A New Species of Trichuris Roederer, 1761 (Nematoda: Trichuridae) from Heteromys Gaumeri Allen & Chapman (Rodentia: Heteromyidae) in Yucatan, Mexico

Syst Parasitol (2016) 93:721–730 DOI 10.1007/s11230-016-9656-6

A new species of Trichuris Roederer, 1761 (Nematoda: Trichuridae) from Heteromys gaumeri Allen & Chapman (Rodentia: Heteromyidae) in Yucatan, Mexico

Jesu´s Alonso Panti-May . Marı´a del Rosario Robles

Received: 16 March 2016 / Accepted: 5 July 2016 Ó Springer Science+Business Media Dordrecht 2016

Abstract In Mexico, four species of Trichuris Introduction Roederer, 1761 have been recorded in wild rodents belonging to the family Heteromyidae. In the present Species of Trichuris Roederer, 1761 (Nematoda: paper, we describe a new species based on specimens Trichuridae) have a worldwide distribution and par- collected from Heteromys gaumeri Allen & Chapman asitise the large intestine (caecum and colon) of a (Heteromyidae: Heteromyinae) in the tropical forests broad range of mammalian hosts, among which are of the Yucatan Peninsula, Mexico. Trichuris silviae n. humans, primates, pigs, horses, and rodents (Cafrune sp. can be differentiated from the congeners described et al., 1999; Anderson, 2000). Characteristics such as in North and South American rodents by morpholog- the spicular tube, the length of the spicule, the shape of ical and morphometric features, such as the possession the proximal and distal cloacal tube, and the vulvar of a wide spicular tube, a thicker proximal cloacal morphology, along with classical morphometric data tube, a shorter distal cloacal tube and a cylindrical have been used with high discriminatory value for spicular sheath. This is the first description of a differentiating species of Trichuris (see Sˇpakulova´, Trichuris spp. from heteromyid rodents in Mexico and 1994; Suriano & Navone, 1994; Rossin & Malizia, the fourth in North America. Despite the broad 2005; Robles & Navone, 2006). Additionally, scan- distribution of Heteromys spp., few cases of Trichuris ning electron microscopy (Lanfredi et al., 1995; infection have been reported. Further studies are Robles & Navone, 2006; Robles, 2011; Torres et al., necessary to verify if the new species is present in 2011), isoenzyme patterns and molecular tools have other heteromyid rodents in order to increase our been used for species identification (Cutillas et al., knowledge about its geographical and host 1996, 2002, 2004; Feliu et al., 2000; Callejoń et al., distribution. 2015). Until now, 25 species of Trichuris have been described from ten families of North and South J. A. Panti-May (&) American rodents, i.e. the Caviidae, Cricetidae, PIMVS Tumben Kuxtal A.C., Calle 12 #64 x 5 y 7, C.P. Ctenomyidae, Dasyproctidae, Echimyidae, Geomyi- 97470 Tixkokob, Yucatań, Mexico e-mail: [email protected] dae, Heteromyidae, Myocastoridae, Octodontidae and Sciuridae. Of these, four species have been recorded in M. R. Robles wild rodents with geographical distributions that ´ Centro de Estudios Parasitologicos y de Vectores Trichuris citelli CEPAVE (CCT- CONICET- La Plata), Universidad include central Mexico: Chandler, Nacional de La Plata (UNLP), Bv 120 e/ 61 y 64, La Plata 1945 from Spermophilus variegatus Erxleben in (1900), Buenos Aires, Argentina 123 722 Syst Parasitol (2016) 93:721–730

