Comparative Parasitology of Wild and Domestic ...

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Trichuris suis. Prevalence (egg): Four of 19 hosts infected (26%). Protozoans. Eimeria sp. Prevalence (egg): Ten of 19 hosts infected (52%). Isospora suis.
Comparative Parasitology of Wild and Domestic Ungulates in the Selva Lacandona, Chiapas, Mexico Author(s): Salvador Romero-Castañón , Bruce G. Ferguson , Dario Güiris , David González , Sergio López , Amelia Paredes , and Manuel Weber Source: Comparative Parasitology, 75(1):115-126. 2008. Published By: The Helminthological Society of Washington DOI: http://dx.doi.org/10.1654/4267.1 URL: http://www.bioone.org/doi/full/10.1654/4267.1

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Comp. Parasitol. 75(1), 2008, pp. 115–126

Comparative Parasitology of Wild and Domestic Ungulates in the Selva Lacandona, Chiapas, Mexico SALVADOR ROMERO-CASTAN˜O´N,1,5 BRUCE G. FERGUSON,1,6 DARIO GU¨IRIS,2 DAVID GONZA´LEZ,3 SERGIO LO´PEZ,1 AMELIA PAREDES,2 AND MANUEL WEBER4 1

El Colegio de la Frontera Sur, Carretera Panamericana y Perife´rico Sur s/n, San Cristo´bal de Las Casas, Chiapas, CP 29220, Mexico ([email protected], [email protected], [email protected]), 2 Policlı´nica y Diagno´stico Veterinario, Boulevard Angel Albino Corzo 635-B, Tuxtla Gutie´rrez, Chiapas, CP 29079, Mexico ([email protected], [email protected]), 3 El Colegio de la Frontera Sur, Avenida del Centenario Km 5.5, Chetumal, Quintana Roo, CP 79900, Mexico ([email protected]), 4 El Colegio de la Frontera Sur, Calle 10 X 61 No. 264, Colonia Centro Campeche, Campeche, CP 24000, Mexico ([email protected]), and 5 Current address: Escuela de Medicina Veterinaria y Zootecnia, Beneme´rita Universidad Auto´noma de Puebla, 4 sur 304. Col. Centro, Tecamachalco, Puebla, CP 75482, Mexico. ABSTRACT: We surveyed gastrointestinal and ectoparasites in wild and domestic ungulates in the Selva Lacandona, Chiapas, Mexico, including Baird’s tapir (Tapirus bairdii), collared peccary (Pecari tajacu), white-lipped peccary (Tayassu pecari), white-tailed deer (Odocoileus virginianus), red brocket deer (Mazama americana), horses (Equus caballus), cattle (Bos taurus), and pigs (Sus scrofa). We collected 97 fresh fecal samples from the domestic species and 46 from the wild species and examined digestive tracts of 21 wild specimens. We identified 18 species of nematodes and 7 species of protozoans in feces and 3 nematode species, 2 trematode species, and 1 cestode species during postmortem examination. Paramphistomid infections in peccaries and deer were both prevalent and intense, representing a potential risk to populations of these ungulates. Ectoparasites included 14 species of Ixodidae and a hippoboscid. Of the endoparasites, 10 are new host records and 15 are new geographic records for Mexico. Ectoparasites included 7 new host records and 14 new geographic records for Mexico. Morisita’s similarity index revealed the greatest similarity between the 2 deer species and between the 2 peccary species, while the greatest similarity between wild and domestic species was between B. taurus and O. virginianus. We discuss possible routes of interspecific transmission as well as the potential of the ectoparasites identified as disease vectors. KEY WORDS: cattle, Cestoda, Chiapas, deer, Hippoboscidae, horses, Ixodidae, Mazama, Nematoda, Odocoileus, Pecari, peccary, pigs, Protozoa, tapir, Tapirus, Tayassu, Trematoda.

