzomys flavescens (Waterhouse) showed high values of P (62.5-100%) and low to high MA (1.7-19.8) (Table 2). Oligoryzomys flavescens is a common species Three helminths species were recovered from in wetlands from Buenos Aires to Misiones Ol. nigripes, in contrast to the five species provinces (Massoia, 1973). It was the third found in O. flavescens. Filarioids and species in abundance in the area (RAI = 1.2). nipostrongylines showed the highest P (Table The total species richness was 16 (11 arthro- 2). The filarioid L. bonaerensis corresponds pod species and five helminths) (Tables 1, 2). to the same species found in O. flavescens The richness was as high as that from wetlands but differs from that recovered from O. rufus. The mites G. wolffsohni and from O. nigripes in Misiones Province Mysolaelaps microspinosus Fonseca were col- (Notarnicola and Navone, 2002). lected with high P (76.9% and 65.4%, respec- tively) and MA (2 and 2.1, respectively). The Akodon azarae (Fischer) louse H. travassosi was also collected in high number of hosts (P = 61.5%, MA = 3.1). In The relative abundance of A. azarae in the contrast, ticks, chiggers, and fleas—with the area was slightly lower than that from O. exception of P. (N.) atopus—were present with flavescens (RAI = 1 vs. 1.2). Akodon azarae low P and MA (Table 2). harbored six arthropod species and five helm- Five species of helminths were recovered inth species (Tables 1, 2). from O. flavescens trapped in the area (Table Hoplopleura aitkeni Johnson, I. loricatus, 1). Nippostrongylines were present with 100% and the mite Androlaelaps rotundus (Fonseca) of P and a high MA. In contrast, E. parasitized A. azarae with higher value of P scapteromae and Protospirura numidica than those observed for each of these criceticola Quentin, Karini and Almeida were arthropods in the remaining host species recovered with low P and MA. These findings trapped in the current study (Table 2). Ixodes pointed out that these rodents include in their loricatus was collected from five out of the diet not only vegetables and seeds but occa- six species of sigmodontines trapped in this sionally also some insect larval stages and study except D. kempi (Table 1). However, mollusks. The filarioid L. bonaerensis ap- immature stages of this were frequently peared with an intermediate P (34.3%) and found parasitizing A. azarae confirming that low MA (3.8). Previous studies registered immature stages are associated with this host. positive associations between L. bonaerensis This result agrees with previous findings where with both, the louse H. travassosi and the mite the immature stages are mainly associated with G. wolffsohni in Hudson. But no association Akodon species and adults with marsupials was observed in another locality from the (Lareschi, 1996; Nava et al., 2004; wetlands of the Río de La Plata (Lareschi et Beldomenico et al., 2005). al., 2003; 2007). E. scapteromae, P. n. Two species of trematodes were recovered criceticola, and Syphacia sp. are new host with low P and MA (Table 2), indicating that records. these rodents probably include mollusks or PARASITES ASSEMBLAGE IN SIGMODONTINES 129

small vertebrates in their diet occasionally. In Data Analysis contrast, nippostrongylines were the most prevalent and registered the highest MA (P = The phenograms obtained using P and MA 95.6%, and MA = 81.6). The remaining nema- values showed similar relationships of the todes found in this area either registered low principal nodes, however D. kempi changed P and MA or they were absent (Table 2). Both the position (Figs. 1A, B). The parasite as- trematodes, E. scapteromae and Z. semblages between both species of oxymycterae are reported in A. azarae for the Oligoryzomys, and between O. rufus and S. first time. aquaticus are the more similar. Akodon azarae unites to this last node, while the assemblage Deltamys kempi Thomas of D. kempi presented the lowest similarity regarding the other host species (Fig. 1A) or Only four specimens of D. kempi were cap- conformed a cluster of low similarity values tured in the area (RAI = 0.2). They harbored with O. rufus, S. aquaticus, and A. azarae (Fig. three arthropods and three helminths species 1B). (Tables 1, 2). Individuals were parasitized with fleas and DISCUSSION one species of Androlaelaps. The morphology of this mite differs from the other known spe- The assemblage of parasites of the cies of Androlaelaps but resembles A. rotundus sigmodontine rodents reported in this study is found frequently in the area (ML unpublished characteristic of the Río de la Plata wetlands, data). However, A. rotundus is known to be a in agreement with previous findings from pel- complex of species as stated Gettinger and lets of Tyto alba (Strigiforme, Aves) in the Owen (2000) in Paraguay. area (Udrizar Sauthier et al., 2005). This is the first time reporting helminths Concerning ectoparasites, previous studies parasitizing D. kempi. The finding of the trema- listed these arthropod species associated with tode L. (M.) cruzi and the flatworm a variety of hosts (Castro et al., 1987; Lareschi Rodentophilus sp. indicates a diet constituted and Mauri, 1998) suggesting that they are by mollusks and arthropod larval stages. The generalists. In the present study, most of the nematode Stilestrongylus sp. 3 appeared with arthropods were collected from two or more high P (75%), similarly to the other host species. However, as stated Poulin et al. sigmodontine rodents in the area. (2008), differences in the values of MA allow

