THERYA NOTES 2024, Vol. 5 : 157-161 DOI: 10.12933/therya_notes-24-164 ISSN 2954-3614

Helminths parasites of heteromyid rodents from semiarid regions of México

Helmintos parásitos de roedores heterómidos de regiones semiáridas de México

Jorge Falcón-Ordaz1, Mitzi F. Aquino-Camacho1, Karla Ladrón de Guevara-Barcenas1, and Jesús A. Fernández2*

1Laboratorio de Morfología Animal, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo. Ciudad del Conocimiento, km 4.5 carretera Pachuca-Tulancingo, C. P. 42181, Mineral de la Reforma. Hidalgo, México. E-mail: profe_7864@uaeh.edu.mx (JF-O); aq420254@uaeh.edu.mx (MFA-C); la333646@uaeh.edu.mx (KLG-B).

2Universidad Autónoma de Chihuahua. Francisco R. Almada km 1, C. P. 31453, Chihuahua. Chihuahua, México. E-mail: afernandez@uach.mx (JAF).

*Corresponding author

As part of an ongoing project to inventory parasitic helminths of heteromyid rodents in México, various semiarid localities in the country have been sampled since 2002, collecting specimens from the genera Chaetodipus, Dipodomys, Heteromys and Perognathus, obtaining a total of 19 helminth species (3 platyhelminthes and 16 nematodes). For the present study, rodent and parasite sampling was carried out during the years 2007, 2008, 2015 and 2017, collecting 60 specimens of the family Heteromyidae (Chaetodipus sp., Dipodomys sp., D. merriami, D. ornatus, Heteromys irroratus and Perognathus flavus) from different semi-arid regions located in the states of Chihuahua, Coahuila, Guanajuato, Hidalgo, México, Puebla and San Luis Potosí. Derived from the dissection of the collected rodents, a total of 11 taxa of helminths were found: 2 cestode species (Hymenolepis morphotype 1 and morphotype 2) and 9 nematode taxa (Capillaria cf. americana, Heteromyoxyuris otomii, Physaloptera sp., Protospirura dipodomis, Pterygodermatites dipodomis, Syphacia sp., Trichuris sp., T. elatoris and Vexillata sp.). The presence of parasites with a indirect life cycle (e.g., Hymenolepis sp. and Pt. dipodomis) indicates that an insect species is part of the rodents diet. Seven of the 11 helminths found in this work coincide with those recorded in previous studies. Our results indicates that the biota of the semi-desert areas of México has elements of Nearctic affinity related it to southern United States of America.

Key words: Cestoda; geographic distribution; mammals; Nematoda; Rodentia.

Como parte de un proyecto en desarrollo para inventariar los helmintos parásitos de roedores heterómidos en México, se ha muestreado desde el año 2002 diversas localidades semiáridas del país, colectando los especímenes de los géneros Chaetodipus, Dipodomys, Liomys y Perognathus, obteniéndose un total de 19 helmintos (3 platelmintos y 16 nematodos). Para el presente estudio se llevaron a cabo muestreos de roedores y sus parásitos durante los años 2007, 2008, 2015 y 2017, recolectándose 60 especímenes de la familia Heteromyidae (Chaetodipus sp., Dipodomys sp., D. merriami, D. phillipsii ornatus, Heteromys irroratus y Perognathus flavus) de diferentes regiones semiáridas localizadas en los estados de Chihuahua, Coahuila, Guanajuato, Hidalgo, Estado de México, Puebla y San Luis Potosí. Derivado de la disección de los roedores recolectados se encontraron un total de 11 taxa de helmintos: 2 céstodos (Hymenolepis morfotipo 1 y morfotipo 2) y 9 nematodos (Capillaria cf. americana, Heteromyoxyuris otomii, Physaloptera sp., Protospirura dipodomis, Pterygodermatites dipodomis, Syphacia sp., Trichuris sp. T. elatoris y Vexillata sp.). La presencia de parásitos con ciclo de vida indirecto (e. g., Hymenolepis sp. y Pt. dipodomis) nos indica que dentro de la alimentación de los roedores existe la presencia de un insecto. Siete de los 11 helmintos encontrados en este trabajo coinciden con los registrados en estudios previos mostrando que la biota de las áreas semidesérticas de México cuenta con elementos de afinidad Neártica que la relacionan con el sur de los Estados Unidos de América.

Palabras clave: Cestoda; distribución geográfica; mamíferos; Nematoda; Rodentia.

