788_Urotrema_2

THERYA, 2020, Vol. 11 (2): 181-192 DOI: 10.12933/therya-20-788 ISSN 2007-3364

First record of Urotrema scabridum (Platyhelminthes), and new records of helminths of Tadarida brasiliensis from Mexican Plateau

Elizabeth A. Martínez-Salazar1*, Andrea J. Medina-Rodríguez1, Rogelio Rosas-Valdez1, Melina Del Real-Monroy2, and Jorge Falcón-Ordaz3

1 Laboratorio de Colecciones Biológicas y Sistemática Molecular, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas. Av. Preparatoria S/N, Campus Universitario II, Col. Agronómica, C. P. 98066. Zacatecas, México. Email: eamsuaz@gmail.com; eamskandii@gmail.com (EAM-S), lunita325@hotmail.com (AJM-R), rogrosas@gmail.com (RR-V).

2 Laboratorio de Genómica Evolutiva, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas. Av. Preparatoria S/N, Campus Universitario II, Col. Agronómica, C. P. 98066. Zacatecas, México. Email: melir17@hotmail.com (MDR-M).

3 Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas. Apartado Postal 1-10, C. P. 42001, Pachuca de Soto. Hidalgo, México. Email: jfalcon.ordaz@gmail.com (JF-O).

*Corresponding author

The Mexican free-tailed bat (Tadarida brasiliensis) is an abundant, widely distributed species in Mexico, except for most of the Yucatán peninsula. We studied the helminth fauna of T. b. mexicana at seven localities in the State of Zacatecas in order to advance the knowledge of helminth parasites of wild vertebrates in northern-central Mexico. Eighty-four bat specimens were examined for the presence of helminth parasites following standard procedures; helminths found were identified and infections were characterized. Of the specimens examined, 65.47 % were parasitized. The helminth fauna comprises five taxa: three digeneans (Dicrocoelium rileyi, Ochoterenatrema labda, and Urotrema scabridum); one cestode (Vampirolepis sp.); and one nematode (Tadaridanema delicatus). We present a brief morphological description of Urotrema scabridum. D. rileyi was the most prevalent and abundant helminth species. The intestine was the habitat most parasitized, with four species. Indirect life cycles predominate, and are related to the insectivorous habits of this host. Further studies on this host-parasite system are necessary to contribute to population monitoring and conservation; biogeographic patterns of helminth parasites of bats should also be studied to explore their origins and evolution in the region. U. scabridum is reported for the first time from Zacatecas. All species are new locality records.

El murciélago de cola libre mexicano (Tadarida brasiliensis), es una especie abundante y ampliamente distribuida en México, excepto en la mayor parte de la península de Yucatán. Para contribuir al conocimiento de los helmintos parásitos de vertebrados de vida silvestre en el centro-norte de México, la fauna helmíntica de T. b. mexicana se estudió en siete localidades del estado de Zacatecas. Se analizaron ochenta y cuatro especímenes de murciélagos de siete localidades dentro de Zacatecas. Los huéspedes fueron examinados para detectar helmintos parásitos siguiendo los procedimientos estándar de revisión, identificación taxonómica y se carcaterizaron las infecciones. El 65.47 % de los huéspedes examinados fueron parasitados. La fauna de helmintos consistió en cinco taxones: tres digéneos (Dicrocoelium rileyi, Ochoterenatrema labda, y Urotrema scabridum); un céstodo (Vampirolepis sp.) y un nemátodo (Tadaridanema delicatus). Se presenta una breve descripción morfológica de Urotrema scabridum. D. rileyi es la especie de helminto más prevalente y abundante. El intestino es el hábitat más parasitado con cuatro especies. El ciclo de vida indirecto es predominante y está relacionado con los hábitos alimentarios insectívoros de este huésped. Es necesario aumentar el número de estudios sobre este sistema huésped-parásito para contribuir al monitoreo de las poblaciones y la conservación, así como realizar estudios sobre patrones biogeográficos de helmintos parásitos de murciélagos que permitan explorar su origen y evolución en la región. U. scabridum se reporta por primera vez de Zacatecas, México. Todas las especies son registros nuevos de localidad.

Key words: Cestoda; Helminth parasites; Mexican free-tailed bat; Mexican Plateau; Nematoda; Trematoda.

© 2020 Asociación Mexicana de Mastozoología, www.mastozoologiamexicana.org

Introduction

Chiroptera is the second most diverse and abundant order of mammals, it is widely distributed worldwide and is most abundant in tropical regions (Hutson et al. 2001). The Mexican free-tailed bat, Tadarida brasiliensis (Molossidae), is abundant in the Western Hemisphere, from the United States of America and southward into Central and South America (Russell et al. 2005). Its distribution range encompasses most of Mexico, except for most of the Yucatan peninsula (Wilkins 1989; Schmidly 1991; Álvarez-Castañeda et al. 2015). This bat species comprises nine valid subspecies (Simmons 2005), one of them is T. b. mexicana. This insectivorous species may occupy different habitats, including urban zones, deserts, and pine-oak forests, where it can often be found in caves, under bridges, abandoned mines, tunnels, tree holes and wall cracks (Tuttle 1994).

Although the Mexican free-tailed bat is a widely distributed species, its helminth fauna has been seldom studied in Mexico (reported in all cases as T. brasiliensis); studies have been carried out in Mexico City and the states of Mexico, Durango, Morelos, Nuevo Leon, Puebla, and Zacatecas (Tuttle 1994, 1942, 1943; Caballero y Caballero and Caballero-Rodríguez 1969; Guzmán-Cornejo et al. 2003; Falcón-Ordaz et al. 2006; García-Prieto et al. 2012; Caspeta-Mandujano et al. 2017; Jiménez et al. 2017; Falcón-Ordaz et al. 2019; Table 1). Sixteen helminth taxa have been recorded parasitizing this bat species in Mexico (Table 1): nine trematodes, two cestodes, four nematodes, and two nematodes. To the best of our knowledge, only four helminth species had been previously recorded in Zacatecas: three platyhelminth species [two digeneans (D. rileyi and O. labda) and one cestode (Vampirolepsis sp.), and one nematode species (T. delicatus).

