Printer Friendly

Nuevos registros hospedatorios y de distribucion geografica de especies de Trichuris (Nematoda: Trichuriidae) de roedores de Argentina con un resumen actualizado de los registros en America.

NEW HOST RECORDS AND GEOGRAPHIC DISTRIBUTION OF SPECIES OF Trichuris (NEMATODA: TRICHURIIDAE) IN RODENTS FROM ARGENTINA WITH AN UPDATED SUMMARY OF RECORDS FROM AMERICA

INTRODUCTION

Species of Trichuris Roederer, 1761 (Nematoda: Trichuridae) have a cosmopolitan distribution and parasitize a broad range of mammalian hosts (Cafrune et al., 1999; Anderson, 2000). Among these, the most common species are Trichuris trichiura (Linnaeus, 1758) from humans, and T muris (Schrank, 1788), T ovis (Abildgaard, 1795), T suis (Schrank 1788), and T. vulpis (Froelich, 1789) from synanthropic and domestic animals (e.g. Knight, 1971; Beer, 1976; Bundy and Cooper, 1989; Callejon et al., 2010). Although, the prevalence and intensity of Trichuris in a host population depend on many factors, host immunologic status, behavior, areas with inadequate sanitation (food and fecal deposition areas mixed); the characteristics of its life cycle and environmental limiting factors have been the main aspects used to explain the geographical distribution (Bundy et al., 1988; Bundy and Cooper, 1989; Grencis et al., 1993; Anderson, 2000).

Whipworm eggs are deposited from host feces to the soil where infective larvae develop within the egg. Development of this larval stage has been shown to be influenced by temperature. Following ingestion of infective eggs by the host, all subsequent larval development to the adult stage occurs in the mucosa of the caecum and colon (Beer, 1973; Bundy and Cooper, 1988, 1989). Infections by trichuriasis are more prevalent in warm and moist tropical regions than in other parts of the world, and occur mainly in North and South America (Bundy and Cooper, 1988, 1989). However, most records are from medical and veterinary surveys (e.g. Bundy and Cooper, 1988; Traub et al., 2004; Gamboa et al., 2005), and comparatively few studies have been carried out on natural infections of Trichuris from wild hosts. In addition, many geographical areas have not been surveyed for Trichuris. Current distribution of the genus might reflect the absence of sample effort rather than the absence of infection (Bundy and Cooper, 1989).

Argentina is the second largest country in South America by land area, after Brazil, and exhibits a wide variety of soil types and climatic conditions (Bertonatti and Corcuera, 2000). The generally temperate climate ranges from subtropical in the north to subpolar in the far south and these environments include different eco-regions. Under natural conditions the rate of development of Trichuris species in this country may differ significantly from the optima, depending on the geographical distribution.

In this country, 8 species of Trichuris have been described and recorded from rodents (Morini et al., 1955; Boero and Boehringer, 1967; Suriano and Navone, 1994; Robles et al., 2006; Robles, 2011; Robles et al., 2012b). The only two records of this genus from wild hosts in other orders are Trichuris tenuis Chandler, 1930 from Lama glama and Vicugna vicugna (Artiodactyla; Cafrune et al., 1999) and T. campanula Linstow, 1889 from Oncifelis geoffroyi (Carnivora; Beldomenico et al., 2005). In general, the information available from many mammalian hosts is poor, hidden and scattered, making it difficult to evaluate the distribution and geographical gaps of the species of Trichuris.

Several parasitological studies on Sigmodontinae rodents (Cricetidae) have been carried out in Argentina in recent years (e.g. Robles and Navone, 2010; Notarnicola and Navone, 2011; Digiani et al., 2012; Robles et al., 2012a, 2012c; Digiani et al., 2013) and among these, three dealt with the taxonomy of Trichuris (Robles and Navone, 2006; Robles et al., 2006; Robles, 2011). However, these are only partial records, because several host species and Trichuris species are still under study.

In this paper, we provide new host and geographical records for Trichuris species from sigmodontine rodents of Argentina. Moreover, we present comprehensive data on previous records of the genus from rodents in North and South America, mainly in Argentina.

MATERIALS AND METHODS

Studied area

This includes the Northeast of Argentina, approximately between 26[degrees] and 35[degrees] S, politically covering the eastern Formosa, Chaco and Santa Fe provinces, the northern Buenos Aires province and Misiones, Corrientes and Entre Rios provinces. Also, the studied area includes the south of Argentina (Patagonia), approximately between 38[degrees] and 54[degrees] S, embracing Chubut, Neuquen, Rio Negro, Santa Cruz and Tierra del Fuego provinces (see Appendix 1, supplementary material for additional details on localities).

Hosts

Sigmodontine rodents were trapped during different field works between 2007 and 2010 (see collectors and support in acknowledgements). Many specimens are still being studied, but partial results were analyzed. Species of hosts with a very low representation (< 5) have not been considered in this paper (except Chelemys macronyx with n = 3). A total of 563 specimens were examined for Trichuris. From the northeast area, 493 specimens belonging to 17 species from 29 localities and 7 provinces were examined as following: Akodon azarae (n = 118) [A. azarae bibianae (n = 12), A. azarae hunteri (n = 106)], Akodon philipmyersi (n = 14), Bruceppatersonius sp. (n = 6), Calomys sp. (n = 13), Euryoryzomys russatus (n = 8), Holochilus brasiliensis (n = 5), H. chacarius (n = 13), Necromys lasiurus (n = 109), Necromys obscurus (n = 11), Nectomys squamipes (n = 5), Oligoryzomys flavescens (n = 37), O. fornesi (n = 10), O. nigripes (n = 71), Oxymycterus rufus (n = 45), Scapteromys aquaticus (n = 5), Sooretamys angouya (n = 8), Thaptomys nigrita (n = 15). From Patagonia we examined 70 specimens belonging to 8 species from 14 localities and 5 provinces as following: Abrothrix hirta (n = 12), A. olivacea (n = 19), Akodon dolores (n = 5), Chelemys macronyx (n = 3), Eligmodontia morgani (n = 6), Euneomys sp. (n = 6), Oligoryzomys longicaudatus (n = 10), Phyllotis xanthopygus (n = 9) (see Appendix 1, supplementary material).

Parasites

Nematodes were collected from the large intestine and caecum and preserved in 70% ethanol. For identification, the worms were prepared and identified following Robles et al. (2006), Robles and Navone (2006) and Robles (2011). Voucher specimens were deposited in the Coleccion de Helmintologia from Museo de La Plata, Argentina (CHMLP).