Michoacan (Garcıá-Prieto et al., 2012); T. dipodomis Facultad de Medicina Veterinaria y Zootecnia- Read, 1956 from Dipodomys phillipsii Gray in Ver- UADY, Municipality of Merida, Yucatan State, Mex- acruz (Garcıá-Prieto et al., 2012); T. elatoris Pfaffen- ico, were captured between March and October 2013 berger & Best, 1989 from D. ordii Woodhouse, D. (see collectors in acknowledgements). Captured merriami Mearns and Chaetodipus hispidus Baird in rodents were transported to the laboratory and were San Luis Potosi (Garcıá-Prieto et al., 2012); and T. euthanised with an intraperitoneal injection of sodium fossor Hall, 1916 from Peromyscus difficilis Allen in pentobarbital. The abdominal cavities and viscera of Hidalgo (Falcon-Ordaz, 1993) and Liomys irroratus the hosts were examined for parasites. Nematodes Gray in Morelos (Eslava-Araujo, 2005). Trichuris were collected from the caecum and 15 specimens fossor is the only species recorded from Mexican were fixed in 10 % formalin, preserved in 70 % rodents of the subfamily Heteromyinae (see Eslava- ethanol, cleared in lactophenol for light microscopy. Araujo, 2005). Drawings were made with the aid of a drawing tube. Moreover, a cosmopolitan species, T. muris One male specimen was dehydrated in ethanol series (75, Schrank, 1788, has been recorded previously for 80, 85, 90, 96 and 100%), dried using the critical point Rattus norvegicus Berkenhout and R. rattus Linnaeus method, and examined with the aid of a scanning electron in the Distrito Federal (Zerecero, 1943; Garcıá-Prieto microscope (SEM, Jeol 6360 LVLV, Tokyo, Japan). et al., 2012), Mus musculus L. from Hidalgo (Pulido- Measurements are presented as follows: holotype Flores et al., 2005) and Yucatan (Panti-May et al., male/allotype female and paratypes, mean and range 2015), and from L. irrotatus in Morelos (Eslava- (in parentheses). All measurements are in micrometres Araujo, 2005). unless otherwise stated. Morphological analysis was Heteromys gaumeri Allen & Chapman, is a performed according Robles et al. (2006), followed in medium-sized rodent endemic to the Yucatan Penin- a series of communications (Robles & Navone, 2006; sula (Schmidt et al., 1989). Its geographic range Robles, 2011; Robles et al., 2014). The type-material includes northern Belize, El Peteń in Guatemala, and is deposited in the Helminthological Collection of the southeastern Mexico (Schmidt et al., 1989). In Mex- Museo de La Plata, La Plata, Buenos Aires, Argentina ico, H. gaumeri occurs from tall to short semi- and in the Coleccioń Nacional de Helmintos of the deciduous tropical forest (Pozo de la Tijera & Instituto de Biologıá-Universidad Nacional Autońoma Escobedo Cabrera, 1999; Hernańdez-Betancourt de Mexico, Mexico City, Mexico. Hosts are deposited et al., 2003; Cime´-Pool et al., 2010; Canul-Cruz in the Mastozoological Collections of the Museo de et al., 2012), secondary deciduous forest (Dowler & Zoologıá (MZ)-UADY, Me´rida, Yucatan, Mexico. Engstrom, 1984) and cultivated fields (Birney et al., 1974; Cime´-Pool et al., 2007), where the predominant Order Enoplida Filipjev, 1929 climate is warm sub-humid with summer rains (Insti- Family Trichuridae Railliet, 1915 tuto Nacional de Estadı´stica y Geografıá, 2015). Heteromys gaumeri plays a key role in the ecology Trichuris silviae n. sp. of seed dispersal in tropical forests through harvesting and eating seeds (Hernańdez-Betancourt et al., 2003; Type-host: Heteromys gaumeri (Allen & Chapman) Canul-Cruz et al., 2012). (Mammalia: Castorimorpha: Heteromyidae), Gau- This paper describes a new species of Trichuris mer’s spiny pocket mouse. based on specimens collected from Heteromys gau- Host vouchers: Symbiotype (female, coll. 27.ix.2013; meri (Heteromyidae: Heteromyinae) from tropical accession number MZ 1025); other host vouchers forests in Yucatan, Mexico. (coll. 25-27.ix.2013) housed at the MZ under accession numbers MZ1022–1024 and MZ1009. Type-locality: Rancho Hobonil (21°01’41.8’’N, Materials and methods 89°00’51.2’’W), Municipality of Tzucacab, Yucatan State, Mexico. Seven specimens of H. gaumeri, six from the Rancho Other locality: Facultad de Medicina Veterinaria y Hobonil of the Universidad Autońoma de Yucatań Zootecnia (20°52006.500N, 89°37004.500W), Municipal- (UADY), Municipality of Tzucacab and one from the ity of Merida, Yucatan State. 123 Syst Parasitol (2016) 93:721–730 723