As part of a research program aimed to compile an inventory of invertebrate parasites of wildlife in Northern-Central Mexico, with emphasis in the Mexican Plateau, the helminth fauna of T. brasiliensis mexicana was studied. The trematode species Urotrema scabridum was recorded for the first time. The aim of this paper is to report on the presence of this trematode in Mexico and expand the known distribution range of the helminth parasite fauna of T. b. mexicana.

Material and Methods

Eighty-four bat specimens were collected from seven localities in the State of Zacatecas between November 2011 and September 2013 (Table 2, Figure 1). The specimens were euthanized with an intraperitoneal overdose of sodic pentobarbital, following the guidelines of the American Society of Mammologists (Sikes et al. 2016; scientific collecting license FAUT-268 to EAMS), and examined for the presence of helminth parasites. The body cavity was exposed by means of a longitudinal incision; all the organs were removed and examined separately under a dissecting stereoscope. Parasites found were first placed in a 0.85 % w/v saline solution, then fixed by sudden immersion in hot (steaming) 70 % ethanol and stored in 70 % ethanol to preserve morphological traits for identification. Nematodes were cleared for morphological study with Ammans’s lactophenol and with a 2:8 ethanol–glycerin mixture. Cestodes were stained with Mayer’s hydrochloric carmine, and whole-mounted in Canada balsam (Hycel de México, Jalisco). Techniques used are fully described elsewhere (Lamothe-Argumedo 1997).

Some of the specimens were photographed with a Leica ICC50HD camera fitted to a Leica DM750 microscope (Leica Microsystems, Wetzlar, Germany). For the new record specimens, morphometric characteristics were measured in micrometers (µm) unless otherwise stated (total body length and width in millimeters, mm). Minimum and maximum values are reported, along with the mean and standard deviation (SD) in parentheses.

Two specimens of the species newly recorded in Zacatecas and one of the dicrocoeliid species were further examined with scanning electron microscopy (SEM) and environmental scanning electron microscope (ESEM), respectively. The former were stored in 4 % formalin, dehydrated through a series of baths of gradually increasing ethanol concentrations, and critical-point dried. Specimens were coated with a gold–palladium mixture and examined under a Hitachi S-2460N (Hitachi, Tokyo, Japan) SEM at 15 kV. The second specimen was observed directly under an ESEM Quanta 250 FEG (Thermo Fisher Scientific Inc., Brno, Czech Republic) operating in low vacuum mode (p between 100 and 130 Pa).

Taxonomic identification was carried out by examining morphological traits and comparing them with taxonomic keys and descriptions in the specialized literature (Macy 1931;Macy 1931 Caballero y Caballero 1942, 1943; Travassos 1944; Bray et al. 1999; Anderson 2000; Lunaschi 2002; Falcón-Ordaz et al. 2006; Lunaschi and Notarnicola 2010). Helminth parasites were identified, counted and their sites of infection recorded. Infection parameters of prevalence (P), mean abundance (MA), mean intensity (MI) and intensity range (IR), were calculated according to Bush et al. (1997; Table 3).

Voucher specimens were deposited into the reference collection of the Colección de Invertebrados no Artrópodos (CINZ) and Colección de Vertebrados (CVZM), Laboratorio de Colecciones Biológicas y Sistemática Molecular, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas. Additional vouchers specimens were entered into the Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico.

Results

Eighty-four bat specimens were collected from seven localities in the State of Zacatecas and examined for the presence of parasites; 65.47 % of the specimens were parasitized. The helminth fauna comprises five species in five different families (Figure 2, 3) the first group, Platyhelminthes, the trematodes Dicrocoelium rileyi (Dicrocoeliidae), Ochoterenatrema labda (Lecithodendriidae), and Urotrema scabridum (Pleurogenidae), and one cestode, Vampirolepis sp. (Hymenolepididae; the second group, Nematoda, Tadaridanema delicatus (Molineidae). Most of the helminth parasites had been previously recorded in Zacatecas, except for the trematode Urotrema scabridum (Table 1; Figure 2) which inhabits the gall bladder and hepatic conduits. A brief morphological description follows.

Class Trematoda

Orden Strigeidida

Family Pleurogenidae (Syn. Urotrematidae Ponche, 1926 according to Tkach et al. 2019).

Urotrema scabridum

Characterization (based on 14 specimens, 12 measured and 2 SEM, Figure 2 and Table 4): body elongated, posterior end truncated, yellow color in vivo and whitish post fixing, total body length (TBL) 2.012 - 3.580 mm (2.944 ± 0.498) by 0.339 - 0.497 mm (0.433 ± 0.049) wide (W). Tegument covered with small spines (a SEM microphotograph shows collapse of the tegument and spines shape). Oral sucker subterminal, 78 - 132 (109 ± 18) long (OSL) by 75 - 146 (119 ± 24) wide (OSW). Ratio of oral sucker width to ventral sucker width 1:1.21 - 1.49. Pre-pharynx short. Pharynx 33 - 58 (49 ± 8) long by 37 - 61 (51 ± ٨) wide. Esophagus 176 - 397 (230 ± 60) long by 17 - 29 (23 ± 4) wide. Ventral sucker on the first third of the body, 107 - 178 (143 ± 21) long (VSL) by 112 - 178 (144 ± 19) wide (VSW). Intestine bifurcation pre-acetabular and narrow, extending to the posterior region of the body to the posterior testis. Ovary intercecal, anterior to testes, 115 - 210 (155 ± 29) long (OL) by 127 - 184 (153 ± 21) wide (OW). Testes tandem; anterior testis 181-334 (247 ± 41) long (ATL) by 160 - 390 (262 ± 60) wide (ATW), posterior testis 207 - 332 (265 ± 41) long (PTL) by 156 - 339 (253 ± 53) wide (PTW). Cirrus sac fusiform, located in the posterior end of the body, 164 - 291 (221 ± 40) long. Genital pore ventral. Vitelline follicles in two lateral fields wrapped around the ceca, both extracecal, several clusters of vitelline glands dorsally situated between ventral sucker and ovary, extending anteriorly to ventral sucker from the anterior testis. Uterus mainly intercecal, the uterine loops descending to posterior end of the body. Eggs 18 - 24 (24 ± 2, n = 60) long (EL) by 10 - 12 (11 ± 1, n = 60) wide (EW).