Data analysis

Quantitative parameters of prevalence (P = specimens parasitized/specimens examined *100), intensity (I = number of parasites in a single infected host), mean intensity (MI = number of parasites/specimens parasitized) and mean abundance (MA = number of parasites/specimens examined) were calculated according to Bush et al. (1997) for each host species and locality (Table 1). Prevalence, MI, I and MA for host species and studied area were given in the text. Prevalence differences were compared by the [chi square] test, and the data were analyzed by use of the Chi squared test employing the correction of Yates or by use of Fisher's exact test (positive cases <5), considering significant at p < 0.05. Statistical analysis was performed with EpiInfo[TM] 7.

RESULTS

Ten species of sigmodontine rodents from Argentina were parasitized with species of Trichuris. Three species of Trichuris were identified to the specific level, and at least 3 others were studied in detail, although these could not be identified to the species level (Table 1).

Published and new records for Trichuris in Argentina are shown in Fig. 1 (also see Tables 1 and 2 for species references). Records of Trichuris from the literature were summarized for Argentina in Table 2 and those for North and South America in Table 3.

Akodon azarae bibianae, A. azarae hunteri and N. lasiurus were parasitized with Trichuris laevitestis Suriano and Navone, 1994. A. azarae bibianae and N. lasiurus are new host records, and 11 localities are new geographical records (Table 1). The total P, MI and MA of T. laevitestis in all host species were 11.9%, 4.03 and 0.48, respectively; and in each host species: A. azarae 16.9%, 3.85 and 0.65 and N. lasiurus 6.42%, 4.57 and 0.29, respectively. T. nigrita were parasitized with a species of Trichuris. This host and Refugio Mocona represent new records for this nematode (Table 1). General features of these specimens suggest that they belong to Trichuris navonae Robles, 2011. However, some diagnostic measurements (in millimeters) such as spicule length (1.9-2.3), distal cloacal tube length (1.7-2.1), proximal cloacal tube lengths (1.2-1.7), present ranges higher than those previously recorded for T. navonae from A. montensis (1.3-2.1, 1-1.9, 0.75-1.5; respectively), verified through their ratios with the posterior portion of body and total body lengths. For this reason, these specimens are listed provisionally as Trichuris cf. T. navonae until more detailed morphometric analyses and molecular comparative studies determine whether they are cryptic species. The P, MI and MA of T. cf. T. navonae in the population of T. nigrita were 66.6%, 1.9 and 1.26, respectively.

[FIGURE 1 OMITTED]

Phyllotis xanthopygus xanthopygus were parasitized with another species of Trichuris. This host subspecies represents a new host record for this nematode. In addition, these results add a new locality and province, Cerro Corona and Rio Negro, respectively (Table 1). General features of these specimens suggest that they belong to Trichuris pardinasi Robles, Navone and Notarnicola, 2006. However, some morphometrical discrepancies (in millimeters) such as spicule lengths were observed (2.5-3.3 in P x. xanthopygus vs. 3.6-5.2 in P bonariensis and P. x. vaccarum). For this reason, these specimens are listed provisionally as Trichuris cf. T. pardinasi. It would be useful to obtain new samples and data from other sources (i.e. genetic data). The P, MI and MA of T. cf. T. pardinasi in P. x. xanthopygus were 28.6%, 10 and 2.86, respectively.

Sooretamys angouya, N. obscurus, H. chacarius, and C. macronyx we re parasitized, each one with 1 species of Trichuris. These findings contitute 4 new host records and 4 new locality records (Table 1). Trichuris specimens from the first 3 host species listed above are mainly characterized by the absence of a spicular tube, a spinose spicular sheath (spines very small, densely arranged), and a slightly protusive or nonprotusive vulva. The Trichuris specimens from C. macronyx are characterized by the presence of a spicular tube, a spinose spicular sheath (spines very small, densely arranged), and a protusive vulva; along with morphometric characters. Morphologically these specimens correspond to 4 different species of Trichuris, suggesting the presence of 2 new species, one from S. angouya and one from H. chacarius; and 2 preliminary unidentified species, one from N. obscurus and one C. macronyx. Until new samples are obtained and molecular comparative studies are concluded these species are listed here as Trichuris sp. The P, MI and MA of the species of Trichuris were in S. angouya, 50%, 4 and 2, respectively; in N. obscurus, 36.4%, 1.5 and 0.54, respectively; in H. chacarius, 16.6%, 18.6 and 3.11, respectively; and in C. macronyx 33%, 10 and 3.33, respectively.

Euryoryzomys russatus and S. aquaticus from Ea. San Nicolas were each parasitized with a Trichuris sp., constituting a new host and a new geographical record, respectively (Table 1). In both cases, species identification was not possible due to the absence of males. The P, MI and MA of the species of Trichuris in each host species were 12.5%, 1, 0.13 and 20%, 1, 0.2, respectively.

Specimens of Trichuris were not distributed homogeneously among the host species and study areas. The prevalence between species pairs: A. azarae with N. lasiurus, T. nigrita and S. angouya; N. lasiurus with N. obscurus, T. nigrita and S. angouya; T. nigrita with E. russatus and H. chacarius were significantly different (p < 0.05). On the other hand, the prevalence between other host species pairs studied did not differ significantly. Moreover, the prevalence between the two studied areas, Northeast (P 9.53%) and South (P 4.41%) of Argentina, were not significantly different (p = 0.25).

In summary, we recorded 9 new hosts (7 species and 2 subspecies) and 16 new geographical records for Trichuris, enlarging significantly their distributional range (Table 1).