Type-material: Holotype male (MLP-He 7113), allo- Male. [Based on the holotype and 9 paratypes.] type female (MLP-He 7114), 12 paratype specimens Body length 13.89; 16.61 (14.95–18.71) mm. Ante- (MLP-He 7115, CNHE 9987) deposited in the rior portion of body 7.27; 8.76 (7.67–9.87) mm Helminthological Collection of the Museo de La Plata long; thick portion of body 6.62; 7.85 (6.78–9.43) (MLP-He) and in the Coleccioń Nacional de Helmin- mm long (Fig. 1A). Anterior body width 82; 93 tos (CNHE) of the Instituto de Biologıá-Universidad (85–110); maximum posterior body width 330; 300 Nacional Autońoma de Mexico, Mexico City, Mexico. (260–330); width at level of oesophago-intestinal Site in host: Caecum. junction 240; 210 (200–230) (Fig. 1B). Total length Prevalence and intensity: Overall prevalence 85.7 % of oesophagus 7.27; 8.76 (7.67–9.87) mm, muscular (6 infected out of 7 rodents examined); overall portion 590; 560 (470–780) long, stichosome portion intensity 1–45 (mean 12) nematodes; type-locality: 6.68, 8.20 (7.16–9.09) mm long. Spicule tube length prevalence 83.3 % (5 out of 6 hosts infected), mean 610, 570 (470–640). Spicule total length 1,360; intensity 14.4 (1–45). 1,390 (1,300–1,480); width 15; 15 (15–19) at tip, Etymology: This species is dedicated to Dr. Silvia 30; 29 (25–30) at midregion, and 50; 40 (30–50) at Hernańdez Betancourt, a well-known mammalogist in base (Fig. 1D). Spicular sheath, when fully Mexico who has contributed to increasing the knowl- extruded, densely spinose 120; 80 (80–130) long edge of rodent ecology, particularly in the Yucatan (Fig. 1E). Proximal cloacal tube 1,270; 1,570 Peninsula. (1,410–1,730) long, 190; 190 (140–220) wide; distal cloacal tube 550; 670 (550–940) long, 100; 90 Description (Figs. 1–2) (70–120) wide (Fig. 1D). Ratio total body length/ posterior portion length 2.10; 2.12 (1.97–2.26). General. [Based on the holotype, allotype and 12 Ratio posterior portion length/ anterior portion paratypes.] Cuticle with fine transversal striation. Ante- length 0.9; 0.90 (0.80–1.03). Ratio total body length/ rior part of body long, narrow, tapered, whip-like; spicule length 10.25; 11.97 (10.68–14.37). Ratio posterior part of body broad, handle-like (Fig. 1A). Ratio posterior portion length/ spicule length 4.89; 5.66 between anterior and posterior body length 0.97:1–1.26:1 (4.99–7.28). Ratio proximal cloacal tube length/ in males and 0.90:1–1.12:1 in females. Stichosome with distal cloacal tube length 2.32; 2.41 (1.79–2.97). single row of stichocytes, and single pair of conspicuous Ratio maximum posterior body width/ posterior cells at level of oesophago-intestinal junction (Fig. 1B, portion length 0.05; 0.04 (0.03–0.04). C). Male with wide spicular tube. Proximal cloacal tube Female. [Based on the allotype and 4 paratypes.] Body united laterally to distal cloacal tube (Fig. 1D). Spicular length 34.11; 23.86 (22.14–26.13) mm. Anterior sheath cylindrical with spines distributed from proximal portion of body 17.47; 12.15 (11.17–13.81) mm long; to distal portion; distal spines sharpened and joined thick portion of body 16.64; 11.71 (10.64–12.44) mm together (Figs. 1E, 2D). Testis reaches to near first fith of long. Anterior body width 130; 110 (90–130); max- proximal cloacal tube (Fig. 1A, arrow). Cloaca subter- imum posterior body width 550; 380 (380–400); width minal, not ornamented. Female with non-protrusive at level of oesophago-intestinal junction 300; 200 vulva located at level of oesophago-intestinal junction (190–220) (Fig. 1C). Total length of oesophagus (Fig. 1C). Anus subterminal; caudal end long (Fig. 1F). 17.35; 12.15 (11.17–13.81) mm, muscular portion Bacillary band located laterally in anterior portion 640; 520 (400–620) long, stichosome portion 16.71; of body (Fig. 2A, B), at 80–1,000 from anterior end of 11.62 (10.56–13.42) mm long. Distance between body, extending to widened part of body 100–190. oesophago-intestinal junction and vulva 0. 25 (0–50) Cuticular inflations bordering bacillary band 170–210 (Fig. 1C). Eggs oval, flat, with bipolar plugs 61–65 9 from anterior end of body, extend to 640–700 from 30–31 (n = 4) (Fig. 1G). Ratio total body length/ anterior end, forming low rings of thick walls and very posterior portion length 2.05; 2.04 (1.90–2.12). reduced interior cavity (Fig. 2B). These structures Ratio posterior portion length/ anterior portion length limit laterally to abundant, visible bacillary glands 0.95; 0.97 (0.90–1.11). Ratio maximum posterior with conspicuous pore (Fig. 2B, C,). Cuticle around body width/ posterior portion length 0.03; 0.03 vulvar aperture with transversally striated pattern. (0.03–0.04).