Taxonomic remarks: The genus Urotrema was first described from specimens collected in the intestine of the greater bulldog bat Noctilio leporinus (originally recorded as Noctilio macropus) and included in Urotrema scabridum as the type species. This species mainly parasitizes insectivorous bats and is widely distributed from North to South America and Africa (Zamparo et al. 2005). It has also been reported in polychrotid lizards (anoles) from Florida and Louisiana (Sellers and Graham 1987; Goldberg et al. 1994), the Caribbean and Central America (Goldberg et al. 1994, Goldberg et al. 1996; Goldberg et al. 1998).

Through the taxonomic history of the genus Urotrema, eight nominal species have been described parasitizing various mammal and lizard species (Zamparo et al. 2005): U. scabridum, U. shillingeri, U. lasiurensis, U. minuta, U. wardi, U. aelleni Baer, 1957, U. macrotestis, and U. shirleyae. However, the validity of some of the species has been questioned (Caballero y Caballero 1942; Caballero and Grocott 1960; Yamaguti 1971; Bray et al. 1999; Tkach et al. 2019). Caballero y Caballero (1942) considered U. scabridum and U. wardi as valid species, and synonymized U. lasiurensis, U. minuta and U. shillingeri. Later on, Caballero and Grocott (1960) synonymized U. aelleni with U. scabridum. Bray et al. (1999) suggested that U. scabridum is a species complex showing intraspecific variation (= U. aelleni, U. lasiurensis, U. macrotestis, and U. shillingeri). At least three species are currently considered valid: “U. scabridum complex”, U. minuta and U. shirleyae. Recently, the phylogenetic position of the genus Urotrema within Digenea was clarified by Tkach et al. (2019) based on the partial sequence of 28S rDNA; they transferred the genus to the Pleurogenidae and showed that the clade of U. scabridum + U minuta + U. shirleyae is phylogenetically closest to Parabascus spp. Our specimens are smaller than those described by Caballero y Caballero (1942) but bigger than the specimens measured by Lunaschi and Notarnicola (2010). Morphological characteristics of the specimens analyzed are shown in Table 4.

Infection parameters: The prevalence, mean abundance, mean intensity, intensity range, site of infection, hosts and localities are shown in Table 3. No helminth parasites were found in the San José de la Parada (Sombrerete) and Susticacán Dam (Susticacán) localities. Platyhelminthes (Trematoda) were the species-richest group. Four of the five helminth taxa inhabit the intestine (O. labda, U. scabridum, Vampirolepis sp. and T. delicatus), with a general intensity from 1 to 101 helminths per infected free-tailed bat. The highest number of parasite species was recorded in the Guadalupe locality, with four helminth species, three trematodes (D. rileyi, O. labda, and U. scabridum), one cestode (Vampirolepis sp.) and one nematode (T. delicatus). Indirect life cycles are predominant in the helminth fauna found. Dricocoelium rileyi was the most prevalent helminth in four localities (Table 3): Guadalupe (42.86 %), Nuevo Mercurio (33.33 %), Sombrerete (57.14 %), and Tepechtitlán (44.44%). Tadaridanema delicatus was the only parasite found in the Zacatecas locality, with 100 % prevalence in three individuals examined. The species D. rileyi and T. delicatus from Nuevo Mercurio showed the same prevalence, mean intensity, and intensity range (Table 3).

Discussion

The helminth fauna of the order Chiroptera in Mexico, has been poorly studied compared to the diversity of Mexican bats (144 spp.; helminths: e. g. García-Prieto et al. 2012; Caspeta-Mandujano et al. 2017; Clarke-Crespo et al. 2017; Jiménez et al. 2017; Salinas-Ramos et al. 2017; Luviano-Hernández et al. 2018; Falcón-Ordaz et al. 2019; bats: Sánchez-Cordero et al. 2014). To the best of our knowledge, only 28 bats species in the families Emballonuridae (one species), Molossidae (two species), Mormoopidae (four species), Natalidae (one species), Phyllostomidae (15 species) and Vespertilionidae (five species) have been examined for helminths (see García-Prieto et al. 2012; Clarke-Crespo et al. 2017; Caspeta-Mandujano et al. 2017; Jiménez et al. 2017; Salinas-Ramos et al. 2017; Luviano-Hernández et al. 2018; Falcón-Ordaz et al. 2019), only 19.44 % of the bat species occurring in Mexico. Mexican insectivorous bats are one of the groups bearing the highest diversity of parasitic helminths. The species bearing the highest richness is the ghost-face bat, Mormoops megalophylla, with 23 helminth species; followed by the Davy´s naked-backed bat, Pteronotus davyi, with 15 helminth species; the Mexican greater funnel-eared bat, Natalus stramineus, with 14 species; and the Mexican free-tailed bat, T. brasiliensis with 17 species (Guzmán-Cornejo et al. 2003; Falcón-Ordaz et al. 2006; García-Prieto et al. 2012; Caspeta-Mandujano et al. 2017; Jiménez et al. 2017; Table 1).