2004). Odocoileus virginianus prospers at forest–field edges (Matschke et al., 1984; Reid, 1997); M. americana prefers forest habitat but may venture into open areas (Reid, 1997); Tay. pecari (Sowls, 1997) and Tap. bairdii (Reid, 1997) prefer forest interior; and P. tajacu is a habitat generalist (Sowls, 1997). Extensive cattle (Bos taurus) ranching is the principal livestocking activity in the area. As in other regions of Chiapas, cattle often graze in fallows and forest edges as well as pastures (Jimenez-Ferrer et al., 2003, http://leades.virtualcentre.org/es/ele/conferencia4/ programa.htm). Farmyard pig (Sus scrofa) production is less common and practiced on a small scale (Naranjo et al., 2004). Horses (Equus caballus) are widely used for transportation and traction and frequently penetrate the forest interior. Forest fragmentation, habitat preferences of several of the wild ungulates, and livestock management combine to produce significant interspecific overlap. This frequently extensive overlap in habitat use and the phylogenetic affiliation among these ungulates

This study documents parasites in wild and domestic ungulates in the Selva Lacandona, Chiapas, Mexico. The Lacandona is a region of increasingly fragmented lowland rainforest that is protected in part within the Montes Azules Biosphere Reserve (MABR). Wild ungulates in the Lacandona include Baird’s tapir (Tapirus bairdii), the white-lipped peccary (Tayassu pecari), the collared peccary (Pecari tajacu), the white-tailed deer (Odocoileus virginianus), and the red brocket deer (Mazama americana). Tapirus bairdii is endangered throughout its distribution (International Union for the Conservation of Nature, 1996), and Tay. pecari faces diminishing populations and range collapse in Mexico (Naranjo et al., 2004). The other 3 species are locally abundant and are among the prey most frequently taken by subsistence hunters in southeastern Mexico and Central America (Naranjo et al.,

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Figure 1. Location of the study area, communities, and transects.

(Young, 1977) create potential for interspecific transmission of parasites and diseases. As has been recently suggested, some attributes of forest fragmentation and management (such as the intensity of tree extraction) might result in altered patterns of host– parasite dynamics in tropical forest ecosystems (Gillespie and Chapman, 2006). Parasites of O. virginianus and the infections it shares with domestic ungulates are well documented in Canada and the United States (e.g., Park et al., 1966; Prestwood et al., 1975; Foreyt and Russell, 1980; Matschke et al., 1984; McKenzie and Davidson, 1989; Forrester et al., 1996; Schmidtmann et al., 1998; Samuel et al., 2001). However, parasite infections in the other wild ungulates are less well known, and no report of these species has been published for Mexico. This survey of endo- and ectoparasites of ungulates in an agricultural frontier region of Mexico is pioneering in both its geographic focus and its comparative nature. Here, we provide initial data on the composition, prevalence, and intensity of parasite infection as well as similarities in parasites found among ungulate hosts. We identify possible instances of interspecific transmission of parasites and potential risks of disease transmission among ungulates and between ungulates and humans.

MATERIALS AND METHODS Study area We worked in the MABR (between 168139N, 908549W and 16869N, 908599W) and in 3 adjacent communities established in recent decades: Playo´n de la Gloria (168099N, 908539W) and Flor de Marque´s (16899N, 908529W), both in the Marque´s de Comillas municipality, and Loma Bonita (16859N, 908589W), in the Ocosingo municipality, in the State of Chiapas, Me´xico (Fig. 1). The mean annual temperature is 258C, and the area receives an average of 3,000 mm of rain, 80% of which falls between June and November (Naranjo et al., 2004). The native vegetation is evergreen lowland rain forest. The land surrounding the communities is a mosaic of pastures, annual crops (principally corn, beans, and chili peppers), cacao plantations, and rain forest in a range of successional stages from young fallows to mature stands (Naranjo et al., 2004). Sampling We sampled January through October 2005, dividing the sampling effort approximately equally between the dry and rainy seasons. Domestic ungulates: Because no opportunity for necropsy arose during the study period, we relied exclusively on fecal collection to sample endoparasites of domestic ungulates. Of the total livestock population in the 3 communities, we collected fecal samples from 5% of B. taurus, 100% of S. scrofa, and 43% of E. caballus individuals. For B. taurus we took samples directly from the rectum, while for the other 2 species we collected feces immediately following