© 2024 Asociación Mexicana de Mastozoología, www.mastozoologiamexicana.org

México has an area of 1,972,547 km², half of which consists of desert and semiarid regions. These areas cover most of the Baja California peninsula, large portions of the coastal plain and the low mountains of Sonora, nearly all of Coahuila and Nuevo León, part of Tamaulipas, and significant portions of Zacatecas, San Luis Potosí, the northeastern region of Guanajuato, Aguascalientes, and nearly all of Querétaro. Desert and semiarid regions are also found across parts of Hidalgo, Puebla, and a small portion of Oaxaca (Tarango 2005; Ceballos et al. 2014).

In México, 243 species of rodents have been recorded, 67 of which are found in the country's arid and semiarid zones (Ceballos et al. 2014). The most abundant family is Cricetidae, with 31 species, followed by Heteromyidae with 25 species, Sciuridae with 10 species, and Geomyidae with 2 species (Ceballos et al. 2014). México is the center of diversity for the Heteromyidae family, which is distributed in both the Nearctic and Neotropical zones. Many members of this family are adapted to arid and semiarid zones, with their highest diversity found in deserts. The family comprises 5 genera (Chaetodipus, Dipodomys, Heteromys, Microdipodops, and Perognathus) and includes approximately 63 species, 36 of which are found in México, distributed across 4 genera (excluding Microdipodops). Of these, 25 species are recorded in arid and semiarid zones (Alexander and Riddle 2005; Ceballos et al. 2014; Fernández et al. 2014; IUCN 2023).

The study of parasitic helminths in rodents of the Heteromyidae family began in México in 1970 with the description of Brachylaima bravoe, a parasite of Liomys (now Heteromys) pictus from Chamela, Jalisco (Caballero-Deloya 1970). Since then, taxonomic studies have been conducted on parasitic helminths of this family, with a total of 31 helminth species recorded (2 Trematoda, 3 Cestoda, and 26 Nematoda). These include 15 species found in Dipodomys, 14 in Heteromys, 7 in Chaetodipus, and 4 in Perognathus (Preisser and Falcón-Ordaz 2019). The majority of the heteromyid helminth species (21 species) have been recorded in the desert and semi-desert areas of Durango, Guanajuato, Hidalgo, Puebla, San Luis Potosí, Tlaxcala, Veracruz, and Zacatecas (Lamothe-Argumedo et al. 2005; García-Prieto et al. 2008; Falcón-Ordaz et al. 2012; Martínez-Salazar et al. 2016; Iturbe-Morgado et al. 2017). Therefore, it is important to continue studying the biodiversity of helminths in this biological system. Here, we present an update on the diversity of helminth species found parasitizing heteromyid rodents distributed in the arid and semiarid areas of México.

In June 2007, July 2008, December 2015, and May, August, October, and December 2017, a total of 60 rodent specimens belonging to the family Heteromyidae were collected in 11 semiarid localities across Chihuahua, Coahuila, Guanajuato, Hidalgo, State of México, Puebla, and San Luis Potosí states in México (Table 1; Figure 1). Rodent capture and handling followed approved methods issued by the American Society of Mammalogists (Kelt et al. 2010; Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2016). Collection permits granted to J. A. Fernández (FAUT-036) were issued by SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales). The collected specimens were euthanized, and their viscera were preserved in 70 % alcohol or 4 % formalin until further examination. Cestodes and nematodes were stored in 70 % alcohol, with cestodes stained using Delafield’s hematoxylin and mounted on slides in Canada balsam. Nematodes underwent morphological study using a mixture of glycerin and 70 % alcohol (2:1) for taxonomic identification. For scanning electron microscopy (SEM), 2 nematodes were dehydrated, critical-point dried, coated with a gold-palladium mixture (QUORUM Q150R), and examined with a Hitachi S-2460 N scanning electron microscope at 15 kV. The collected helminths were deposited in the Colección Nacional de Helmintos (CNHE) at the Instituto de Biología, UNAM, while mammal specimens (skin and skull) were deposited in the Colección de Mamíferos at the Facultad de Zootecnia and Ecología of the Universidad Autónoma de Chihuahua (UACH-M) and the Colección Nacional de Mamíferos (CNM), UNAM. Prevalence, intensity, and abundance values were calculated following the methodology of Bush et al. (1997).

Out of the 60 rodent specimens examined, 23 (38.33 %) were observed to be parasitized by helminths. A total of 470 worms were collected, representing 11 taxa of helminths from 2 phyla (Platyhelminthes and Nematoda), spanning 7 families (Hymenolepidae, Capillaridae, Oxyuridae, Ornithostrongylidae, Rictularidae, Spirocercidae, and Trichuridae (Table 1; Figure 2).