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Fig. 1 Trichuris silviae n. sp. ex Heteromys gaumeri. A, Male, total view (arrow indicates posterior extremity of the testis); B, Male, oesophago-intestinal junction and proximal portion of the testis, lateral view; C, Female, oesophago-intestinal junction and vulva, lateral view; D, Male, posterior extremity, spicule, spicular tube, proximal and distal cloacal tube, and spiny spicular sheath, lateral view; E, Male, detail of the posterior extremity and spiny spicular sheath, lateral view; F, Female, posterior extremity, lateral view; G, Egg. Scale-bars: A, 1,000 lm; B–D, 200 lm; E, F, 100 lm; G, 60 lm

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Remarks Suriano & Navone, 1994, T. pampeana Suriano & Navone, 1994, T. pardinasi Robles, Navone & Notar- Trichuris silviae n. sp. was compared with 25 species nicola, 2006, T. navonae Robles, 2011, T. bradleyi of Trichuris described from North and South Amer- Babero, Cattan, & Cabello, 1975, T. chilensis Babero, ican rodents (Chandler, 1945; Tiner, 1950; Cameron Cattan & Cabello, 1976, T. elatoris, T. robusti Babero & Reesal, 1951; Morini et al., 1955; Read, 1956; & Murua, 1990, T. travassosi Correa, Lanfredi, Pinto Frandsen & Grundmann, 1961a; Todd & Lepp, 1972; & Souza, 1992, and T. bainae Robles, Cutillas, Panei Babero et al., 1975; Barus et al., 1975; Babero et al., & Callejo´n, 2014, by the presence of a spicular tube (in 1976; Babero & Murua, 1987; Pfaffenberger & Best, these 12 species, the spicule lies entirely within the 1989; Babero & Murua, 1990; Gomes et al., 1992; distal cloacal tube). Suriano & Navone, 1994; Robles et al., 2006; Robles, Among the 11 species with spicular tube (i.e. T. 2011; Torres et al., 2011; Robles et al., 2014). citelli, T. perognathi Chandler, 1945, T. neotomae Trichuris silviae n. sp. differs from 12 species parasitic Chandler, 1945, T. peromysci Chandler, 1946, T. in American rodents, i.e. T. opaca Barker & Noyes, madisonensis Tiner, 1950, T. fossor, T. dipodomis, T. 1915, T. myocastoris Enigk, 1933, T. bursacaudata fulvi Babero & Murua, 1987, T. laevitestis Suriano &

Fig. 2 Scanning electron micrographs of Trichuris silviae n. sp. ex Heteromys gaumeri. A, Detail of bacillary glands (arrow) in the proximal portion of bacillary band; B, Cuticular inﬂations (arrow) bordering the bacilar band in its proximal portion; C, Detail of bacilary glands in the distal portion of the bacillary band; D, Male, posterior extremity and spiny spicular sheath, ventro-lateral view. Scale-bars:A,C,10lm; B, D, 20 lm 123 726 Syst Parasitol (2016) 93:721–730

Navone, 1994, T. stansburyi Frandsen & Grundmann, citelli, T. perognathi, T. neotomae, T. gracilis, T. 1961, and T. thrichomysi Torres, Nascimento, dipodomis, T. leavitestis, T. stansburyi, T. chilensis Menezes, Garcia, Santos, Maldonado, Miranda, Lan- and T. bainae by the lack of a marked prominence or fredi & Souza, 2011) the new species can be differ- evagination. entiated from T. fossor, T. fulvi, T. laevitestis, and T. Most morphometric features of T. silvae n. sp. thrichomysi in having a shorter spicular tube; no data overlap with T. peromysci. However, the new species for the remaining species are available. Table 1 shows has a longer distal cloacal tube (550–940 vs comparative data highlighting the main distinctive 380–530 lm) and shorter spicular sheath (80–130 vs features (i.e. spicular length, spicular sheath shape and 260–360 lm). Females of T. silviae n. sp. also have distal cloacal tube length) of T. silviae n. sp. in relation smaller eggs (61–65 9 30–31 vs 87–90 9 40 lm). to the congeners described with a spicular tube A comparison of the length of the bacillary bands, described from North and South American rodents. and the size, shape and distribution of the bacillary The new species can be separated from T. opaca, T. glands, as well as their number, with respect to the fossor, T. citelli, T. neotomae, T. dipodomis and T. transversal cuticular striations, showed some differ- bursacaudata by the presence of a cylindrical spicular ences with other species previously studied under sheath. Among species with a cylindrical spicular SEM such as T. myocastoris, T. travassosi, T. pam- sheath, the new species differs from T. laevitestis, T. peana, T. pardinasi, T. laevitestis, T. navonae and T. thrychomysi, T. pampeana, T. pardinasi, T. navonae, bainae. The bacillary band of T. silviae n. sp. begins T. elatoris, and T. bainae by the distribution and shape anteriorly to that reported for T. laevitestis, but is of spines and from T. peromysci, T. fulvi, T. stansburyi, similar to the remainig species. The cuticular inﬂa- T. bradleyi, and T. robustis by the length of the tions of the new species form low walls and narrow spicular sheath. rings and appear to have a lower density than those The new species has a shorter spicule than T. observed in other species (Gomes et al., 1992; myocastoris, T. fulvi, T. laevitestis, T. thrichomysi, T. Lanfredi et al., 1995; Rossin & Malizia, 2005; Robles bursacaudata, T. pampeana, T. pardinasi, T. bradleyi, & Navone, 2006; Robles et al., 2006; Robles, 2011; T. chilensis, T. robusti, T. travassosi and T. bainae and Robles et al., 2014). Although there may be an effect a longer spicule than T. perognathi, T. neotomae, T. of the preparation of the material, this observation was madisonensis, T. stansburyi and T. elatoris. Moreover, conﬁrmed under light microscope. T. silviae n. sp. has a shorter distal cloacal tube than T. citelli, T. myocastoris, T. bursacaudata, T. pampeana, T. pardinasi, T. navonae, T. bradleyi, T. chilensis, T. Discussion robusti, T. travassosi and T. bainae and a longer distal cloacal tube than T. perognathi and T. peromysci. Twenty-six species of Trichuris have been described Although males of T. gracilis Rudolphi, 1819 and in American rodents, considering the new species. T. dolichotis Morini, Boero & Rodrigues, 1955 have Although the ranges of some morphometric features not been described, females of T. gracilis can be overlap among these species and some of them share separated from the new species by the length of the morphological characteristics, the combination of body (38.5–39.6 vs 22.1–34.1 mm), the length of the these characters allows species differentiation. The anterior portion of the body (21.5–27.4 vs 11.2–17.5 unique features of T. silviae n. sp., such as the presence mm) and the size of the eggs (50–59 9 23–28 vs 61–65 of a wide spicular tube, a thicker proximal cloacal 9 30–31 lm), and females of T. dolichotis differ by tube, a shorter distal cloacal tube, a cylindrical the ratio posterior portion/ anterior portion of body spicular sheath with sharp and joined together spines, length (1.33 vs 0.90–1.11) and the size of the eggs (75 a non-protrusive vulva, and different morphometric 9 45 vs 61–65 9 30–31 lm). characters and ratios, in combination, support the Females of T. silviae n. sp. have a smaller distance distinct status of this species. from the oesophago-intestinal junction to vulva than T. Althougth the original description of the species of madisonensis, T. gracilis, T. fulvi, T. bradleyi, T. Trichuris described in heteromyids (i.e. T. dipodomis, chilensis, T. elatoris and T. bainae. In addition, the T. elatoris and T. perognathi) or recorded in Mexican vulva of the new species is distinguishable from T. rodents (e.g. T. citelli and T. fossor) are incomplete, 123 Syst Parasitol (2016) 93:721–730 727

Table 1 Comparative data for the main distinctive features between Trichuris silviae n. sp. (highlighted in bold) and other Trichuris spp. with spicular tube described from North and South American rodents Species Type-host (Family) Type-locality Length or shape Reference

Spicule (1,300–1,480 lm) T. neotomae Chandler, Neotoma fuscipes Baird Hastings Natural History 1,150–1,230 Chandler (1945) 1945 (Cricetidae) Reservation, California, USA T. perognathi Chaetodipus californicus Hastings Natural History 900–1,150 Chandler (1945) Chandler, 1945 californicus Merriam Reservation, California, (Heteromyidae)a USA T. madisonensis Tiner, Tamias striatus L. (Sciuridae) Madison, Wisconsin, USA 830–950 Tiner (1950) 1950 T. stansburyi Frandsen Peromyscus maniculatus Stansbury Island, Utah, USA 860–1,160 Frandsen & & Grundmann, 1961 sonoriensis Le Conte Grundmann (Cricetidae) (1961a) T. fulvi Babero & Ctenomys fulvus phillipiensis San Pedro Atacama, 3,470–3,710 Babero & Murua Murua, 1987 Philippi (Ctenomyidae) Tarapaca, Chile (1987) T. laevitestis Suriano Scapteromys aquaticus Thomas Punta Lara, Buenos Aires, 3,000–3,650 Suriano & & Navone, 1994 (Cricetidae) Argentina Navone (1994) T. thrichomysi Torres Thrichomys apereoides Lund Capita˜o Andrade, Minas 1,860–2,780 Torres et al. et al., 2011 (Echimyidae) Gerais, Brazil (2011) Distal cloacal tube (550–940 lm) T. peromysci Chandler, Peromyscus californicus Gambel Hastings Natural History 370–520 Chandler (1946) 1946 (Cricetidae) Reservation, California, USA T. citelli Chandler, Spermophilus beecheyi Hastings Natural History 1,000–1,300 Chandler (1945) 1945 Richardson (Sciuridae)b Reservation, California, USA Cylindrical spicular sheath with spines T. fossor Hall, 1916 Thomomys talpoides Allen Crested Buttes and With distal Hall (1916) (Geomyidae)c Livermore, Colorado, USA spherical bulge and spiny T. dipodomis Read, Dipodomys ordii Woodhouse Santa Fe, New Mexico, USA Campanuliform Read (1956) 1956 (Heteromyidae) and spiny a Cited as Perognathus californicus californicus; b Cited as Citellus beecheyi; c Cited as Thomomys fossor

these species are well distinguished when compared well conserved, showing some differences in the with T. silviae n. sp. However, furher revisions are distribution of the glands, and different sizes and needed to clarify some morphological features (e.g. shapes of the cuticular inﬂations compared to those distal cloacal tube) of these Trichuris spp. for which no observed in six other studied species (Gomes et al., drawings and/or photos are provided in their original 1992; Lanfredi et al., 1995; Rossin & Malizia, 2005; descriptions. Robles & Navone, 2006; Robles et al., 2006; Robles, The bacillary band of T. silviae n. sp. was studied 2011). Since the bacillary bands are not known for all under light microscopy, and only a few studies include Trichuris spp., it is possible that the importance of this SEM descriptions of this structure. Although ﬁxation structure will be assessed only when new studies with can alter the structure of the bacillary bands (Wright, detailed descriptions, illustrations, and photographs 1975), in the new species the bands appear to be very are provided. 123 728 Syst Parasitol (2016) 93:721–730

The type-host of T. silviae n. sp., H. gaumeri, determine if Trichuris spp. occur in other heteromyids belongs to a genus of Neotropical hosts, abundant rodents. from southern Mexico to Ecuador, Colombia and Venezuela (Rogers & Gonza´lez, 2010). However, Acknowledgements We would like to thank to Drs Silvia information on species of Trichuris parasitising Hernańdez-Betancourt and Marco Torres-Castro for their support in the field work, to the staff of the Laboratorio de Heteromys spp. is scarse. In Mexico, no previous Parasitologıá-FV-UADY, Mexico for their help; to Erendira study has reported the presence of Trichuris spp. in Martıńez for her support in the Laboratorio de Zoologıá-FV- Heteromys spp. Considering heteromyid hosts, only T. UADY; to Dr. Graciela Navone for her support in the dipodomis, T. elatoris, T. fossor and T. muris have Laboratorio de Parasitologıá-CEPAVE, Argentina; to Josh Taylor for the critical reading of the manuscript and for the been reported in Mexico (Eslava-Araujo, 2005; revision to English, and to two anonymous referees for their Garcıá-Prieto et al., 2012). valuable suggestions to improve this paper. The geographical distribution of H. gaumeri (Yucatan Peninsula) does not overlap with areas Funding Fieldwork was partly supported by the FOMIX- CONACYT FOMIX-YUC-2008-108929 (Sensibilidad y vul- where other wild rodent hosts of Trichuris spp. have nerabilidad de los ecosistemas costeros del sureste de Me´xico been recorded (Falcon-Ordaz, 1993; Eslava-Araujo, ante el Cambio Clima´tico Global). MRR is member of 2005; Garcıá-Prieto et al., 2012). In Costa Rica, a CONICET. Trichuris sp. has been reported in H. desmarestianus Gray (Chinchilla-Carmona et al., 2013). Further Compliance with ethical standards studies are necessary to verify if the new species occurs in other sympatric rodents in order to Conflict of interest The authors declare that they have no increase our knowledge on its geographical and conflict of interest. host distribution. Ethical approval All applicable institutional, national and Trichuris silviae n. sp. is the first species described international guidelines for the care and use of animals were from heteromyids in Mexico and the fourth in North followed. Host capture was conducted under license from America (Chandler, 1945; Read, 1956; Pfaffenberger Mexican Ministry of Environment (SGPA/DGVS/02528/13). & Best, 1989). Also, this is the sixth record of Trichuris spp. from rodents in Mexico, including the cosmopolitan T. muris recorded in native and non- References native rodents (Eslava-Araujo, 2005; Garcıá-Prieto et al., 2012). The family Heteromyidae consists of six Alexander, L. F., & Riddle, B. R. (2005). Phylogenetics of the new world rodent family Heteromyidae. Journal of Mam- genera (Chaetodipus Merriam, Dipodomys Gray, malogy, 86, 366–379. Heteromys, Liomys Merriam, Microdipodops Merriam Anderson, R. C. (2000). Nematode parasites of vertebrates: and Perognathus Wied-Neuwied) with more than 57 Their development and tranmission. 2nd edition. species distributed from Canada to Ecuador (Alexan- Wallingford, Oxon: CAB International, 650 pp. Babero, B. B., Cattan, P. E., & Cabello, C. (1975). Trichuris der & Riddle, 2005). The helminth fauna of hetero- bradleyi sp. n., a whipworm from Octodon degus in Chile. myids comprises more than sixteen nematode genera Journal of Parasitology, 61, 1061–1063. (see Read & Millemann, 1953; Grundmann, 1957; Babero, B. B., Cattan, P. E., & Cabello, C. (1976). A new spe- Frandsen & Grundmann, 1961b; Decker et al., 2001; cies of whipworm from the rodent Akodon longipilis in Chile. Transactions of the American Microscopical Soci- Falcon-Ordaz & Garcıá-Prieto, 2005). ety, 95, 232–235. Among heteromyids, Chaetodipus formosus Mer- Babero, B. B., & Murua, R. B. (1987). The helminth fauna of riam, C. hispidus, C. californicus, C. penicillatus Chile. X. A new species of whipworm from a Chilean Woodhouse, Dipodomys deserti Stephens, D. merri- rodent. Transactions of the American Microscopical Society, 106, 190–193. ami, D. microps Merriam, D. ordii, D. phillipsii, D. Babero, B. B., & Murua, R. B. (1990). A new species of spectabilis Merriam, H. desmarestianus and L. irro- whipworm from a South American hystricomorph rodent. ratus have been reported as hosts of Trichuris spp. Memorias do Instituto Oswaldo Cruz, 85, 211–213. from Costa Rica, Mexico, and USA (Doran, 1955; Barus, V., Majumdar, G., & Mikailov, T. K. (1975). Morphol- ogy and taxonomy of Trichocephalus myocastoris (Enigk, Grundmann, 1957; Munger & Slichter, 1995; Decker 1933). Folia Parasitologica, 22, 207–213. et al., 2001; Garcıá-Prieto et al., 2012; Chinchilla- Birney, E. C., Bowles, J. B., Timm, R. M., & Williams, S. L. Carmona et al., 2013). Additional field studies could (1974). Mammalian distributional records in Yucatan and 123 Syst Parasitol (2016) 93:721–730 729

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