A total of 8 species of Trichuris from 11 rodent species have been recorded in Argentina since 1955 (Morini et al., 1955; Boero and Boehringer, 1967; Suriano and Navone, 1994; Rossin and Malizia, 2005; Robles and Navone, 2006; Rossin et al., 2010; Robles et al., 2006; Robles, 2011; Robles et al., 2012b). These species are distributed approximately from 25[degrees] 12'S to 43[degrees] 51 'S and from 70[degrees] 43 'W to 53[degrees] 54'W (Tables 1 and 2). A total of 24 species of Trichuris from 33 rodent species have been recorded in the Americas since 1955. These species are distributed from Manitoba (N) (Canada) to Texas (S) and from California (W) to Maryland (E) (USA); and in South America from Trinidad (N) (Republic of Trinidad and Tobago) to La Pampa (S) (Argentina) and from Minas Gerais (W) (Brazil) to La Hauyca (E) (Chile) (Table 3) (Lent and Freitas, 1936; Chandler, 1945; Tiner, 1950; Cameron and Reesal, 1951; Morini, et al. 1955; Read, 1956; Boero and Boehringer, 1967; Kenneth and Lepp, 1972; Barus et al., 1975; Babero et al., 1975, 1976; Babero and Murua, 1987; 1990; Pfaffnberger and Bests, 1989; Correa Gomes et al., 1992; Suriano and Navone, 1994; Goncalves et al., 2002; Rossin and Malizia, 2005; Robles and Navone, 2006; Robles et al., 2006; Rossin et al., 2010; Robles, 2011; Robles et al., 2012b).

DISCUSSION

Each species of Trichuris geographically located in Argentina can be distinguished by diagnostic features. In several cases (e.g., Trichuris specimens obtained from C. macronyx, E. russatus, N. obscurus, and S. aquaticus), observed differences in morphological and metric traits prevent us a confident specific assignation. Two possible new species were found from S. angouya and H. chacarius each one. However, new and more detailed studies and material are necessary to clarify the alpha taxonomy of Trichuris in Argentina.

To date, a total of 24 species of Trichuris have been described from 10 families of rodents in America, Caviidae (1 species), Cricetidae (8), Ctenomyidae (4), Dasyproctidae (1), Echymyidae (1), Geomyidae (1), Heteromyidae (3), Myocastoridae (1), Octodontidae (1), and Sciuridae (3). Of these, 8 species have been reported from Argentina, including Trichuris dolichotis Morini, Boero and Rodriguez, 1955, T. myocastoris Enigk, 1933, T. laevitestis T. bursacaudata Suriano and Navone, 1994, T. pampeana Suriano and Navone, 1994, T. pardinasi, T. navonae, T. cf. T. thrichomysi Lopes Torres et al., 2012 (Morini et al., 1955; Boero and Boehringer, 1967; Suriano and Navone, 1994; Robles et al., 2006; Robles, 2011; Robles et al., 2012b) and 4 additional species, not identified to specific level, mentioned in this paper (Tables 1, 2 and 3).

Furthermore, a total of 9 species of Trichuris have been recorded from 14 sigmodontines (A. azarae, A. montensis, A. hirta, C. macronyx, E. russatus, H. chacarius, O. nigripes, P. bonariensis, P. xanthopygus, N. lasiurus, N. obscurus, T. nigrita, S. aquaticus, and S. angouya; Tables 1, 2 and 3). Sigmodontine rodents are distributed predominantly in South America, with a few species having a Central and North American distribution, and this subfamily includes approximately 400 species (Patton et al., in press). Despite the large number of potential host species, only about 3.5% of sigmodontine rodent species have been recorded as hosts for species of Trichuris. Among these hosts, 86% of infections were recorded in Argentina (Morini et al., 1955; Boero and Boehringer, 1967; Suriano and Navone, 1994; Robles and Navone, 2006; Robles et al., 2006; Robles, 2011; Robles et al., 2012b). This number may represent only a small fraction of the species of Trichuris that occurs in sigmodontine rodents, and additional surveys of this group should yield both new species and records.

The distribution of Trichuris species among the species of sigmodontine rodents in the surveyed localities showed a range of prevalence between 9.1-85.7% (samples of 2 or < specimens were not considered). Although the prevalence values given for some localities may be questionable because of the low number of specimens examined, these data give a new overview of the regional distribution of Trichuris. Trichuris cf. T navonae and Trichuris sp. from 3 localities in Misiones showed the highest prevalence (85.7%, 75% and 50%) (Table 1). However, T. laevitestis from A. a. hunteri of Arroyo Caraballo (I = 35, MA = 8.8) and Trichuris sp. from H. chacarius of INTA-IPAF NEA (MI = 18.6, MA = 4.3) showed the highest intensities.

The significant differences observed in the prevalences of the species of Trichuris among host species probably relate to a combination of factors, including host immunologic status, behavior of the host species and characteristics of environment where the eggs were deposited. However, the prevalences between the two studied areas, northeast and south of Argentina, were not significantly different (p > 0.05). Since this is a limited study, these results are not conclusive and surely new data on the soil and microenvironment characters, home range and behavior of host species, and experimental studies will lead to clearer hypotheses about the limiting factors of Trichuris present in wild mammals and extreme geographical areas.

Because of this, a previous hypothesis about the global geographical distribution (tropical and subtropical areas) of genus Trichuris should be revisited. To date, different studies have demonstrated that the embryonation period varies between 9-37 days and 25-35 [degrees]C for T. trichiura, T. muris and T vulpis (Beer, 1971, 1976). A field survey in southern England found that egg development in T suis was greatly retarded at ground temperatures of 4-20[degrees] C, with an embryonation period of 434-630 days (Burden and Hammet, 1979). Moreover, species of Trichuris have been infrequently recorded in high latitudes (Tiner, 1950; Burden and Hammet, 1979; Sardella and Fugassa, 2009). These examples may explain why trichuriasis in humans is presently almost unknown in cold regions; and in the same way, in rodents.

Patagonia presents unique environment characteristics, comprising a series of plateaus and high plains, a vegetation in open patches, and a temperate climate, which ranges from subtropical in the north to subpolar in the far south and at higher elevations (e.g. Soriano, 1956; Leon et al., 1998). To date, in the subpolar areas there have been no previous records of Trichuris in Patagonia, except in archaeological samples (Sardella and Fugassa, 2009). However, in this survey, a population of this tropical-subtropical nematode is recorded for the first time from 40[degrees] S (T. cf. T. pardinasi and Trichuris sp., see Table 1).

In the context of the hypothesis above referred to the absence of Trichuris in the north, west and south of Argentina is consistent with a lower degree of sampling effort with respect to other areas in the country (Fig. 1). Parasitological studies have been carried out in the northeast area of Argentina for a long time, while these studies in Patagonian area have begun recently. It is likely that future studies will reveal the presence of more species and a more accurate host and geographical distribution, mainly in the southern portion of the country.

Consequently, more surveys on different host groups are necessary to determine whether the scarcity of infections of the genus Trichuris in regions of high latitude is due to the absence of sample effort or to environmental effects on the survival of infective stages.