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defecation. We ensured that our sample of B. taurus represented animals subjected to a range of management conditions by selecting 3 animals from each of 3 different enclosures in each of the 3 communities. These grazing areas included open pasture, grazed tree fallows, and pasture–fallow mixtures. We sampled ectoparasites only from B. taurus, using the same sampling scheme and individuals as for endoparasites. We collected 5 ectoparasites .4.5 mm long from the head, neck, belly, scrotum, or udder and tail of each host (Secretarı´a de Agricultura, Ganaderı´a, Desarrollo Rural, Pesca y Alimentacio´n, 2003, unpublished manual, Tuxtla Gutie´rrez, Chiapas, Mexico). To evaluate ectoparasite intensity, we counted all ticks .4.5 mm long on 1 side of the animal’s body and multiplied the result by 2. We sampled only animals that had not been treated for endo- or ectoparasites during the previous 6 mo. Wild ungulates: Once monthly over the 10-mo study period, we collected fresh feces from the ground (and from the water in the case of Tap. bairdii) along 10 transects following trails and streams. Seven transects were within MABR, and 3 were in the vicinity of the communities. The transects averaged 2,142 6 608 (6SD) m, for a total length of over 21 km. Additionally, we collected parasites from ungulates taken by subsistence hunters from the 3 communities. To this end, we lived in the communities and accompanied hunting parties for 12 d of each month. To increase our sample size, we also trained hunters to collect ectoparasites and to preserve the digestive tracts of their prey in a 10% formaldehyde solution. We sampled ectoparasites using the same protocol described for domestic animals. We examined the digestive tract from esophagus to rectum for adult nematodes, trematodes, and cestodes, and we collected feces from the rectum. We labeled and preserved ecotoparasites and adult gastrointestinal parasites in 70% alcohol and fecal samples in 10% formalin (1 volume formalin per 4 of feces). Analysis and terminology Samples were processed at the Policlı´nica y Diagno´stico Veterinario Laboratory, Tuxtla Gutierrez, Chiapas. Flotation techniques were used to identify nematode and cestode eggs and protozoan oocysts, while sedimentation techniques were used for trematode eggs (Thienpont et al., 1979). Ectoparasites and adult helminths were identified using available taxonomic keys (Whitlock, 1960; Lapage, 1971; Jones et al., 1972; Thienpont et al., 1979; Graciolli and Barros, 2003). Specimens were deposited in the parasite collection of El Colegio de la Frontera Sur, Chetumal campus, Mexico (ECOPA). The ecological and epidemiological terms used in this study follow Margolis et al. (1982). We calculated prevalence for each species of parasite, as well as intensity of adult gastrointestinal parasites and ectoparasites for each host species. We could not use the MacMaster technique (Thienpont et al., 1979) to calculate egg intensity because of the low density of eggs in the feces of the wild ungulates. We chose Morisita’s similarity index to quantify resemblance in parasite assemblages across host species because this measure is independent of sample size (Krebs, 1999). We used SIMIL software (Pe´rez-Lo´pez and SolaFerna´ndez, 1993, http://entomologia.iespana.es/descargas/ calculodelasmedidasdesimilitnd.html) for this analysis.

Figure 2. Similarity in ecto- and endoparasite communities among ungulates (dendrogram based on Morisita’s similarity index).

RESULTS We obtained 97 fecal samples from domestic ungulates and 46 from wild ungulates. We sampled 21 hunted animals, mostly P. tajacu. We identified 25 parasite species through fecal tests, including 18 nematodes and 7 protozoans. We identified 6 parasite species through postmortem examination, including 3 nematodes, 2 trematodes, and 1 cestode. Sus scrofa harbored the greatest diversity of intestinal parasites, with 12 species, while the 2 peccary species hosted the greatest variety of endoparasites among the wild ungulates, with 7 species each. We sampled 52 B. taurus and 12 wild ungulates for ectoparasites. Of the 16 parasite species encountered, 15 were ticks in the family Ixodidae, and 1 was a dipteran from the family Hippoboscidae. Mazama americana hosted the greatest diversity of ectoparasites, with 8 species. Based on Morisita’s similarity index, the greatest similarity in parasite community composition for endo- and ectoparasites combined was between the 2 peccary species (0.50; 7 species in common) and between the 2 deer species (0.48, 3 species in common; Fig. 2). The greatest similarity between wild and domestic species was between B. taurus and O. virginianus (0.29; 5 spp. in common). Similarity in endoparasite communities followed a similar pattern and was greatest between the 2 deer species (0.5; 1 species in common), and between the 2 peccaries (0.416; 4 species in common). Bos taurus and O. virginianus had a similarity index of 0.276, with 2 species in common (Fig. 3).

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Figure 3. Similarity in endoparasite communities among ungulates (dendrogram based on Morisita’s similarity index).

Figure 4. Similarity in ectoparasite communities among ungulates (dendrogram based on Morisita’s similarity index).

Site of infection: Stomach. The greatest similarity for ectoparasites was that between the 2 peccaries (0.873; 3 species in common), followed by the 2 deer (0.422; 2 species in common). Bos taurus and O. virginianus had a similarity index of 0.332 with 3 species in common (Fig. 4). Tayassuidae Pecari tajacu (Linnaeus, 1758) (Syn. Tayassu tajacu Linnaeus, 1758) Digestive tracts of 13 P. tajacu adults were inspected, and 5 were also examined for ectoparasites. These animals were hunted in the MABR (n ¼ 4 for endoparasites, n ¼ 1 for ectoparasites; 168139N, 908549W), and near the communities of Loma Bonita (n ¼ 5 for endoparasites, n ¼ 3 for endoparasites; 16859N, 908589W) and Flor de Marque´s (n ¼ 4 for endoparasites, n ¼ 1 for ectoparasites; 16899N, 908529W). Fifteen fecal samples from the same localities were tested. Because not all of the ticks infecting this host were identified, we calculated intensity for all ixodids combined: 35.6 6 7.6, 26–44.

Specimens deposited: ECOPA 018 (3 vials). Prevalence (egg): Three of 15 hosts infected (20%). Additional reports from P. tajacu: None. Remarks: Pecari tajacu represents a new host record for G. urosubulatus. Oesophagostomum sp. Prevalence (egg): Two of 15 hosts infected (13%). Parabronema pecariae Ivaschkin, 1960 Prevalence and intensity: Four of 13 hosts infected (31%, 8.7 6 10.4, 1–24). Site of infection: Stomach. Additional reports from P. tajacu: New Mexico, U.S.A. (Samson and Donaldson, 1968); Texas, U.S.A. (Samuel and Low, 1970; Corn et al., 1985); Brazil (Vicente et al., 2000). Specimens deposited: ECOPA 019 (4 vials).

Nematoda Globocephalus urosubulatus Alesandrini, 1909 Prevalence and intensity (necropsy): Three of 13 hosts infected (23%, 2.3 6 0.57, 2–3).

Remarks: Mexico is a new locality record for P. pecariae. Paraostertagia sp. Prevalence (egg): One of 15 hosts infected (7%).

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Texicospirura turki Chitwood and Cordero de Campillo, 1966

Remarks: Mexico is a new locality record for A. cajennense.

Prevalence and intensity: One of 13 hosts infected (8%, 2).

Amblyomma inornatum Banks, 1909

Site of infection: Stomach. Additional reports from P. tajacu: Texas (Chitwood and Cordero de Campillo, 1966; Samson and Donaldson, 1968; Samuel and Low, 1970; Corn et al., 1985); New Mexico (Chitwood and Cordero de Campillo, 1966).

Prevalence: Three of 5 hosts infected (60%). Additional reports from P. tajacu: Texas (Samuel and Low, 1970; Meleney, 1975). Specimens deposited: ECOPA 024 (3 vials). Remarks: Mexico is a new locality record for A. inornatum.

Specimens deposited: ECOPA 020 (1 vial). Remarks: Mexico is a new locality record for T. turki. Trematoda Paramphistomum sp. Prevalence and intensity: Eight of 13 hosts infected (61%, 51.6 6 37.2, 12–119). Sites of infection: Stomach, large intestine. Additional reports from P. tajacu: None. Specimens deposited: ECOPA 021 (8 vials). Remarks: Pecari tajacu represents a new host record for this genus.

Amblyomma pecarium Dunn, 1933 Prevalence: Two of 5 hosts infected (40%). Additional reports from P. tajacu: Belize and Mexico (Fairchild et al., 1966). Specimens deposited: ECOPA 025 (2 vials). Tayassu pecari (Link, 1795) The 2 white-lipped peccaries examined were hunted between January and October 2005 in the MABR (168139N, 908549W) and near Flor de Marque´s (16899N, 908529W). Tests were performed on 4 fecal samples. Because not all of the ticks infecting this host were identified, we calculated intensity for all ixodids combined: 62 6 11.3, 54–70.

Cestoda Moniezia benedeni Moniez, 1879

Nematoda

Prevalence and intensity: One of 13 hosts infected (8%, 27).

Bunostomum sp. Prevalence (egg): One of 4 hosts infected (25%).

Site of infection: Small intestine. Additional reports from P. tajacu: Texas (Samson and Donaldson, 1968; Samuel and Low, 1970; Corn et al., 1985). Specimens deposited: ECOPA 022 (1 vial). Remarks: Mexico is a new locality record for M. benedeni. Arthropoda Amblyomma cajennense Fabricius, 1787 Prevalence: One of 5 hosts infected (20%). Additional reports from P. tajacu: Texas (Samuel and Low, 1970; Meleney, 1975) and Panama (Fairchild et al., 1966). Specimens deposited: ECOPA 023 (1 vial).

Oesophagostomum sp. Prevalence (egg): One of 4 hosts infected (25%). Parabronema pecariae Prevalence and intensity: One of 2 hosts infected (50%, 17). Site of infection: Stomach. Additional reports from Tay. pecari: Brazil (Vicente et al., 2000). Specimens deposited: ECOPA 026 (1 vial). Remarks: Mexico is a new locality record for this genus. Paraostertagia sp. Prevalence (egg): Two of 4 hosts infected (50%).

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Trichostrongylus sp.

Cervidae

Prevalence (egg): Two of 4 hosts infected (50%). Trematoda Paramphistomum sp. Prevalence and intensity: One of 2 hosts infected (50%, 326). Site of infection: Stomach. Specimens deposited: ECOPA 027 (1 vial). Remarks: Tayassu pecari represents a new host record for this genus. Cestoda Moniezia benedeni Prevalence and intensity: One of 2 hosts infected (50%, 11).

Odocoileus virginianus (Zimmermann, 1780) Two adult white-tailed deer, hunted between January and October, 2005, near Loma Bonita (16859N, 908589W) and Flor de Marque´s (16899N, 908529W), were examined for endoparasites. Three fecal samples from the same localities were also tested. Ectoparasites were also collected from the second animal. Because not all of the ticks infecting this host were identified, we calculated intensity for all ixodids combined: 32. Nematoda Bunostomum sp. Prevalence (egg): One of 3 hosts infected (33%). Capillaria sp. Prevalence (egg): One of 3 hosts infected (33%).

Site of infection: Small intestine. Specimens deposited: ECOPA 028 (1 vial). Remarks: Tayassu pecari represents a new host record for M. benedeni. Arthropoda Amblyomma cajennense Prevalence: One of 2 hosts infected (50%). Additional reports from Tay. pecari: Bolivia (Robbins et al., 1998). Specimens deposited: ECOPA 029 (1 vial). Remarks: Mexico is a new locality record for A. cajennense. Amblyomma inornatum Prevalence: One of 2 hosts infected (50%). Specimens deposited: ECOPA 030 (1 vial). Remarks: Tayassu pecari represents a new host record for A. inornatum. Amblyomma pecarium Prevalence: Two of 2 hosts infected (100%). Additional reports from Tay. pecari: Belize and Mexico (Fairchild et al., 1966) and Bolivia (Robbins et al., 1998). Specimens deposited: ECOPA 031 (2 vials).

Trematoda Paramphistomum cervi Zeder, 1790 Prevalence and intensity: One of 2 hosts infected (50%, 317). Sites of infection: Rumen and abomasum. Specimens deposited: ECOPA 032 (1 vial). Remarks: Odocoileus virginianus represents a new host record for P. cervi. Arthropoda Amblyomma maculatum Koch, 1844 Prevalence: One of 1 host infected (100%). Additional reports from O. virginianus: U.S.A. (Smith, 1977). Specimens deposited: ECOPA 033 (1 vial). Remarks: Mexico is a new locality record for A. maculatum. Boophilus annulatus Say, 1821 Prevalence: One of 1 host infected (100%). Additional reports from O. virginianus: Mexico (Weber, 1992, unpublished data; Villarreal, 1999); U.S.A. (Smith, 1977 unpublished thesis, University of Georgia, U.S.A.). Specimens deposited: ECOPA 034 (1 vial).

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Dermacentor albipictus Packard, 1869 Prevalence: One of 1 host infected (100%). Additional reports from O. virginianus: U.S.A. (Smith, 1977 unpublished thesis, University of Georgia, U.S.A.).

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Amblyomma pseudoconcolor Aragao, 1908 Prevalence: One of 4 hosts infected (25%). Specimens deposited: ECOPA 039 (1 vial). Remarks: Mazama americana represents a new host record for A. pseudoconcolor.

Specimens deposited: ECOPA 035 (1 vial). Remarks: Mexico is a new locality record for D. albipictus. Ixodes scapularis Say, 1821 Prevalence: One of 1 host infected (100%). Additional reports from O. virginianus: U.S.A. (Smith, 1977 unpublished thesis, University of Georgia, U.S.A.). Specimens deposited: ECOPA 036 (1 vial). Remarks: Mexico is a new locality record for I. scapularis. Mazama americana (Erxleben, 1777) Four adult red brocket deer hunted between January and October 2005 near Flor de Marque´s (16899N, 908529W) were examined for gastrointestinal parasites and ectoparasites. Five fecal samples from the same localities were also tested but revealed no parasites. Because not all of the ectoparasites infecting this host were identified, we calculated intensity for all ixodids and hippoboscids combined: 28.5 6 10.1, 16–40.

Anocentor nitens Neumann, 1897 Prevalence: One of 4 hosts infected (25%). Specimens deposited: ECOPA 040 (1 vial). Remarks: Mazama americana represents a new host record for A. nitens. Dermacentor albipictus Prevalence: Three of 4 hosts infected (75%). Specimens deposited: ECOPA 041 (1 vial). Remarks: Mazama americana represents a new host record for D. albipictus. Haemaphysalis sp. Prevalence: One of 4 hosts infected (25%). Additional reports from M. americana: Cooley, 1946 (cited in Jones et al., 1972) reports Haemaphysalis juxtacochi but the collection location is unclear. Specimens deposited: ECOPA 042 (1 vial). Ixodes scapularis Prevalence: Two of 4 hosts infected (50%).

Trematoda

Specimens deposited: ECOPA 043 (1 vial).

Paramphistomum cervi

Remarks: Mazama americana represents a new

Prevalence and intensity: Four of 4 hosts infected (100%, 260.2 6 55.3, 211–324). Sites of infection: Rumen and abomasum. Specimens deposited: ECOPA 037 (1 vial). Remarks: Mazama americana represents a new host record for P. cervi.

host record for I. scapularis. Ixodes sp. Prevalence: One of 4 hosts infected (25%). Specimens deposited: ECOPA 044 (1 vial). Lipoptena mazamae Rondani, 1878 Prevalence: Four of 4 hosts infected (100%).

Arthropoda Amblyomma americanum Linnaeus, 1758 Prevalence: One of 4 hosts infected (25%). Specimens deposited: ECOPA 038 (1 vial). Remarks: Mazama americana represents a new host record for A. americanum.

Additional reports from M. americana: For Mazama sp. in Central and South America (Bequaert, 1957). Specimens deposited: ECOPA 045 (1 vial). Remarks: Mexico is a new locality record for L. mazamae.

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Tapiridae Tapirus bairdii Gill, 1865 Nineteen fecal samples were collected between January and October 2005 in the MABR (168139N, 908549W and 16869N, 908 599W).

Oesophagostomum sp. Prevalence (egg): Two of 52 hosts infected (4%). Ostertagia sp. Prevalence (egg): Four of 52 hosts infected (8%). Trichostrongylus axei

Nematoda

Prevalence (egg): Three of 52 hosts infected (6%).

Bunostomum sp. Prevalence (egg): Two of 19 hosts infected (10%). Remarks: Mexico is a new locality record for this genus.

Protozoans Eimeria sp. Prevalence (egg): Nine of 52 hosts infected (18%). Arthropoda

Nematodirus sp. Prevalence (egg): Sixteen of 19 hosts infected (84%). Remarks: Tapirus bairdii represents a new host record for this genus. Tapironema coronatum Prevalence (egg): One of 19 hosts infected (5%). Remarks: Mexico is a new locality record for T. coronatum.

Amblyomma cajennense Prevalence: Thirty of 52 hosts infected (58%). Specimens deposited: ECOPA 046 (1 vial). Amblyomma maculatum Prevalence: Seven of 52 hosts infected (13%). Specimens deposited: ECOPA 047 (1 vial). Boophilus annulatus Prevalence: Fifteen of 52 hosts infected (29%).

Trichonema sp.

Specimens deposited: ECOPA 048 (1 vial).

Prevalence (egg): Two of 19 hosts infected (10%). Remarks: Mexico is a new locality record for this genus.

Boophilus microplus Camestrini, 1887 Prevalence: Seventeen of 52 hosts infected (32%). Specimens deposited: ECOPA 049 (1 vial).

Bovidae Bos taurus

Dermacentor andersoni Stiles Prevalence: One of 52 hosts infected (2%).

Fecal samples and ectoparasites were collected from 52 animals; 18 in Loma Bonita (16859N, 908589W), 18 in Flor de Marque´s (16899N, 908529W), and 16 in Playo´n de la Gloria (168099N, 908539W). We calculated intensity for all ixodids combined: 24 6 12.8, 8–72.

Hyalomma sp.

Nematoda

Ixodes scapularis

Bunostomum sp. Prevalence (egg): Three of 52 hosts infected (6%).

Specimens deposited: ECOPA 050 (1 vial).

Prevalence: Two of 52 hosts infected (4%). Specimens deposited: ECOPA 051 (1 vial).

Prevalence: Three of 52 hosts infected (6%). Specimens deposited: ECOPA 052 (1 vial).

Capillaria sp. Prevalence (egg): Two of 52 hosts infected (4%).

Equidae Equus caballus

Haemonchus sp. Prevalence (egg): Four of 52 hosts infected (8%).

Fecal samples were collected from 26 animals: 7 in Loma Bonita (16859N, 908589W), 6 in Flor de

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Marque´s (908529N, 16899W), and 13 in Playo´n de la Gloria (168099N, 908539W).

Trichostrongylus sp.

Nematoda

Trichuris suis

Strongyloides sp.

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Prevalence (egg): One of 19 hosts infected (5%).

Prevalence (egg): Four of 19 hosts infected (26%).

Prevalence (egg): One of 26 hosts infected (4%). Protozoans

Strongylus sp. Prevalence (egg): Four of 26 hosts infected (15%). Trichonema sp. Prevalence (egg): Six of 26 hosts infected (23%).

Eimeria sp. Prevalence (egg): Ten of 19 hosts infected (52%). Isospora suis Prevalence (egg): Six of 19 hosts infected (31%).

Trichostrongylus axei Prevalence (egg): Two of 26 hosts infected (8%). Trichostrongylus sp. Prevalence (egg): Two of 26 hosts infected (8%). Triodontophorus sp. Prevalence (egg): Seven of 26 hosts infected (27%). Suidae Sus scrofa Fecal samples were collected from 19 animals: 15 in Loma Bonita (16859N, 908589W), 2 in Flor de Marque´s (908529N, 16899W), and 2 in Playo´n de la Gloria (168099N, 908 539W). Nematoda Ascaris suum Prevalence (egg): Seven of 19 hosts infected (37%). Globocephalus urosubulatus Prevalence (egg): One of 19 hosts infected (5%). Metastrongylus sp. Prevalence (egg): Two of 19 hosts infected (10%). Oesophagostomum sp. Prevalence (egg): Five of 19 hosts infected (26%). Paraostertagia sp. Prevalence (egg): One of 19 hosts infected (5%). Strongyloides sp. Prevalence (egg): Two of 19 hosts infected (10%).

DISCUSSION We provide 10 new host reports and 15 new geographic records for parasites of wild ungulates in Mexico. Two-thirds of the 30 endoparasite taxa identified were nematodes. Of these, Nematodirus sp. in Tap. bairdii exhibited the greatest prevalence (84%). Identified through eggs in fecal samples, this parasite is common in bovids and cervids (Samuel et al., 2001) and has also been found in alpaca (Lama pacos) and vicun˜a (Vicugna vicugna) in Peru (Becklund, 1963). This is the first report from a monogastric ungulate. Nematodirus can cause acute enteritis in ruminants (Soulsby, 1987). Parabronema pecariae (order Spiruroidea), was among the most prevalent nematodes in both peccary species. Observed prevalence was consistent with that reported for P. tajacu in Texas (Samuel and Low, 1970) but much greater than that found in another study in the same region (Corn et al., 1985). The nematodes infecting the broadest range of hosts were Bunostomum sp. (B. taurus, O virginianus, Tay. pecari, and Tap. bairdii) and Oesophagostomum sp. (B. taurus, S. scrofa, Tay. pecari, and P. tajacu). Identified by egg flotation, both species were present at low prevalence. Infestation occurs orally, and in the case of Bunostomum sp. also through the skin (Quiroz, 1994). Both S. scrofa and P. tajacu were infected by Globocephalus urosubulatus, although at low intensity in the latter host. Severe infestations can cause anemia in S. scrofa (Soulsby, 1987). Trichonema sp., identified from eggs, was also shared by wild and domestic ungulates. This nematode exhibited high prevalence in both E. caballus and Tap. bairdii and is know to cause catarrhal descamative enteritis in equines (Soulsby, 1987). The trematodes collected were paramphistomids, present in all deer species and peccary species.