AB

Fig. 1. Phenograms based on prevalence matrix data (A) and mean abundance matrix data (B) of the six host rodent species. See abbreviations in Table 1. 130 Mastozoología Neotropical, 16(1):121-133, Mendoza, 2009 GT Navone et al. http://www.sarem.org.ar to identify principal versus auxiliary hosts. invertebrates. Moreover, pieces of inverte- Then, among others, in the present study S. brates, mainly coleopterans were observed in aquaticus was identified as the principal host the stomach of these rodents during the dis- of L. manguinhosi, while A. azarae was of A. sections. This observation also agrees with the rotundus. behavior of S. aquaticus and O. rufus, which Among helminths, nipotrongylines, and are frequently trapped near rushes and meadow filarioids are host-specific. The former group strands while A. azarae, Oligoryzomys spp. was collected from all host species harboring and D. kempi were trapped on graminoid grass- a specific complex (Table 1). In contrast, land. species of filarioids were found parasitizing The parasite assemblages from both species only O. rufus and Oligoryzomys spp. in the of Oligoryzomys are the more similar, consti- study area. These findings agree with those tuting the same node in both, P and MA from the northern locality Otamendi phenograms (Figs 1A, B). This finding could (Notarnicola, 2004). Thus, S. aquaticus, A. be explained as a result of their phylogenetic azarae, and D. kempi were not susceptible to affinity or by sharing the same microhabitats acquire filarioids in the wetlands. —arboreal and tall grass climbers. The nodes Because wetlands exhibit periods of flood, conformed by S. aquaticus and O. rufus are sometimes the water is retained for a long time. present in the P and MA phenograms with a The frequency and timing of floods determine lower similarity than those from Oligoryzomys either the absence or low abundance of ticks, spp. This similarity probably is a result of the fleas, and trichurids. Fleas and trichurids are convergence of their use of microhabitats in dominant in arid areas (Lareschi et al., 2004; this area, such as wet grasslands and borders Robles et al., 2006). Although parasite com- of flooding areas. The remaining species, A. munities retain their components along host azarae and D. kempi, showed a different po- distribution, characteristics of microhabitats sition in the phenogram depending on the data such as the hydroperiod and presence of other matrix used (P or MA data). However, the mammals may produce some changes in the similarity was much lower compared with the composition of communities. other nodes. The parasite assemblages of A. From another point of view, it can be in- azarae and D. kempi are different from those ferred the compound microhabitat and the diet of S. aquaticus-O. rufus. This result indicates of a host by knowing the arthropod and helm- that these rodent species use different micro- inths infracommunity. For example, the pres- habitats, even though they are sympatric spe- ence of immature stages of I. loricatus para- cies. The topologic instability of D. kempi sitizing the sigmodontines indicates that mar- observed in the phenograms could be related supials are frequent in the area, as mentioned to the small sample size. Nava et al. (2004), and Beldomenico et al. Not only wetlands are main resources of (2005). Moreover, cysts of the nematodes water, they also constitute important reservoirs Physalopteridae, whose adults are parasites of of biodiversity due to a variety of microhabi- the marsupials, were also recovered from these tats (Schnack, 2001). In this study, wetlands rodents. Relating to the diet, larval infective from the Río de la Plata display a high stages of trematodes as well as some nema- biodiversity of parasites associated with todes develop in mollusks and coleopterans sigmodontine rodents. Despite the complexity respectively. The finding of these parasites in of the area studied, it was possible to establish S. aquaticus and O. rufus with intermediate P the host-parasite associations and to explain and MA suggest that they might include im- the variability observed between the popula- portant quantities of invertebrates on their tions of the sigmodontines. This knowledge diets. Akodon azarae, Oligoryzomys spp., and can be used as target for biological conserva- D. kempi showed low P and MA of these tion and ecological impact of parasitism in the parasites indicating they occasionally include area (Schnack, 2001; Hugot et al., 2001). PARASITES ASSEMBLAGE IN SIGMODONTINES 131

AKNOWLEDGEMENTS Buenos Aires. Editorial L.O.L.A. (Literature of Latin America), Argentina, 97 pp. HUGOT JP, P BAUJARD, and S MORAND. 2001. We thank Cecilia Ezquiaga that helped in the prospection; Biodiversity in helminths and nematodes as a field to Ulyses Pardiñas and Julia Diaz for the critical reading of study: an overview. Nematology 3:199-208. of the manuscript; to Lucas Garbin for the English lan- JONES C, W McSHEA, M CONROY, and T KUNZ. guage revision. This investigation was financed by the 1996. Capturing mammals. Pp 115-155, in: Mea- CONICET (PIP 3000) and the UNLP (N363). suring and monitoring biological diversity. Standard methods for mammals (DE Wilson, FR Cole, JD LITERATURE CITED Nichols, R Rudron, M Foster, eds.). Smithsonian Institution Press, Washington and London. BARQUEZ RM, MM DÍAZ, and RA OJEDA (eds.). KRASNOV BR, GI SHENBROT, SG MEDVEDEV, VS 2006. Mamíferos de Argentina. Sistemática y VATSCHENOK, and IS KHOKHLOVA. 1997. Host- Distribución. 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Recibido 31 mayo 2007. Aceptado 21 abril 2008. Editor asociado: UFJ Pardiñas PARASITES ASSEMBLAGE IN SIGMODONTINES 133