ONLINE SUPPLEMENTARY MATERIAL

APPENDIX 1

List of examined rodents

http://www.sarem.org.ar/wp-content/uploads/2014/06/SAREM_MastNeotrop_21-1_Robles-sup1.doc

AKNOWLEDGEMENTS

We offer thanks to Carlos Galliari, Marcela Lareschi, Juliana Notarnicola, Joaquin Pardinas, Ulyses Pardinas, Juliana Sanchez, Pablo Teta, Daniel Udrizar Sauthier, and collaborators for their cooperation in host collections. To Ulyses Pardinas and Carlos Galliari for the identification of the hosts. To Mike Kinsella for the valuable critical reading of the manuscript and for the revision into English. To Luciana Riccialdelli and Santiago Favoretti for their help with the map. To Lorena Zonta for her assistance with statistic test. To Juliana Notarnicola and an anonymous reviewer for their contribution on the manuscript. This study was funded by Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET), Agencia Nacional de Promocion Cientifica y Tecnologica (ANPCyT) (PICT 0924 to GN; PICT 0547- PIP 6179 to U. Pardinas; PICT 1634 to MRR) and Universidad Nacional de La Plata (N627 to GN). GN and MRR are members of CONICET.

LITERATURE CITED

ANDERSON RC. 2000. Nematode parasites of vertebrates. Their Development and Tranmission. 2nd ed. CAB International, ed. Wallingford, Oxon, U. K.

BABERO BB and RB MURUA. 1987. The helminth fauna of Chile. X. A new species of whipworm from a Chilean Rodent. Transactions of the American Microscopical Society 106:190-193.

BABERO BB and RB MURUA. 1990. A new species of whipworm from a South American hystricomorph rodent. Memorias do Instituto Oswaldo Cruz 85: 211-213.

BABERO BB, PE CATTAN, and C CABELLO. 1975. Trichuris bradleyi sp. n. a whipworm from Octodon degus in Chile. Journal of Parasitology 61:198-206.

BABERO BB, PE CATTAN, and C CABELLO. 1976. A new species of whipworm from the rodent Akodon longipilis in Chile. Transactions of the American Microscopical Society 95:232-235.

BARUS V, G MADJUMDAR, and TK MIKAILOV. 1975. Morphology and taxonomy of Trichocephalus myocastoris (Enigk, 1933). Folia Parasitologica 22:207-213.

BEER RJS. 1971. Whipworms of domestic animals. Veterinary Bulletin 41:343-349.

BEER RJS. 1973. Studies on the biology of the life-cycle of Trichuris suis Schrank, 1788. Parasitology 67:253-262.

BEER RJS. 1976. The relationship between Trichuris trichura (Linnaeus, 1758) of the man and Trichuris suis (Schrank, 1788) of the pig. Research in Veterinary Science 20:47-54.

BELDOMENICO PM, JM. KINSELLA, MM UHART, GL GUTIERREZ, J PEREIRA, H DEL VALLE FERREYRA, and CA MARULL. 2005. Helminths of Geoffroy's cat, Oncifelis geoffroyi (Carnivora, Felidae) from the Monte desert, central Argentina. Acta Parasitologica 50:263-266.

BERTONATTI C and J CORCUERA. 2000. Situacion ambiental Argentina 2000. Fundacion Vida Silvestre Argentina, Buenos Aires.

BOERO JJ and IK BOEHRINGER. 1967. Los parasitos del carpincho (Hydrochoerus hydrochoeris) y del quiya (Myocastor coypus). Revista de la Facultad de Ciencias Veterinarias, La Plata 21:161-172.

BUNDY DAP and ES COOPER. 1988. Trichuriasis 2nd ed. Pp. 120-156, en: Tropical and geographical medicine (KS Warren and AA. Mahmoud, eds). McGraw-Hill, New York.

BUNDY DAP and ES COOPER. 1989. Trichuris and Trichuriasis in humans. Advances in Parasitology 28:107-173.

BUNDY DAP, SP KAN, and R ROSE. 1988. Age-related prevalence, intensity and frecuency distribution of gastrointestinal helminth infection in urban slum children from Kuala Lumpur, Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene 82:289-294.

BURDEN DJ and NC HAMMET. 1979. The development and survival of Trichuris suis ova on pasture plots in the south of England. Research in Veterinary Science 26:66-70.

BUSH AO, KD LAFFERTY, JM. LOTZ and AW SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575-583.

CAFRUNE MM, DH AGUIRRE and LG RICKARD. 1999. Recovery of Trichuris tenuis Chandler, 1930, from camelids (Lama glama and Vicugna vicugna) in Argentina. Journal of Parasitology 85:961-962.

CAMERON TWM and MR REESAL. 1951. Studies on the endoparasitic fauna of Trinidad mammals. Canadian Journal of Zoology 29:276-289.

CALLEJON R, M DE ROJAS, C NIEBERDING, P FORONDA, C FELIU, D GUEVARA, and C CUTILLAS. 2010. Molecular evolution of Trichuris muris isolated from different Muridae hosts in Europe. Parasitology Research 107:631-641.

CHANDLER AC. 1945. Trichuris species from California. Journal of Parasitology 31:284-287.

CORREA GOMES D, RM LANFREDI, RM PINTO, and W DE SOUZA. 1992. Description of Trichuris travassosi n. sp. (Nematoda: Trichurinae) from a Brazilian rodent, by light and scanning electron microscopy. Memorias do Instituto Oswaldo Cruz 87:1-10.

DIGIANI MC, J NOTARNICOLA, and GT NAVONE. 2012. The genus Guerrerostrongylus (Nematoda, Heligmonellidae) in cricetid rodents from the Atlantic Rain Forest of Misiones, Argentina: Emended description of Guerrerostrongylus zetta (Travassos, 1937) and description of a new species. 2012. Journal of Parasitology 98:985-991.

DIGIANI MC, J NOTARNICOLA, and MS PAULOS. 2013. Mazzanema n. gen. and Mazzanema fortuita n. comb. for Longistriata fortuita Freitas, Lent and Almeida, 1937 (Nematoda, Heligmonellidae), a parasite of the marsh rat Holochilus chacarius (Rodentia, Cricetidae) from Northern Argentina. Journal of Parasitology 99:816-820.