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Transmission is through ingestion of metacercaria that emerge from aquatic snails of the genus Lymnaea (Trejo et al., 1989; Quiroz, 1994). These helminths can cause severe diarrhea as well as intestinal and intermaxillary edemas (Quiroz, 1994). Given that their prevalence and intensity were among the highest detected, this parasite represents a potential risk to host populations. The only cestode collected, Moniezia benedeni, was present in both peccaries at low prevalence and moderate intensity, consistent with previous reports for P. tajacu in Texas (Samuel and Low, 1970; Corn et al., 1985). This helminth can induce intestinal irritation, abdominal edema, diarrhea with constipation, and anemia (Lapage, 1971). It is transmitted indirectly via orbatid mites (Lapage, 1971; Soulsby, 1987). We found protozoans only in B. taurus and S. scrofa. Of these, I. suis and Eimeria sp. were prevalent in S. scrofa. Ectoparasites We report 7 new host records and 14 new locality records for Mexico of ectoparasites of wild ungulates. Of the 15 ixodid species collected, the most prevalent was Amblyomma cajennense, present on B. taurus, P. tajacu, and Tay. pecari. These ticks can transmit Rickettsia rickettsii, the bacterium that causes Rocky Mountain spotted fever in the United States, Canada, and central and western Mexico (Acha and Szyfres, 1992; Samuel et al., 2001). The tick Boophilus annulatus, identified from B. taurus and O. virginianus, can transmit the pyroplasm Babesia bovis (Soulsby, 1987; Samuel et al., 2001). Boophilus annulatus is also a vector of bovine anaplasmosis (Samuel et al., 2001). Another common parasite on these 2 hosts was Ixodes scapularis, which we also found on M. americana. This suggests a possible chain of transmission from B. taurus to M americana mediated by O. virginianus, whose habitat preference overlaps with that of the other 2 hosts. Ixodes scapularis can transmit pyroplasmosis (Soulsby, 1987). Dermacentor albipictus, present in both deer species, can transmit anaplasmosis and has been reported to cause severe alopecia in moose and caribou (Samuel, 1989; Welch et al., 1990; Samuel et al., 2001). We identified A. americanum and A. pseudoconcolor from M. americana. The former tick transmits tularemia and is also a vector of Babesia cervi and Babesia odocoilei (Waldrup et al., 1989; Samuel et al., 2001) and Ehrlichia chaffeensis (Samuel et al., 2001; Varela et al., 2004). The hippoboscid L. mazamae, identified in all 4 M.

americana, can transmit cervid trypanosomiasis (Trypanosoma cervi) and may be a vector of Bartonella spp. (Baker, 1967; Forrester et al., 1996). The wild ungulates exhibited the greatest intensity of ectoparasite infestation. Pathogen isolation studies are necessary to evaluate the risk that these parasites might pose to their hosts. We found the greatest similarity in parasite communities between wild hosts belonging to the same families (Tayassuidae, Cervidae), probably reflecting similarities in diet and habitat preferences. Similarity between domestic and wild hosts was relatively low for endoparasites, but we observed some similarity in ectoparasites between cattle and wild ungulates, particularly O. virginianus. This finding is based on a single O. virginianus specimen but suggests the possibility that this host, which favors fragmented landscapes, edges, and pastures (Matschke et al., 1984), acts as a permanent reservoir for some ticks. While many of the parasites collected are shared among host families, others exhibit a degree of specificity. Such is the case of those ectoparasites that infest only the 2 peccary species (A. inornatum and A. pecarium) or only M. americana (L. mazamae). Several endoparasites (P. pecariae, T. turki, M. benedeni) were also specific to the peccaries, suggesting coevolution between the hosts and these parasites (Adamson and Caira, 1994). By contrast, those parasites that use intermediate hosts exhibit less specificity, an adaptation that increases their probability of reaching their final hosts (Adamson and Caira, 1994). The paramphistomids, identified in 4 host species, conformed to this generalization. Several of the ectoparasites identified present zoonotic potential (e.g. Ewing et al., 1997; Samuel et al., 2001; Fang et al., 2002; Jacobs et al., 2003; Halos et al., 2004). Pathogen isolation studies are needed to evaluate the degree of risk.

ACKNOWLEDGMENTS We are grateful to Eduardo Naranjo Pin˜era of El Colegio de la Frontera Sur, Rube´n Jime´nez Alvarez, and the hunters and ranchers of the study communities for their generous collaboration during the field work. We also thank Emmanuel Valencia Barrera, Adria´n Sarabia Rangel, and Alejandro Flamenco Sandoval of El Colegio de la Frontera Sur for help with the figures and Reinaldo Jose´ da Silva for bibliographic material helpful in determination of

˜O ´ N ET AL.—PARASITES OF UNGULATES IN CHIAPAS ROMERO-CASTAN

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