APPENDIX

Host species

Material deposited in the Colección de Mastozoología, Museo de La Plata (CMMLP), with number of collection (MLP) and field numbers corresponding to the localities (B: La Balandra; H: Hudson, PB: Palo Blanco, PL: Punta Lara, and T: Los Talas); and Instituto de Limnología de La Plata (ILPLA). Akodon azarae: B 014, 047, 050, 053, 056, 064; H 006, 007, 008, 016, 024, 035, 047; PL 334, 335, 336, 340, 341; T 055; ILPLA 181, 182, 185, 190. Deltamys kempi: H 064; T050; ILPLA 179, 180. Oligoryzomys flavescens: MLP 08.IV.97.52, 10.VIII.00.10, 10.VIII.00.09, 05.XII.01.33, 01.X.01.11, 02.X.01.01, 01.VIII.00.29, 01.VIII.00.35, 01.VIII.00.37, 08.X.97.51, 01.VIII.00.33, 01.VIII.00.28, 01.VIII.00.36, 08.X.97.53; B 010, 046, 055, 067, 073, 080; H 063; PB 018, 002, 010; PL 310, 323, 338. Oligoryzomys nigripes: MLP 08.VIII.00.10, 08.IV.97.59, 08.IV.97.58, 01.VIII.00.31, 01.VIII.00.34, 01.VIII.00.30, 01.VIII.00.27; H 044. Oxymycterus rufus: MLP 20.XII.00.22, 20.XII.00.23, 20.XII.00.21, 08.IV.97.36, 25.IV.01.02, 20.XII.00.20, 08.IV.97.43, 08.IV.97.41, 05.XII.01.32, 08.VIII.00.04, 08.IV.97.25, 08.IV.97.40, 08.IV.97.38, 08.IV.97.26, 08.IV.97.33, 08.IV.97.28, 08.IV.97.39, 08.IV.97.24, 26.V.99.08, 08.IV.97.31, 08.IV.97.29, 08.IV.97.34, 08.VIII.00.03, 08.IV.97.27, 08.IV.97.23, 08.IV.97.37, 08.IV.97.32, 08.IV.97.44, 08.IV.97.72, 17.XIII.01.03, 17.XII.01.05, 17.XIII.01.02, 17.XII.01.06, 08.IV.97.35; B 048, 058, 061, 063, 068; H 028, 036; PL 301, 302, 303, 304, 305, 307, 309, 314, 318, 322, 324, 342; ILPLA 163, 164,165, 166, 170. Scapteromys aquaticus: MLP 08.IV.97.05, 08.IV.97.10, 08.IV.97.12, 08.IV.97.11, 08.IV.97.13, 08.IV.97.03, 08.IV.97.04, 08.IV.97.17, 08.IV.97.19, 08.IV.97.15, 08.IV.97.01, 08.IV.97.02, 08.IV.97.18, 08.IV.97.20, 08.IV.97.16, 08.IV.97.14, 08.IV.97.07, 08.IV.97.22, 08.IV.97.06, 08.IV.97.08, 08.IV.97.21; B 001, 003, 004, 005, 006, 007, 008, 009, 016, 017, 026, 027, 028, 029, 030, 031, 032, 033, 038, 039, 040, 041, 042, 043, 052, 057, 059, 062, 069, 070, 071, 072, 074, 075, 077, 078; H 033, 053, 055, 021, 023; PB 000, 007, 015, 016, 019, 020, 022, 023, 024, 025, 026, 027, 028, 029, 030, 031, 033, 034, 035, 036, 037, 038, 039, 040, 041, 042; PL 306, 308, 313, 316, 319, 320, 325, 339; T 001, 003, 005, 006, 007, 008, 009, 011, 014, 020, 021, 022, 023, 026, 027, 029, 030, 031, 033, 035, 036, 037, 039, 040, 041, 042, 043, 044, 045, 046, 053, 056; ILPLA 188, 189.

Parasite species Material deposited in the Colección de Helmintología Museo de La Plata (CHMLP) with the following numbers: Litomosoides bonaerensis—CHMLP 4610 Litomosoides oxymycteri—CHMLP 4611 Trichuris laevitestis—CHMLP 5625-5629. Syphacia carlitosi—CHMLP 5545-5551.

Note: For revision of the specimens deposited in the Colección de Entomología Museo de La Plata (CEMLP) contact Dr. Norma Diaz with the numbers of the host collection above mentioned.