GAMBOA MI, G NAVONE, L KOZUBSKY, E COSTAS, L SUSEVICH, M CARDOZO, M GARRAZA, and P MAGISTRELLO. 2005. Geohelmintosis en tres poblaciones suburbanas con diferente condicion sociocultural. Parasitologia Latinoamericana 60:244.

GONCALVES AQ, JJ VICENTE, and RM PINTO. 2002. Nematodes of Amazonian vertebrates deposited in the Helminthological Collection of the Oswaldo Cruz Institute with new records. Revista Brasileira de Zoologia, Curitiba 19:453-465.

GRENCIS RK, KJ. ELSE, AJ BANCROFT, and DAP BUNDY. 1993. Trichuris Update '93. Parasitology Today 9:309-310.

KENNETH ST and DL LEEP. 1972. Redescription of Trichuris fossor Hall, 1916 (Nematoda: Trichuridae) from the Northern Pocket Gopher, Thomomys talpoides. Proceedings of the Helminthological Society of Washington 39:203-205.

KNIGHT RA. 1971. Redescriptions of Trichuris discolor (von Linstow, 1906) and T. skrjabini (Baskakov, 1924) from domestic ruminants in the United States and comparison with T. ovis (Abildgaard, 1795). Journal of Parasitology 57:302-310.

LENT H and JFT FREITAS. 1936. Sobre o Trichuris da nutria. Anais da Academia Brasileira de Ciencias 8:319-322.

LEON RJC, D BRAN, M COLLANTES, JM PARUELO, and A SORIANO. 1998. Grandes unidades de la Patagonia extra andina. Ecologia Austral 8:125-144.

MORINI EG, BOERO J, and A RODRIGUEZ. 1955. Parasitos intestinales en el "Marra" (Dolichotis patagonum patagonum). Publicacion Mision de Estudios de Patologia Regional Argentina 26:83-89.

NOTARNICOLA J and GT NAVONE. 2011. Litomosoides pardinasi n. sp. (Nematoda, Onchocercidae) from two species of cricetid rodents in Northern Patagonia, Argentina. Parasitology Research 108:187-194.

PATTON J, UFJ PARDINAS, and G D'ELIA (eds.). 2014. Mammals of South America. Volume 2, Rodents. The University of Chicago Press, Chicago, IL.

PFAFFENBERGER GS and T BEST. 1989. Trichuris elatoris sp. n. (Nematoda: Trichuridae) from the Texas kangaroo rat (Dipodomys elator). Proceedings of the Helminthological Society of Washington 56:76-81.

READ CP. 1956. Trichuris dipodomis, n. sp., from Ord's Kangaroo Rat. Proceedings of the Helminthological Society of Washington 23:119.

ROBLES MR. 2011. New species of Trichuris (Nematoda: Trichuridae) from Akodon montensis Thomas, 1913 of the Paranaense forest in Argentina. Journal of Parasitology 97:319-327.

ROBLES MR and GT NAVONE. 2006. Redescription of Trichuris laevitestis (Nematoda: Trichuridae) from Akodon azarae and Scapteromys aquaticus (Sigmodontinae: Muridae) in Buenos Aires province, Argentina. Journal of Parasitology 92:1053-1057.

ROBLES MR and GT NAVONE. 2010. Redescription of Syphacia venteli Travassos, 1937 (Nematoda: Oxyuridae) from Nectomys squamipes in Argentina and Brazil and description of a new species of Syphacia from Melanomys caliginosus in Colombia. Parasitology Research 106:1117-1126.

ROBLES MR, GT NAVONE, and J NOTARNICOLA. 2006. A new species of Trichuris (Nematoda: Trichuriidae) from Phyllotini Rodents in Argentina. Journal of Parasitology 92:100-104.

ROBLES MR, O BAIN, and GT NAVONE. 2012a. Description of a new Capillariinae (Nematoda: Trichuridae) from Scapteromys aquaticus (Cricetidae: Sigmodontinae) from Buenos Aires, Argentina. Journal of Parasitology 98:627-639.

ROBLES MR, C GALLIARI, and GT NAVONE. 2012b. New records of nematode parasites from Euryzygomatomys spinosus (Mammalia: Echimyidae) in Misiones province, Argentina. Mastozoologia Neotropical 19:353-358.

ROBLES MR, CJ PERFUMO, JM KINSELLA, and GT NAVONE. 2012c. Angiostrongylus morerai from Akodon species (Rodentia: Sigmodontinae) from Sierra de la Ventana, Buenos Aires, Argentina: histopathological and parasitological studies. Journal of Parasitology 98:1133-1138.

ROSSIN MA and AI MALIZIA. 2005. Redescription of Trichuris pampeana (Nematoda: Trichuridae) from the South American subterranean rodent Ctenomys talarum Thomas, 1898 (Rodentia: Octodontidae). Journal of Parasitology 91:127-130.

ROSSIN MA, AI MALIZIA, JT TIMI, and R POULIN. 2010. Parasitism underground: Determinants of helminth infections in two species of subterranean rodents (Octodontidae). Parasitology 137:1569-1575.

SARDELLA NH and MH FUGASSA. 2009. Paleoparasitological analysis of rodent coprolites in holocenic samples from Patagonia, Argentina. Journal of Parasitology 95:646-650.

SORIANO A. 1956. Los distritos floristicos de la Provincia Patagonica. Revista de Investigaciones Agricolas (Argentina) 10:321- 357.

SURIANO DM and GT NAVONE. 1994. Three new species of the genus Trichuris Roederer, 1761 (NematodaTrichuridae) from Caviomorph and Cricetid rodents in Argentina. Research and Reviews in Parasitology 54:39-46.

TINER JD. 1950. Two new species of Trichuris from North America with description of Trichuris leporis (Nematoda: Aphasmidia). Journal of Parasitology 36:350-354.

TRAUB RJ, ID ROBERTSON, P IRWIN, N MENCKE, and RC THOMPSON. 2004. The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Tropical Medicine and International Health. 9:688-701.

Maria del Rosario Robles and Graciela T. Navone

Centro de Estudios Parasitologicos y de Vectores CEPAVE (CCT-CONICET La Plata) (UNLP), Calle 2 # 584, (1900) La Plata, Buenos Aires, Argentina [correspondence: Maria del Rosario Robles <rosario@cepave.edu.ar>].
Table 1

New hosts and geographical records for species of Trichuris
in Argentina with data of Prevalence (P), Intensity (I),
Mean Intensity (MI) and Mean Abundance (MA) by locality
and host species; numbers and symbols refer to Fig. 1.

