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.
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
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).
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).
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).
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.
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).
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
List of examined rodents
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.
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 <email@example.com>].
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.
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||texto en ingles|
|Author:||del Rosario Robles, Maria; T. Navone, Graciela|
|Date:||Jun 1, 2014|
|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.|