The highest species richness of parasites was observed in 2 rodent species, each harboring 3 species of helminths. Heteromys irroratus from Hidalgo, State of México, and Puebla was parasitized by 2 morphotypes of the genus Hymenolepis, and Vexillata sp.; meanwhile, Dipodomys merriami, from 3 localities in Coahuila and 1 in San Luis Potosí, was found parasitized by Protospirura dipodomis, Pterygodermatites dipodomis, and Syphacia sp. In Guanajuato, 2 nematode taxa, Capillaria cf. americana, and Trichuris sp., were collected from D. phillipsii ornatus. Three additional species of rodents were found parasitized by 1 taxa of nematode each: Chaetodipus sp. with Physaloptera sp., Dipodomys sp. with T. elatoris, both rodents collected in Chihuahua; and Perognathus flavus from Guanajuato with H. otomi.

The species and genera that exhibited the highest abundance at a locality (Table 1) were H. otommi, Syphacia sp., and Vexillata sp. with 115, 122, and 137 individual worms, respectively. It is noteworthy that Syphacia sp. and Vexillata sp. were collected from a single individual rodent each, while H. otomii was found in all 3 P. flavus individuals collected. Protospirura dipodomis also displayed high abundance with 45 individual worms, distributed across 4 localities (3 in Coahuila and 1 in San Luis Potosí). Other species of helminths were less abundant and were only found in 1 individual rodent each (Table 1).

In this study, we identified 6 species of helminths with monoxenous (direct) life cycles and 5 species with heteroxenous (indirect) life cycles. The presence of the parasites with monoxenous cycles suggests that their transmission is a result of caecotrophy, a behavior observed in animals that consume feces (Iturbe-Morgado et al. 2017). On the other hand, the presence of parasites with indirect life cycles, such as Hymenolepis morphotypes 1 and 2, P. dipodomis, Pt. dipodomis, and Physaloptera sp., indicates the presence of intermediate hosts like beetles, cockroaches, crickets, or grasshoppers. This suggests that the rodents parasitized by helminths with indirect life cycles likely have a diet that includes insects (Decker et al. 2001; Fedynich et al. 2001; Iturbe-Morgado et al. 2017).

Preisser and Falcón-Ordaz (2019) have been the only authors to date compiling records of 19 parasitic helminths (3 platyhelminths and 16 nematodes) in rodents of the family Heteromyidae in the semiarid regions of México. Some of these helminths such as H. longejector, Pt. dipodomis, and T. elatoris, are distributed among several host species throughout this region, including rodent species belonging to the genera Chaetodipus and Dipodomys. This host distribution can potentially be explained by co-evolution by descent, indicating that their ancestors were associated with each other in the past, and species inherited this association (Falcón-Ordaz et al. 2012; Iturbe-Morgado et al. 2017).

Although most helminth species had previously been collected from various locations in the semi-desert areas of México (Table 1), all records in this study represent new locations, expanding the geographic distribution of all species. It is noteworthy that Capillaria cf. americana has been discovered for the first time in México, and the genus Syphacia is parasitizing a species of Dipodomys for the first time as well.

With this study, the species richness of helminths parasitizing rodents of the family Heteromyidae has expanded to include 3 platyhelminths and 20 nematode species, with D. merriami hosting 13 species, while Chaetodipus sp., D. ornatus, and H. irroratus have been recorded with 5 species each (Preisser and Falcón-Ordaz 2019). Based on the composition of the helminth biota found in this study and previous works, it is possible to infer that the semi-desert region of México shares elements of Nearctic affinity, particularly with southwestern United States (New Mexico and Texas), as indicated by the presence of Hymenolepis sp., P. dipodomis, Pt. dipodomis, and Trichuris sp. (Decker et al. 2001; Falcón-Ordaz et al. 2012).

Acknowledgements

We are grateful to B. Mendoza-Garfias for her assistance in processing samples for the SEM photographs in the Laboratorio de Microscopía y Fotografía de la Biodiversidad I (IB-UNAM) and L. Garcia-Prieto for loaning specimens of the CNHE (IB-CNHE). Thanks to the reviewers for their thoughtful comments that helped improve our manuscript.

Literature cited

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Preisser, W. C., and J. Falcón-Ordaz. 2019. A checklist of the parasitic helminths of cricetid and heteromyid rodents in Mexico. Therya 10:329-341.

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Associated editor: Romeo A. Saldaña Vázquez.

Submitted: January 22, 2024; Reviewed: June 10, 2024.

Accepted: June 11, 2024; Published on line: June 19, 2024.

Figure 1. Map of semiarid areas of México (area shaded gray) showing the localities studied (codes in Table 1 in the Localities column).

Table 1. Localities in the arid and semiarid zones of México where rodents were collected for the helminth parasite survey. The characterization of the infection is also presented. The accession number of helminth in the Colección Nacional de Helmintos (CNHE) is show, n/d = not deposited. * Indirect life cycle; †Direct life cycle; ‡ Small and large intestine; § Stomach; || Intestinal cecum; # New host; ¶ New locality.

Phyllum

Family

Helminths collected (Intensity)

Host

(Sample size of hosts/number of host infected).

Localities

(numbers represent localities on Figure 1)

Prevalence %

Mean intensity

Abundance

CNHE

Platyelmintes

Hymenolepididae

Hymenolepis morphotype 1*‡#¶

1

Heteromys irroratus (3/1)

Cerro Gordo, Santiago Tolman, Mpio. Otumba, State of México (10)

33.33

1

0.33

n/d

Hymenolepis morphotype 2*‡ #¶M232

5

Heteromys irroratus (3/1)

1 km. S Sta. Cruz Coyotepec, Mpio. San Juan Atenco, Puebla (11)

33.3

5

1.66

n/d

Capillaridae

Capillaria

cf. americana † ||#¶

5

Dipodomys phillipsii ornatus (2/1)

2.5 km al SE de Mineral De Pozos, Mpio. Mineral De Pozos, Guanajuato (7)

50

1

2.5

11804

Oxyuridae

Syphacia sp. † ||#¶

122

Dipodomys merriami (6/1)

4.6 km S Ejido Mayran, Mpio. San Pedro de las Colonias, Coahuila (1)

16.66

122

20.33

n/d

Heteromyoxyuris otomii † ||¶

115

Perognathus flavus (3/3)

12.6 km al SE de Mineral De Pozos, Cuarto Blanco, Mpio. Dr. Mora, Guanajuato (8)

100

38.33

38.33

n/d

Nematoda

Ornithostrongylidae

Vexillata sp. †‡¶

137

Heteromys irroratus (3/1)

Ejido Gavillero, Mpio. Huichapan, Hidalgo (9)

33.33

137

45.66

n/d

Rictularidae

Pterygodermatites dipodomis *‡¶

5

Dipodomys merriami (10/1)

Ejido 4 de Marzo, Mpio. Parras, Coahuila (2)

10

5

0.5

11796

Spirocercidae

Protospirura dipodomis *§¶

2

Dipodomys merriami (6/2)

4.6 km S Ejido Mayran, Mpio. San Pedro de las Colonias, Coahuila (1)

33.33

1

0.33

11794

26

Dipodomys merriami (10/5)

Ejido 4 de Marzo, Mpio. Parras, Coahuila (2)

50

5.2

2.6

11795, 11798, 11799

5

Dipodomys merriami (6/2)

5 km S Ejido Talia, Mpio. Parras, Coahuila (3)

33.33

2.5

0.83

11797

12

Dipodomys merriami (2/2)

15km NE Villa de Reyes, Mpio. Villa de Reyes, San Luis Potosí (6)

100

6

6

11805

Physaloptera sp. * § #¶M366

24

Chaetodipus sp. (2/1)

Granjas Universitarias, Chihuahua (4)

50

24

12

8198

Trichuridae

Trichuris elatoris † || #¶M371

3

Dipodomys sp. (2/1)

Chihuahua, Chihuahua (5)

50

3

1.5

n/d

Trichuris sp. † || #¶M381

8

Dipodomys phillipsii ornatus (2/1)

2.5 km al SE de Mineral De Pozos, Mpio. Mineral De Pozos, Guanajuato (7)

50

8

4

n/d

Figure 2. Some species of nematodes collected. a - c. Male of Protospirura dipodomis. a) Scanning electron micrograph. Oral opening in face view (→ teeth; + pseudolabium, * papilla). b) Anterior end with an oral cavity (#). c) Posterior end showing caudal papilla (). d - e) Vexillata sp. d) Male caudal bursa, lateral view. e) Female, whole worm. f) Male of Pterygodermatites dipodomis showing the combs in the anterior end (“). g) Male, whole worm of Heteromyoxyuris otomii. h) Posterior end of male of Trichuris elatoris showing the spicule sheath. i). Female, whole worm of Syphacia sp.