Previous studies had reported four species parasitizing the Mexican free-tailed bat in Concepción del Oro, Zacatecas: Two digeneans (D. rileyi and O. labda), one cestode (Vampirolepsis sp.) and one nematode (T. delicatus) (Guzmán-Cornejo et al. 2003; Falcón-Ordaz et al. 2006). The trematodes were recovered in their adult form; this is the group with the highest number of species parasitizing T. brasiliensis mexicana from Zacatecas, compared to cestodes and nematodes which together account for 40 % of the species diversity.

The trematode D. rileyi was the most important helminth in terms of infection parameters, showing the highest prevalence, mean abundance, mean intensity and intensity range in five localities: Tepechitlán (examined in October 2012, not found in May 2011; Medina-Rodríguez pers. obs.), Guadalupe (Zacatecas, October 2011, May and June 2012), Sombrerete (August 2012), San Felipe Nuevo Mercurio (Mazapil, April 2012; see Table 3; Martínez-Salazar, Pers. Obs.). In addition, Guzmán-Cornejo et al. (2003) also reported infections by this species in Concepción del Oro, Zacatecas (n = 3 of the 28 hosts examined in October 1997 and April 1988).

Although the life cycles of the majority of the helminth fauna of bats are still unknown, we can infer some information from their occurrence and their host species; most of the information available in the literature is for the supra-specific level (Yamaguti 1975; Schmidt 1986; Olsen 1986; Anderson 2000). The life cycle of D. rileyi is completely unknown; however, the life cycle of Dicrocoelium dendriticum has been described as infecting wild and domestic mammals (typically ruminants, not reported in bats) and, very occasionally, humans; its intermediate hosts are terrestrial snails (i.e. Zebrina sp., and Cionella sp.) and ants (i.e. Formica sp.). Pojmańska (2008) suggests that, in general, the Dicrocoeliid-type life cycle involves two intermediate hosts (a terrestrial snail and an arthropod): The xiphidiocercaria leaves the first intermediate host (snail) and becomes encysted in the second intermediate host (an arthropod), which is finally ingested by the definitive host. In Mexico, D. rileyi exclusively parasitizes T. brasiliensis as definitive host (Caballero y Caballero-Rodríguez 1969; Guzmán-Cornejo et al. 2003; García-Prieto et al. 2012; Jiménez et al. 2017; Falcón-Ordaz et al. 2019), but it has also been reported in T. brasiliensis cyanocephala and Vespertilio humeralis from the United States (Macy 1931). There are published reports on the presence of D. rileyi in four species of terrestrial snails from Zacatecas (Naranjo-García 2014) including Holospira (Holospira) temeroso and Humboldtiana (Humboldtiana) chrysogona in Concepción del Oro; Humboldtiana (Humboldtiana) bicincta in Sierra de Mascarón, Mazapil; and Humboldtiana (Humboldtiana) tescola in San Tiburcio, Mazapil (Thompson 2011). The presence of D. rileyi in these five localities in Zacatecas suggests that its intermediate host on which the Mexican free-tailed bat feeds could be present at least from May to October. It is necessary to further examine the genera Holospira and Humboldtiana in Concepción del Oro; as well as Humboldtiana in Mazapil to confirm their role as intermediate hosts of this trematode species in Zacatecas. On the other hand, some 14 Formicidae species have been recorded in Zacatecas (Vásquez-Bolaños 2011) but their helminth fauna has not yet been examined as a possible intermediate host. Further studies on the diversity of terrestrial snails and arthropods (ants) in Guadalupe, Mazapil, Sombrerete and Tepechitlán would help to understand the life cycle of D. rileyi in Zacatecas, as well as those of other helminth parasites of wild vertebrates.

Ochoterenatrema labda is an intestinal parasite that has bats as the only known definitive host; it parasitizes bats from United States, Mexico, Panama, Chile and Argentina. Originally described from T. brasiliensis from Bosque de Chapultepec, Mexico City and Natalus stramineus from Tlalpan, Mexico City (Caballero y Caballero 1943; Caballero y Caballero 1964; Cain 1966; Guzmán-Cornejo et al. 2003; Lunaschi and Notarnicola 2010; García-Prieto et al. 2012; Jiménez et al. 2017), it is the only species that has been reported parasitizing several bat species in Mexico (Balantiopteryx plicata, Mormoops megalophylla, Myotis velifer, Natalus mexicanus, Pteronotus davyi, and T. brasiliensis; García-Prieto et al. 2012; Caspeta-Mandujano et al. 2017; Jiménez et al. 2017). Guzmán-Cornejo et al. (2003) reported this species of digenetic trematode as the most prevalent and abundant helminth in T. brasiliensis from Concepción del Oro, Zacatecas. By contrast, our data showed D. rileyi as the species with highest infection parameters (Table 3). The taxonomic status of this genus has been questioned; Yamaguti (1958) suggested that it is a synonym of Prosthodendrium. However, Cain (1966) and later Yamaguti (1971) considered the genus as valid. Lunashi (2002) provided a redescription of O. labda and considered both genera as valid, as Ochoterenatrema can be distinguished mainly by the presence of a pseudogonotyl to the left of the ventral sucker. A taxonomic revision of this genus was published by Tkach et al. (2003), but a molecular analysis of Ochoterenatrema and Prosthodendrium is necessary to clarify this issue. The life cycle of this intestinal trematode has not been elucidated and little is known of its intermediate hosts; however, the family Lecithodendriidae requires three hosts: a mollusk, an arthropod, and a vertebrate (Bray et al. 2008; Lord et al. 2012). In general, the xiphidiocercaria (the first developmental stage) occurs in prosobranch mollusks; larvae of aquatic insects are the intermediate hosts for metacercariae (encysted stage; Yamaguti 1971); chiropterans become infected when they consume infected adult insects, and the adult parasite develops (Lord et al. 2012).