          Trichuris         Host              Locality *
          species           species

1         T.                A. azarae         7 km S Puerto Las
          laevitesitis      bibianae **       Palmas, Chaco **

                                              INTA-IPAF NEA,
                                              Formosa **

                            A. azarae         Arroyo de las
                            hunteria          Brusquitas,
                                              Buenos Aires **

                                              Punta Indio,
                                              Buenos Aires **

                                              Zarate,
                                              Buenos Aires **

                                              Arroyo Caraballo,
                                              Entre Rios **

                                              Colonia Villa Elisa,
                                              Entre Rios **

                                              Oliveros, Santa Fe **

                            N lasiurus **     Finca La Adelita,
                                              Laguna Paiva,
                                              Corrientes **

                                              Pergamino,

                                              Buenos Aires **

                                              Uranga, Santa Fe **

2         T. cf. navonae    T. nigrita **     Refugio Mocona,
                                              Misiones **

                                              Desembocadura Arroyo
                                              Paranay-Guazu,
                                              Misiones (c)

                                              Balneario Municipal
                                              de Aristobulo del
                                              Valle, Misionesc

3         T. cf. T.         R xanthopygus     Cerro Corona,
          pardinasi         xanthopygus **    Meseta de Sumuncura,
                                              Rio Negro **

4         Trichuris sp. 1   H. chacarius **   INTA-IPAF NEA,
                                              Formosa *

5         Trichuris sp. 2   5. Angouya **     Refugio Mocona,
                                              Misiones#

                                              Reserva de Usos
                                              Multiples Guarani,
                                              Misiones **

6         Trichuris sp. 3   C. macronyx **    Canadon de la Madera,
                                              Sierra de Tepuel,
                                              Chubut **

7         Trichuris sp. 4   N. obscuras **    Arroyo de las
                                              Brusquitas,
                                              Buenos Aires#

[double   Trichuris sp.     E. russatus **    Arroyo Paraiso,
dagger]                                       Misiones (c)

[double   Trichuris sp.     S. aquaticush     Estancia San Nicolas,
dagger]                                       Corrientes **

          Trichuris         Host               Prevalence
          species           species

1         T.                A. azarae          25% (1/4)
          laevitesitis      bibianae **

                                              33.3% (1/3)

                            A. azarae         37% (10/27)
                            hunteria

                                              9.1% (1/11)

                                              18.2% (2/11)

                                               25% (1/4)

                                              12.5% (3/24)

                                                 (1/1)

                            N lasiurus **     14.3% (2/14)

                                              12.5% (2/16)

                                              16.6% (3/18)

2         T. cf. navonae    T. nigrita **      75% (3/4)

                                               33% (1/3)

                                              85.7% (6/7)

3         T. cf. T.         R xanthopygus        (2/2)
          pardinasi         xanthopygus **

4         Trichuris sp. 1   H. chacarius **   23.1% (3/13)

5         Trichuris sp. 2   5. Angouya **      50% (2/4)

                                                 (2/2)

6         Trichuris sp. 3   C. macronyx **    33.3% (1/3)

7         Trichuris sp. 4   N. obscuras **    36.4% (4/11)

[double   Trichuris sp.     E. russatus **       (1/1)
dagger]

[double   Trichuris sp.     S. aquaticush      20% (1/5)
dagger]

          Trichuris         Host              Intensity or
          species           species           Mean intesity

1         T.                A. azarae              2+
          laevitesitis      bibianae **

                                                   4+

                            A. azarae          1.9 (19/10)
                            hunteria

                                                   2+

                                                 1 (2/2)

                                                   35+

                                                 2 (6/3)

                                                   7+

                            N lasiurus **       1.5 (3/2)

                                                 3 (6/2)

                                               7.6 (23/3)

2         T. cf. navonae    T. nigrita **        2 (6/3)

                                                   6+

                                               1.16 (7/6)

3         T. cf. T.         R xanthopygus       10 (20/2)
          pardinasi         xanthopygus **

4         Trichuris sp. 1   H. chacarius **    18.6 (56/3)

5         Trichuris sp. 2   5. Angouya **       7 (14/2)

                                                 1 (2/2)

6         Trichuris sp. 3   C. macronyx **         10+

7         Trichuris sp. 4   N. obscuras **      1.5 (6/4)

[double   Trichuris sp.     E. russatus **         1 +
dagger]

[double   Trichuris sp.     S. aquaticush          1 +
dagger]

          Trichuris         Host                 Mean
          species           species            abundance

1         T.                A. azarae          0.5 (2/4)
          laevitesitis      bibianae **

                                              1.33 (4/3)

                            A. azarae         0.7 (19/27)
                            hunteria

                                              0.2 (2/11)

                                              0.2 (2/11)

                                              8.8 (35/4)

                                              0.3 (6/24)

                                                7 (7/1)

                            N lasiurus **     0.2 (3/14)

                                              0.4 (6/16)

                                              1.3 (23/18)

2         T. cf. navonae    T. nigrita **      1.5 (6/4)

                                                2 (6/3)

                                                1 (7/7)

3         T. cf. T.         R xanthopygus      10 (20/2)
          pardinasi         xanthopygus **

4         Trichuris sp. 1   H. chacarius **   4.3 (56/13)

5         Trichuris sp. 2   5. Angouya **     3.5 (14/4)

                                                1 (2/2)

6         Trichuris sp. 3   C. macronyx **    3.3 (10/3)

7         Trichuris sp. 4   N. obscuras **    0.5 (6/11)

[double   Trichuris sp.     E. russatus **      1 (1/1)
dagger]

[double   Trichuris sp.     S. aquaticush      0.2 (1/5)
dagger]

* See complete data in supplementary material; ** denotes
a new host and/or a new locality records.
(a) Robles and Navone, 2006; (b) Suriano and Navone, 1994;
(c) Robles, 2011. * shared record; + intensity.

Table 2
Host and geographical data for the species of
Trichuris previously recorded from rodents in
Argentina; numbers and symbols refer to Fig. 1.

           Trichuris         Host species      Locality
           species

1          T. laevitestis    Akodon azarae     Punta Lara
                             hunteri

                                               La Balandra

                                               Reserva Otaniendi

                                               Cerro de la Gloria

                             Scapteromys       Punta Lara
                             aquaticus

                                               La Balandra

                                               Los Talas

                                               Palo Blanco

2          T. navonae        Akodon            Balneario Municipal
                             montensis         de Aristobulo
                                               del Valle

                                               Club Pesca
                                               Paranay-Guazu

                                               Desembocadura arroyo
                                               Paranay-Guazu

                                               Arroyo Salamanca

                                               Salto El Paraiso,
                                               arroyo Paraiso

                                               Arroyo Oveja
                                               Negra--Ruta 21

                                               Parque Provincial
                                               Cruce Caballero

                                               Parque Provincial
                                               Mocona **

                                               Puerto Peninsula

3          T. pardinasi      Phyllotis         Cerro Destierro,
                             bonariensis       Sierra de la
                                               Ventana

                                               Abra de la Ventana,
                                               Sierra de la
                                               Ventana

3          T. pardinasi      Phyllotis         Pampa de Achala
                             xanthopygus
                             vaccarum

8          T. bursacaudata   Ctenomys          Punta de Indio
                             talarum

9          T. dolichotis     Dolichotis        Jardin zoologico,
                             patagonum         Ciudad de Buenos
                                               Aires *

[lambda]   T. myocastoris    Myocastor         Region del Delta *
                             coypus

                                               Region Chaquena *

[phi]      T. pampaeana      Ctenomys          Santa Rosa
                             azarae

                             Ctenomys          Necochea
                             australis

                             Ctenomys          Necochea
                             talarum

                                               Mar de Cobo, Pdo.
                                               Mar Chiquita

[chi]      T. cf.            Euryzygomatomys   Cuartel Rio
           thrichomysi       spinosus          Victoria, Ruta
                                               14 km 273, INTA

           Trichuris         Host species          Coord S
           species

1          T. laevitestis    Akodon azarae     34[grados]47'30"
                             hunteri

                                               34[grados]55'51"

                                                34[grados]09'

                                                36[grados]06'

                             Scapteromys       34[grados]47'30"
                             aquaticus

                                               34[grados]55'51"

                                               34[grados]52'05"

                                               34[grados]52'24"

2          T. navonae        Akodon            27[grados]05'17"
                             montensis

                                               26[grados]40'32"

                                               26[grados]40'39"

                                               26[grados]36'53"

                                               27[grados]13'49"

                                               27[grados]8'20"

                                               26[grados]30'50"

                                               27[grados]9'23"

                                                25[grados]40'

3          T. pardinasi      Phyllotis         38[grados]1'25"
                             bonariensis

                                                38[grados]4'3"

3          T. pardinasi      Phyllotis         31[grados]37'19"
                             xanthopygus
                             vaccarum

8          T. bursacaudata   Ctenomys          35[grados]16'27"
                             talarum

9          T. dolichotis     Dolichotis        34[grados]34'44"
                             patagonum

[lambda]   T. myocastoris    Myocastor         34[grados]21'32"
                             coypus

                                               27[grados]20'27"

[phi]      T. pampaeana      Ctenomys          36[grados]36'33"
                             azarae

                             Ctenomys           38[grados]33>
                             australis

                             Ctenomys           38[grados]33>
                             talarum

                                                37[grados]58'

[chi]      T. cf.            Euryzygomatomys    26[grados]46'
           thrichomysi       spinosus

           Trichuris         Host species           Coord W
           species

1          T. laevitestis    Akodon azarae      58[grados]0'5"
                             hunteri

                                               57[grados]43'0.6"

                                                 58[grados]57'

                                                 57[grados]46'

                             Scapteromys        58[grados]0'5"
                             aquaticus

                                               57[grados]43'0.6"

                                               57[grados]49'20"

                                               57[grados]48'47"

2          T. navonae        Akodon             54[grados]57'9"
                             montensis

                                               54[grados]48'51"

                                                54[grados]50'8"

                                               54[grados]46'51"

                                               54[grados]02'24"

                                               53[grados]55'31"

                                               53[grados]59'54"

                                               53[grados]54'10"

                                                 54[grados]38'

3          T. pardinasi      Phyllotis         62[grados]54'39"
                             bonariensis

                                                62[grados]1'17"

3          T. pardinasi      Phyllotis         64[grados]54'39"
                             xanthopygus
                             vaccarum

8          T. bursacaudata   Ctenomys          57[grados]15'38"
                             talarum

9          T. dolichotis     Dolichotis        58[grados]24'55"
                             patagonum

[lambda]   T. myocastoris    Myocastor         58[grados]40'53"
                             coypus

                                                58[grados]47'9"

[phi]      T. pampaeana      Ctenomys           64[grados]19'2"
                             azarae

                             Ctenomys            58[grados]45'
                             australis

                             Ctenomys            58[grados]45'
                             talarum

                                                 57[grados]34'

[chi]      T. cf.            Euryzygomatomys    54[grados] 18'
           thrichomysi       spinosus

           Trichuris         Host species        Province
           species

1          T. laevitestis    Akodon azarae     Buenos Aires
                             hunteri

                                               Buenos Aires

                                               Buenos Aires

                                               Buenos Aires

                             Scapteromys       Buenos Aires
                             aquaticus

                                               Buenos Aires

                                               Buenos Aires

                                               Buenos Aires

2          T. navonae        Akodon              Misiones
                             montensis

                                                 Misiones

                                                 Misiones

                                                 Misiones

                                                 Misiones

                                                 Misiones

                                                 Misiones

                                                 Misiones

                                                 Misiones

3          T. pardinasi      Phyllotis         Buenos Aires
                             bonariensis

                                               Buenos Aires

3          T. pardinasi      Phyllotis           Cordoba
                             xanthopygus
                             vaccarum

8          T. bursacaudata   Ctenomys          Buenos Aires
                             talarum

9          T. dolichotis     Dolichotis        Buenos Aires
                             patagonum

[lambda]   T. myocastoris    Myocastor         Buenos Aires
                             coypus

                                                  Chaco

[phi]      T. pampaeana      Ctenomys            La Pampa
                             azarae

                             Ctenomys          Buenos Aires
                             australis

                             Ctenomys          Buenos Aires
                             talarum

                                               Buenos Aires

[chi]      T. cf.            Euryzygomatomys     Misiones
           thrichomysi       spinosus

           Trichuris         Host species      References
           species

1          T. laevitestis    Akodon azarae     Suriano and
                             hunteri           Navone, 1994

                                               Robles and
                                               Navone, 2006

                                               Robles and
                                               Navone, 2006

                                               Robles and
                                               Navone, 2006

                             Scapteromys       Suriano and
                             aquaticus         Navone, 1994