In our study we found the trematode U. scabridum, which had not been previously recorded in Zacatecas, even though this species ranges from North America to South America (Font and Lotz 2008). To the best of our knowledge, only one species of the genus Urotrema has been reported parasitizing Mexican bats: U. scabridum. This is a parasite of the Mexican free-tailed bat, and has been recorded in several localities in Mexico, including Acolman, State of Mexico; Cueva de la Boca (Santiago) and Cueva San Bartolo (Santa Catarina), Nuevo León; Nombre de Dios, Durango; and Río Salado (Zapotitlán), Puebla (Caballero y Caballero 1942; García-Prieto et al. 2002; Guzmán-Cornejo et al. 2003), and an unspecified locality in the State of Morelos (Caspeta-Mandujano et al. 2017). It has also been found in N. stramineus from Tlalpan, Mexico City (Caballero y Caballero 1942). This is the first time this species has been recorded in the State of Zacatecas; the nearest locality where this species had been previously recorded is in the State of Nuevo León (Guzmán-Cornejo et al. 2003). A study on the morphological and molecular variation of this species throughout its distribution range would help to confirm whether or not this is a species complex, as its taxonomic history suggests (e. g., Caballero y Caballero 1942; Caballero and Grocott 1960; Bray et al. 1999; Table 4). Life cycles and larval morphology of the Urotrematidae are still completely unknown. Bats acquire this urotrematid parasite by ingesting insects that act as intermediate hosts and harbor encysted metacercariae (Bray et al. 2008).

The taxonomic history of the genera Vampirolepis and Rodentolepis has been controversial. Both genera parasitize chiropterans and share several morphological characteristics, particularly in their body structure. However, the distinguishing difference between these two genera is the number of ovaries, two in Rodentolepis and one in Vampirolepis (Khalil et al. 1994), a characteristic that we confirmed in our study. We were not able to identify all of our specimens to the species level because some of them could not be mounted adequately for morphological study. Nevertheless, we were able to observe some diagnostic characteristics (e. g., presence of an armed rosette endowed with 32 hooks; Medina-Rodríguez, pers. obs.) that allowed identification at the genus level as Vampirolepis sp. Distinctive features of this genus include between 18 and 50 hooks; linear disposition of the testicles, divided into two groups by the ovary; and transversely elongated proglottids. Only V. decipiens has been reported parasitizing T. brasiliensis in Mexico (García-Prieto et al. 2012); collecting more specimens of Vampirolepis would help to clarify the identity of the species present in Zacatecas. Hymenolepididae generally exhibit an indirect life cycle (insects are the intermediate host that is ingested by the vertebrate host) and parasitize insectivorous bats (Bray et al. 2008; Roberts and Janovy 2009).

Tadaridanema delicatus is widely distributed across North and South America (Falcón-Ordaz et al. 2006; Cheuiche et al. 2015); in the State of Zacatecas it is the species with the widest known geographic distribution, having been recorded in six localities (Table 2, Figure 1): Tepechitlán (Tepechitlán), Guadalupe (Zacatecas), Zacatecas (Zacatecas), Sombrerete (Sombrerete), and San Felipe Nuevo Mercurio (Mazapil); it was also previously reported from Concepción del Oro, Zacatecas by Guzmán-Cornejo et al. (2003) and Falcón-Ordaz et al. (2006). It occurs in simpatry with D. rileyi in four localities (Table 2, 3), with exception of Zacatecas (Zacatecas), where we examined only one bat and found three individuals of T. delicatus. Additionally, T. delicatus has been recorded parasitizing T. brasiliensis mexicana from the States of Durango, Nuevo León, and Puebla (Falcón-Ordaz et al. 2006), as well as Molossus ater from the State of Sinaloa (unspecified locality; Cain and Studier 1974).

The life cycle of Tadaridanema spp. is unknown. However, it has been suggested that members of the family Molineidae have a direct life cycle in which the females release numerous eggs into the intestine of the vertebrate definitive host. The eggs are afterwards released to the external medium through the feces, where the first-stage starts developing; later on, they develop into infective third-stage larvae (Roberts and Janovy 2009). It has also been suggested that Molineidae can utilize insects as paratenic hosts (Bush et al. 2001), which could increase the possibility of bats being parasitized by nematodes. However, this hypothesis must be tested in T. delicatus.

The parasites’ infection mechanism can be related to the host’s life style and habitat use (Kunz et al. 1995; McWilliams 2005). This bat species lives in colonies numbering up to millions of individuals (McCracken et al. 1994); this favours infection through their grooming habits and the accumulation of guano in humid environments that harbour a unique ecosystem, including parasites and hosts (Kerth 2008; Altringham 2011). That bats usually host only one parasite taxon is to be expected since some bats are dietary specialists. Parasites are obtained from what bats eat and, being dietary specialists, bats may be predisposed to become parasitized only by the helminth that uses its prey items as intermediate host. Although many species of insectivorous bats have a diversified diet including insects from different orders and families, some species selectively feed on only one type of prey and show foraging habitat specificity. Thus, mayfly and beetle specialists such as Myotis lucifugus, and moth specialists such as Lasiurus borealis and T. brasiliensis are less likely to have multi-parasitism than species showing generalist feeding habits (Hilton and Best 2000). These bats roost in a variety of places, including caves, rock crevices, bridges, culverts, highway overpasses and other structures in urban areas (Scales and Wilkins 2007). Infection of insectivorous bats by indirect life cycle parasites occurs outside urban areas as insects are attracted by the city lights (Rydell 2006), and bats prey on them. On the other hand, when bats return to overnight in the colony, the high humidity and feces accumulation in the place, together with the bats’ self-cleaning or cleaning between colony members habits, allow the bats to acquire direct life cycle parasites either by autoinfection, by contact between the colony members or by the site’s humidity that favours the development of direct life cycle helminths (Bray et al. 2008; Bush et al. 2001; Roberts and Janovy 2009; Lord et al. 2012).

No easily discernable pattern could be found in the diversity of helminths recorded in this bat species in urban areas (localities as Tepechitán, Guadalupe, Zacatecas or Sombrerete) versus those recorded in natural environments (as San Felipe Nuevo Mercurio). Five helminth species were recorded in Guadalupe, four in Sombrerete and three in San Felipe Nuevo Mercurio, and most of them were Platyhelminthes (indirect life cycle). These results might be related to the asymmetric sampling effort (Table 2, 3).

Trematodes showed the highest species richness, and some six helminth species have been reported parasitizing T. brasiliensis in Mexico. This pattern had been previously observed in insectivorous bats in North America (Table 1): D. rileyi, P. beltrani, O. labda, P. vespertilionis, and U. scabridum (Guzmán-Cornejo et al. 2003; in García-Prieto et al. 2012; Jiménez et al. 2017). Two of these indirect life cycle species, D. rileyi and O. labda, and the nematode T. delicatus (considered as a direct life cycle parasite) have been reported as typical helminth fauna of T. brasiliensis in Zacatecas and occur in sympatry in the localities of Guadalupe, Sombrerete and San Felipe Nuevo Mercurio. These species had been previously reported in the same condition in Nuevo León and Puebla (Table 1; Guzmán-Cornejo et al. 2003).

Tadarida brasiliensis is an opportunistic, generalist, insectivorous bat species (Kunz et al. 1995). Food items forming its diet have been generally identified to the order level and, in some cases, to the family level. This bat mainly consumes insects in the orders Lepidoptera (moths), Coleoptera (beetles) and, occasionally, Diptera (true flies), Hemiptera (stinkbugs), Homoptera (leafhoppers), Hymenoptera (wasps), Neuroptera (lacewings) and Odonata (dragon flies, damselflies; Fabián et al. 1990; Kunz et al. 1995; Whitaker et al. 1996; McWilliams 2005; Armstrong 2008). In the United States and Brazil, Coleoptera and Lepidoptera are consumed with higher frequency and volume during the summertime (Fabián et al. 1990; McWilliams 2005). Studies on the bat’s diet and monitoring the populations in those localities could help to elucidate the indirect life cycles of the helminth fauna of the Mexican free-tailed bat.

The diversity of invertebrates in Zacatecas is almost unknown; studies on the diversity of terrestrial snails and arthropods are necessary to better understand parasite life cycles in wild vertebrates. Monitoring wildlife and their parasites is crucial for conservation and for understanding biogeographic patterns and the evolution of host-parasite interactions. It is, therefore, necessary to further study the helminth parasites of bats to explore their origin and evolution in this region. In this paper, we present the first record of U. scabridum in Zacatecas and new locality records for all the helminth taxa recorded.

Acknowledgements

We thank C. Raudales, V. Flores, L. Landeros, B. Velázquez, E. Esparza, O. Romo, J. González, M. Bravo, and C. Vázquez for their assistance with fieldwork. We also thank E. Sánchez, S. Trejo, and A. Olmedo for their assistance in the laboratory. We thank the communities that graciously donated biological material. We are grateful to B. Mendoza-Garfias for her assistance processing samples for SEM photography at the Laboratorio de Microscopía Electrónica y Fotografía de la Biodiversidad, Instituto de Biología, UNAM; and to G. J. Labrada Delgado who helped with the specimens characterization. We thank the Nanoscience and Nanotechnology Research National Laboratory (LINAN) at IPICyT, for granting access to their facilities for ESEM photographs. We thank J. A. Fernández and the anonymous reviewers for their suggestions to the manuscript. E. A. Martínez-Salazar was partially supported by Conacyt grant FOMIX-ZAC-2011-01-C01-170798, and by PRODEP-SEP’s program “Apoyo a la incorporación de nuevos PTC’’ (UAZ-PTC-169). These results are part of the projects UAZ-2016-37096 (E. A. Martínez-Salazar was the project principal investigator) and UAZ-2016-37097 (R. Rosas-Valdez was the project principal investigator).

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Associated editor: Jesús Fernández

Submitted: March 26, 2019; Reviewed: April 8, 2019;

Accepted: January 22, 2020; Published on line: March 18, 2020.

Table 1. Summary of helminth fauna of Tadarida brasiliensis in Mexico. G = gall bladder and hepatic conduits; I = Intestine; S = Stomach.

Helminths

Locality/State

Reference

Platyhelminthes

Trematoda

Dicrocoeliidae

Dicrocoelium sp.G

Cueva San Bartolo (Santa Catarina), Nuevo León.

García-Prieto et al. 2002

Dicrocoelium rileyi G

Campus Chamilpa (UAEM), Morelos; Concepción del Oro, Zacatecas; Cueva de La Boca (Santiago), Nuevo León; Cueva del Guano (Santa Catarina), Nuevo León; Cueva San Bartolo (Santa Catarina), Nuevo León; Nombre de Dios, Durango; Río Salado (Zapotitlán), Puebla; Tequixquiac, State of Mexico.

Caballero y Caballero, and Caballero-Rodríguez 1969; García-Prieto et al. 2002; Guzmán-Cornejo et al. 2003; Caspeta-Mandujano et al. 2017; Falcón-Órdaz et al. 2019

Platynosomum beltrani I

Monterrey, Nuevo León.

Caballero y Caballero and Caballero-Rodríguez 1969

Lecithodendriidae

Limatulum limatulum I

Campus Chamilpa (UAEM), Morelos; Cuicatlán, Morelos.

Caballero y Caballero and Bravo 1950; Caspeta-Mandujano et al. 2017

Limatulum oklahomense I

Zoológico de Chapultepec, México City.

García-Prieto et al. 2012

Ochoterenatrema labda I

Bosque de Chapultepec, México City; Concepción del Oro, Zacatecas; Cueva de La Boca (Santiago), Nuevo León; Cueva San Bartolo (Santa Catarina), Nuevo León; Nombre de Dios, Durango; Río Salado (Zapotitlán), Puebla; State of México; Campus Chamilpa Campus Chamilpa (UAEM), Morelos.

Caballero y Caballero 1940; Caballero y Caballero 1943; García-Prieto et al. 2002; Guzmán-Cornejo et al. 2003; Caspeta-Mandujano et al. 2017

Paralecithodendrium naviculum I

Azcapotzalco, México City.

Caballero y Caballero, 1940

Plagiorchiidae

Plagiorchis vespertilionis I

Azcapotzalco, México City; Bosque de Chapultepec, México City; Locality unknown, Morelos.

Caballero y Caballero 1940; Caballero y Caballero 1943; Caspeta-Mandujano et al. 2017

Pleurogenidae

Urotrema scabridum I

Acolman, State of México; Cueva de La Boca (Santiago), Nuevo León; Cueva San Bartolo (Santa Catarina), Nuevo León; Nombre de Dios, Durango; Río Salado (Zapotitlán), Puebla; Locality unknown, Morelos.

Caballero y Caballero 1942; García-Prieto et al. 2002; Guzmán-Cornejo et al. 2003; Caspeta-Mandujano et al. 2017

Cestoda

Vampirolepis decipiens I

Campus Chamilpa (UAEM), Morelos.

Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Vampirolepsis sp.I

Concepción del Oro, Zacatecas; Cueva de La Boca (Santiago), Nuevo León; Río Salado (Zapotitlán), Puebla.

Guzmán-Cornejo et al. 2003

Nematoda

Acuaridae

Acuaridae gen. sp.S

Campus Chamilpa (UAEM), Morelos.

Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Capillaridae

Aonchotheca speciosa S

Campus Chamilpa (UAEM), Morelos.

Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Capillaria palmata S

Campus Chamilpa (UAEM), Morelos.

Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Ornithostrongylidae

Allintoshius tadaridae I

Alcoman, State of México; Bosque de Chapultepec, México City; Cueva El Salitre, Morelos.

Caballero y Caballero 1942; Caspeta-Mandujano et al. 2017

Molineidae

Tadaridanema delicatus I

Campus Chamilpa (UAEM), Morelos; Concepción del Oro, Zacatecas; Cueva de La Boca (Santiago), Nuevo León; Nombre de Dios, Durango; Río Salado (Zapotitlán), Puebla

Guzmán-Cornejo et al. 2003; Falcón-Ordaz et al. 2006; data in Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Nematoda gen. sp.I

Campus Chamilpa (UAEM), Morelos.

Jiménez et al. 2017; Caspeta-Mandujano et al. 2017

Table 2. Localities surveyed in Zacatecas, Mexico for helminth parasites. Locality codes are used in Figure 1 and Table 3.

Code

Locality, municipality

Geographic coordinates (elevation)

Sample size (number of host infected)

Collection date (month/year)

1

Tepechitlán, Tepechitlán

21° 40’ 13.4” N; -103° 19’ 42” W (1,788 masl)

n = 18 (8)

5/2012

10/2012

2

Guadalupe, Zacatecas

22° 44’ 38.1” N; -102° 30’ 53.6” W (2,479 masl)

n = 35 (27)

11/2011

05/2012

06/2012

3

Zacatecas, Zacatecas

22°46’28.63” N; -102° 32’ 39.66” W 2,379 masl)

n = 1 (1)

06/2013

4

Sombrerete, Sombrerete

23° 38’ 4.47” N; -103° 38’ 29.51” W (2,307 masl)

n = 7 (5)

08/2012

5

San José de la Parada, Sombrerete

23° 31’ 52.7” N; -103° 36’ 16.6” W (2,163 masl)

n = 1 (0)

08/2013

6

Susticacán Dam, Susticacán

22° 36’ 38.42” N; -103° 8’ 40.01” W (2,081 masl)

n = 1 (0)

09/2013

7

San Felipe Nuevo Mercurio, Mazapil

24° 13’ 35.08” N; -102° 9’ 16.48” W (1,731 masl)

n = 21 (12)

04/2012

Figure 1. Sampling localities in Zacatecas, Mexico. Municipalities: 1= Tepechitlán; 2 and 3 = Zacatecas; 4 and 5 = Sombrerete; 6 = Susticacán; 7= Nuevo Mercurio. *8 = Concepción del Oro. Previous records are shown in Table I. Codes for localities are shown in Table 2.

Table 3. Infection parameters of helminth parasites of the free-tailed bat, Tadarida brasiliensis mexicana in seven localities from Zacatecas, Mexico. L = Locality (codes as in Figure 1 and Table 2). Abbreviations: 1) Infection sites: I = Intestine, G = gall bladder and hepatic conduits. 2) Life cycle: CD = Direct, CI= Indirect. 3) Ecological parameters: n = Total number of parasites collected, HIP = Host infected by parasite, P (%) = Prevalence, MA = Mean abundance, MI = Mean intensity, IR = Intensity range. * = Accession numbers in the CINZ and CNHE collections.

Helminth species

L

n

P (%) (HIP)

MA

MI

IR

Accession Number*

Platyhelminthes:

Trematoda

Dicrocoeliidae

Dicrocoelium rileyiG, CI

1

60

44.44 (8)

3.33

7.50

1 - 23

CINZ158; CNHE 11103

2

95

42.86 (15)

2.71

6.33

1 - 40

CINZ150; CINZ155; CNHE 11104

4

85

57.14 (4)

12.14

21.25

2 - 48

CINZ09; CNHE 11105

7

101

33.33 (7)

4.81

14.43

1 - 52

CINZ 10; CNHE 11106

Lecithodendriidae

Ochoterenatrema labdaI, CI

2

22

11.43 (4)

0.63

5.50

1 -15

CINZ151; CINZ154; CNHE 11107

4

1

14.29 (1)

0.14

1

1

CINZ 11

7

3

4.76 (1)

0.14

3

3

CINZ 12

Pleurogenidae

Urotrema scabridumI, CI

2

40

11.43 (4)

1.14

10

4 - 27

CINZ156; CNHE 11108

Cestoda

Hymenolepididae

Vampirolepis sp.I, CI

2

6

14.29 (5)

0.17

1.20

1 - 2

CINZ148; CINZ153; CNHE 11109

4

1

14.29 (1)

0.14

1

1

CINZ 13

Nematoda

Molineidae

Tadaridanema delicatusI, CD

1

2

11.11 (2)

0.11

1

2

CINZ159

2

67

40.00 (27)

1.91

4.79

1 - 12

CINZ149; CINZ152; CINZ157 CNHE 11110

3

3

100 (1)

3.00

3

3

CINZ 14; CNHE 11111

4

9

28.57 (9)

1.29

4.50

3 - 6

CINZ 15; CNHE 11112

7

18

33.33 (7)

0.86

2.57

1 - 6

CINZ 16; CNHE 11113

Figure 2. General morphology and ESEM-SEM photomicrographs of Urotrema scabridum from Zacatecas, Mexico. Optical microscopy: a) Whole body, ventral view; b) Oral sucker, ventral view; c) Ventral sucker, ventral view; d) Ovary, vitelline follicles arranged in two lateral fields and anterior end of the uterus, ventral view; e) Testis in tandem, ventral view; f) Uterine loops with eggs between testes, ventral view; g) Cirrus sac located in the posterior end of the body, ventral view. ESEM: h) Whole body, ventral view; i) Oral sucker, ventral view; j) Ventral sucker, ventral view. SEM: k and l) Eggs, ventral view. Scale bars are shown in each microphotograph.

Table 4. Morphometric comparison of Urotrema scabridum with some previous records.

Characteristic1

Present work

Caballero y Caballero (1942)2

Caballero y Caballero and Grocott (1960)3

Lunaschi and Notarnicola (2010)4

Distribution

Mexico

Mexico

Panama

Argentina

TBL (mm)

2.01 - 3.58

4.53 - 5.29

2.08 - 2.30

1.70 - 2.50

OSL

78 - 132

102 - 143

91 - 137

133 - 142

OSW

75 - 146

123 - 163

108 - 125

123 - 142

VSL

107 - 178

175 - 245

121 - 125

128 - 144

VSW

112 - 1782

135 - 233

125 - 133

134 - 152

OL

115 - 210

208 - 237

166 - 175

154 - 218

OW

127 - 184

155 - 163

158 - 187

112 - 209

ATL

181 - 334

300 - 350

133 - 141

128 - 323

ATW

160 - 390

200

146 - 162

134 - 285

PTL

207 - 332

310 - 380

133 - 187

112 -351

PTW

156 - 339

200 - 220

154 - 183

122 - 323

EL

18 - 24

22 - 24

21

21 - 22

EW

10 - 12

12 - 14

12

10 - 13

1 Acronyms as listed in the description of U. scabridum in the main text.

2 Host: Natalus stramineus and T. brasiliensis.

3 Host: Phyllostomus hastatus panamensis Allen 1904

4 Hosts: Myotis levis; Molossops temminckii; Eumops bonariensis; and T. brasiliensis.

Figure 3. Helminth parasites of the free-tailed bat from Zacatecas, Mexico (excluding the new record). Platyhelminthes: Trematoda: a) Dicrocoelium rileyi, full body, ventral view; b) ESEM of Dicrocoelium rileyi, full body, ventral view; c) Ochoterenatrema labda, full body, ventral view. Cestoda: Vampirolepis sp.: d) Anterior end, ventral view; e) Immature proglottids, ventral view. Nematoda: Tadaridanema delicatus: f) Female anterior end, ventral view; g) Female posterior end, ventral view; h) Synlophe at midbody level, apical view; i) Male, posterior end, ventral view. Scale bars are shown in each microphotograph.

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THERYA es publicada por la Asociación Mexicana de Mastozoología A. C.  Se distribuye bajo una Licencia de Creative Commons Atribución-NoComercial-SinDerivar 4.0 Internacional.

DERECHOS DE AUTOR Y DERECHOS CONEXOS, THERYA es una publicación digital cuatrimestral editada por la Asociación Mexicana de Mastozoología A. C.  Hacienda Vista Hermosa 107, Colonia Villa Quietud, Coyoacan 04960.  Distrito Federal, México.  Telefono (612) 123-8486, www.mastozoologiamexicana.org.  Editor responsable: Dr. Sergio Ticul Álvarez Castañeda (therya@cibnor.mx).  Reservas de Derechos al Uso Exclusivo No. 04-2009-112812171700-102, ISSN: 2007-3364 ambos otorgados por el Instituto Nacional de Derechos de Autor.  Responsable de la última actualización de este número, Unidad de informática de la Asociación Mexicana de Mastozoología A. C.  Dr. Sergio Ticul Álvarez Castañeda.  Instituto Politécnico Nacional 195.  La Paz, Baja California Sur, C. P. 23096.  Tel 612 123 8486.