                                               Robles and
                                               Navone, 2006

                                               Robles and
                                               Navone, 2006

                                               Robles and
                                               Navone, 2006

2          T. navonae        Akodon            Robles, 2011
                             montensis

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

                                               Robles, 2011

3          T. pardinasi      Phyllotis         Robles
                             bonariensis       et al., 2006

                                               Robles
                                               et al., 2006

3          T. pardinasi      Phyllotis         Robles
                             xanthopygus       et al., 2006
                             vaccarum

8          T. bursacaudata   Ctenomys          Suriano and
                             talarum           Navone, 1994

9          T. dolichotis     Dolichotis        Morini et al., 1955
                             patagonum

[lambda]   T. myocastoris    Myocastor         Boero and
                             coypus            Boehringer, 1967

                                               Boero and
                                               Boehringer, 1967

[phi]      T. pampaeana      Ctenomys          Suriano and
                             azarae            Navone, 1994

                             Ctenomys          Rossin et al., 2010
                             australis

                             Ctenomys          Rossin and
                             talarum           Malizia, 2005

                                               Rossin and
                                               Malizia, 2005

[chi]      T. cf.            Euryzygomatomys   Robles
           thrichomysi       spinosus          et al., 2012

* Area not detailed; ** This locality is very near
to Refugio Mocona (see Table 1)

Table 3

Host and geographical data previously recorded for species of
Trichuris from rodents in America excluding Argentinean records.

Trichuris species      Host species              Host family

T. leporis             Spermophilus               Sciuridae
(Froelich, 1789)       richardsonii
                       ([section])

T. gracilis            Dasyprocta leporina *,   Dasyproctidae
(Rudolphi, 1819)       D. fuliginosa

T. opaca Barker et     Ondatra zibethicus,       Cricetidae
Noyes, 1915            Microtus
                       pennsylvanicus

T. fossor Hall, 1916   Thomomys                   Geomyidae
                       talpoides ([dagger]),
                       T. bottae

T. myocastoris         Myocastor coypus         Myocastoridae
Enigk, 1933

T. citelli Chandler,   Spermophilus beecheyi      Sciuridae
1945                   ([double dagger])

T. perognathi          Perognathus              Heteromyidae
Chandler, 1945         californicus
                       californicus,
                       P. pennicillata

T. neotomae            Neotoma fuscipes          Cricetidae
Chandler, 1945

T. peromysci           Peromyscus                Cricetidae
Chandler, 1946         californicus

T. madisonensis        Tamias striatus            Sciuridae
Tiner, 1950

T. dipodomys           Dipodomys ordii,         Heteromyidae
(Read, 1956)           D. phillipsi

T. bradleyi Babero,    Octodon degus            Octodontidae
Cattan and Cabello,
1975

T. chilensis Babero,   Abrothrix                 Cricetidae
Cattan and Cabello,    longipilis (a)
1976

T. fulvi Babero et     Ctenomys fulvus           Ctenomyidae
Murua, 1987            phillipiensis

T. elatoris            Dipodomys elator,        Heteromyidae
Pfaffnberger and       D. merriami, D. ordii
Best, 1989

T. robusti Babero      Ctenomys robustus         Ctenomyidae
and Murua, 1990

T. travassosi          Oligoryzomys              Cricetidae
Correa Gomes,          nigripes #
Lanfredi, Pinto and
Souza, 1992

Trichuris species      Host species              Host family

T. thrichomysi         Thrichomys apereoides,    Echimyidae
Lopes Torres           Euryzygomatomys
et al., 2011           spinosus

Trichuris species            Locality         Country

T. leporis                   Manitoba          Canada
(Froelich, 1789)

T. gracilis             State of Amazonas     Trinidad
(Rudolphi, 1819)                               Brazil

T. opaca Barker et     Nebraska, Wisconsin,     USA
Noyes, 1915               Ohio, Wyoming,
                             Maryland

T. fossor Hall, 1916   California, Wyoming      USA

T. myocastoris              San Pablo          Brazil
Enigk, 1933

T. citelli Chandler,        California          USA
1945

T. perognathi               California          USA
Chandler, 1945

T. neotomae                 California          USA
Chandler, 1945

T. peromysci                California          USA
Chandler, 1946

T. madisonensis             Wisconsin           USA
Tiner, 1950

T. dipodomys             New Mexico, Utah       USA
(Read, 1956)

T. bradleyi Babero,          Santiago          Chile
Cattan and Cabello,
1975

T. chilensis Babero,         Santiago          Chile
Cattan and Cabello,
1976

T. fulvi Babero et     San Pedro de Atacama    Chile
Murua, 1987

T. elatoris                   Texas            Mexico
Pfaffnberger and
Best, 1989

T. robusti Babero           La Hauyca          Chile
and Murua, 1990

T. travassosi           Rio Grande do Sul      Brazil
Correa Gomes,
Lanfredi, Pinto and
Souza, 1992

Trichuris species            Locality         Country

T. thrichomysi             Minas Gerais        Brazil
Lopes Torres
et al., 2011

([section]) Cited as Citellus richardsoni by Tiner, 1950; * Cited
as Cavia agouti by Rudolphi, 1819; ([dagger]) Cited as Thomomys
fossor by Hall, 1916; ([double dagger]) Cited as Citellus beecheyi
by Chandler, 1945; [alpha] Cited as Akodon longipilis by Babero,
Cattan and Cabello, 1976; # Cited as Oryzomys nigripes by Correa
Gomes et al., 1992. Families of Argentinean records, Caviidae: T.
dolichotis; Cricetidae: T. laevitestis, T. pardinasi and T.
navonae; Ctenomyidae: T. bursacaudata and T. pampeana.
COPYRIGHT 2014 Sociedad Argentina para el Estudio de los Mamiferos
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2014 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:texto en ingles
Author:del Rosario Robles, Maria; T. Navone, Graciela
Publication:Mastozoologia Neotropical
Date:Jun 1, 2014
Words:6601
Previous Article:Patrones estacionales de distribucion espacial y area de accion del piche lloron, Chaetophractus vellerosus (Cingulata: dasypodidae), en Magdalena,...
Next Article:Estableciendo limites: distribucion geografica de los micromamiferos terrestres (Rodentia y Didelphimorphia) de Patagonia centro-oriental.
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters