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Parasites and commensals of the shovel-headed treefrog Diaglena spatulata (Amphibia: Hylidae) in Western Mexico.

Treefrogs (family Hylidae) are the most specious family of anurans in Mexico with 96 described species (ParraOlea et al., 2014). The parasitic fauna of these frogs has been poorly studied by researchers, since complete surveys of helminths have been performed only for Agalychnis dacnicolor, Dendropsophus microcephalus, Pseudacris hypochondriaca, Smilisca cyanosticta, and Smilisca baudinii from northern and southeastern Mexico. These species harbor an important richness and abundance of nematodes and trematodes, with cestodes and acanthocephalans being uncommon (Guillen-Hernandez et al., 2000; Goldberg et al., 2001; Goldberg and Bursey, 2002; Goldberg et al., 2002; Martinez-Salazar et al., 2013).

Additionally, there are isolated records of helminths for other treefrogs: Anotheca spinosa, Dendropsophus ebraccatus, Diaglena spatulata, Ecnomiohyla miotympanum, Hyla eximia, Hyla plicata, Scinax staufferi, Trachycephalus typhonius, and Triprion petasatus (Walton, 1940; Martinez-Villarreal, 1969; Baker and Adamson, 1977; Guillen-Hernandez, 1992; Goldberg et al., 2003; Mata-Lopez et al., 2008; Martinez-Salazar et al., 2009; Velarde-Aguilar et al., 2015).

The shovel-headed treefrog, D. spatulata, is a large frog (snout-vent length: males to 87 mm, females to 101 mm) characterized by integumentary cranial co-ossification, a casqued head longer than broad, and moderately large terminal discs on the digits (Duellman, 2001). This species is endemic to Mexico, known from the Pacific coast from central Sinaloa to the Isthmus of Tehuantepec, Oaxaca. Individuals show important variation in dorsal coloration related to their geographical distribution, and inhabit lowland xerophytic matorral, xeric and thornscrub forest, tropical scrub forests, tropical deciduous forest, and riparian vegetation. Breeding activity is restricted to the rainy season (mainly June-October) as they use temporary ponds and streams formed by rainfall for breeding (Dixon and Heyer, 1968; Garcia and Ceballos, 1994; Duellman, 2001). Shovel-headed treefrogs are arboreal and usually nocturnal (Garcia and Ceballos, 1994), feeding mainly on crickets, grasshoppers, spiders, beetles, and larvae of butterflies (Ordoniez-Ifarraguerri, 2012). However, researchers have performed no specific studies on biological interactions or habitat use on this species. Because the parasites, commensals, and symbionts inhabiting a particular species provide important information on the habits of the host, such as diet and habitat use (Bolek and Coggins, 2000, 2001; Yoder and Coggins, 2007), the principal aim of this work is examining individuals of D. spatulata for the presence of parasites and other organisms to contribute to the knowledge of this anuran species.

MATERIALS AND METHODS--We collected a total of 21 adult shovel-headed treefrogs by hand during night surveys in Colima and Jalisco states, Western Mexico. In July 2008 we obtained 16 frogs from disturbed grassy areas in Colima: five individuals (including an amplectant pair) were collected from a temporary pond beside a road near Highway 98 between Minatitlan and Manzanillo (19[degrees]11'10"N, 104[degrees]11'16"W, elevation 438 m; Site 1), while the other 11 were collected from a pond with a breeding chorus next to a road beside Highway 54 near Ixtlahuacan (19[degrees]01'33" N, 103[degrees]47'36"W, elevation 238 m; Site 2). In July 2009 we collected five frogs (mean snout-vent length 87 mm [range = 80-92 mm]) on vegetation and in water from a breeding chorus in a temporary pond at a pristine tropical dry forest in the Chamela-Cuixmala Biosphere Reserve, Jalisco (19[degrees]30'02"N, 105[degrees]02'04"W, elevation 50 m).

We sacrificed all frogs by an overdose of sodium pentobarbital, and dissected and studied them for internal parasites and commensals using a stereomicroscope. We examined all tissues and organs including the oral cavity, eyes, body surface, muscle, lungs, stomach, intestine, gall bladder, liver, and urinary system. We counted in situ all organisms encountered, then fixed and preserved them using conventional techniques for subsequent taxonomic identification under light microscopy. We stained platyhelminthes (Cestoda) with Meyer's paracarmin, dehydrated through a graded ethanol series, cleared in methyl salicylate, and mounted in Canada balsam. We cleared Nematoda (Secernentea) and Annelida (Oligochaeta) with lactophenol or glycerol and mounted them on temporary slides (Lamothe-Argumedo, 1997; Govedich et al., 2010). We studied some specimens by scanning electron microscopy, for which we dehydrated them in ethanol series, dried them using the critical point technique, coated them with gold, and examined them with a Hitachi SU1510 scanning electron microscope (Hitachi High-Technologies Corporation, Tokyo, Japan). To identify parasites we consulted taxonomic keys and species descriptions (e.g., Bursey and Goldberg, 1994; Khalil et al., 1994; Pinder et al., 1998; Mata-Lopez et al., 2008; Gibbons, 2010).

We characterized the infections following Bush et al. (1997) and tested significant differences for the mean abundance and prevalence of helminths recorded in two or three study sites. We used nonparametric tests (Wilcoxon rank-sum statistic and Kruskal-Wallis test) for comparisons because data did not conform to normal distributions (Shapiro-Wilk tests). Analyses were performed using R version 3.0.3 (R Development Core Team, 2013).

We deposited voucher specimens of helminths and oligochaetes in the Coleccion Nacional de Helmintos, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Mexico City (accession numbers listed in Table 1). Some frogs from Colima were deposited in the Herpetological Collection at The University of Texas, Arlington, with the following accession numbers: UTA A 59781, 59782, 59785, 59795, 59796, 59798, 59805, and 59825. Frogs from Jalisco were not preserved as voucher specimens because the species was already well represented in the herpetological collection of Chamela Biological Station, Universidad Nacional Autonoma de Mexico.

RESULTS AND DISCUSSION--Fourteen of 16 frogs collected were positive for parasites or commensals in Colima, and all five individuals collected from Jalisco were positive. We recorded six taxa inhabiting internal organs of D. spatulata (Table 1) and found no significant differences in prevalence and abundance between studied sites, except for Parapharyngodon chamelensis. This nematode species exhibited higher infection levels in Jalisco than in Colima (prevalence: [chi square] = 12.05, df = 2, P = 0.0024; mean abundance: [chi square] = 7.22, df = 2, P = 0.03).

This work is one of the few studies on parasites and commensals of treefrogs from Western Mexico (e.g., Goldberg et al., 2001; Goldberg and Bursey, 2002; Mata-Lopez et al., 2008; Martinez-Salazar et al., 2013; VelardeAguilar et al., 2015). There are only three previous helminthological records for Diaglena spatulata: Cosmocercella diaglenae from three localities in Jalisco (Mata-Lopez et al., 2008); Parapharyngodon hylidae from Tepalcatepec-Jilotlan Road, Jalisco; and Parapharyngodon chamelensis from Chamela, Jalisco (Velarde-Aguilar et al., 2015). In the present study, we recorded C. diaglenae and Parapharyngodon chamelensis for the first time in Colima, while the plerocercoid of the family Proteocephalidae and the nematodes Aplectana and Physalopteroides bahamensis, as well as the oligochaete Dero (Allodero), represent new records for the shovel-headed treefrog. Additionally, we recorded Physalopteroides bahamensis and Dero (Allodero) for the first time in Mexico.

We found material assigned to Proteocephalidea in the plerocercoid stage, presenting a scolex with four simple suckers; both characteristics correspond to the order (Khalil et al., 1994). We did not assign it to a lower taxonomic level due to the incomplete development of many taxonomic characters at that larval stage. We identified oligochaetes from Dero (Allodero) by the presence of a fossa around the anus, ventral setae, and absence of dorsal setae (Pinder et al., 1998). We did not assign these specimens to a species due to the poor state of preservation of most of them. The characteristics we observed in male individuals of the nematodes of Aplectana did not match those exhibited by any of the described species in the genus and may represent a new species. The arrangement of postcloacal papillae that we observed in the males was partially similar to that in Aplectana itzocanensis and Aplectana incerta (Baker, 1985), but the number of precloacal papillae (six pairs) does not correspond to either of these species (which present eight pairs). In addition, our specimens presented spicules smaller than those reported for A. incerta. We have identified the physalopterins as Physalopteroides bahamensis because they presented all taxonomic characters of this species (see Bursey and Goldberg, 1994); nevertheless, their examination under scanning electron microscope revealed the presence of an interolateral labial tooth that was not mentioned in the original description of the species (made with light microscopy). We could not observe this feature under a light microscope, thus we suggest the need for a redescription based on observations under both kinds of microscopes. We identified specimens as Cosmercella diaglenae due to the number, structure, and position of plectanes in males; egg size in females; and host type (see Mata-Lopez et al., 2008). Finally, we identified Parapharyngodon chamelensis by the following characters in males: presence of equinate anterior cloacal lip, a protuberance in the posterior cloacal lip, and the caudal papillae pattern consisting of three pairs plus a single papilla (see Velarde-Aguilar et al., 2015).

The life cycles of most of the organisms found in D. spatulata have not been examined, but according to the known life cycles of proteocephalid cestodes, the infection may occur through the ingestion of aquatic intermediate hosts such as copepods (Scholz, 1999; Falavigna et al., 2003; de Chambrier et al., 2009). Members of Parapharyngodon are found in insectivorous reptiles and amphibians (Adamson, 1981) and species of this genus may have monoxenous life cycles with hosts getting infected by ingesting eggs that are sometimes deposited on plants through fecal pellets (Roca, 1999; Anderson, 2000; Carretero et al., 2006). The species C. diaglenae could have infected the treefrogs by two routes, since species in Cosmocercinae can produce thin-shelled eggs that larvate in utero or develop in the external environment into first-stage larvae (e.g., Cosmocercoides variabilis). Outside the host, eggs hatch and first-stage larvae develop and molt twice to the infective third stage. The final host becomes infected by ingestion of larvae (Aplectana courdieri) or by skin penetration (Cosmocerca commutate, Cosmocercoides variabilis', Anderson, 2000). The life cycle of Physalopteroides bahamensis is unknown, with species of Physalopterinae occurring rarely in amphibians (Anderson, 2000); some studies, however, indicate that physalopterines generally use insects as intermediate hosts (Goldberg and Bursey, 1989; Anderson, 2000). The development to third stage infective larvae of Thubunaea and Abbreviata caucasica, for example, has been reported to occur in beetles, cockroaches, crickets or grasshoppers (Basir, 1949; Poinar and Quentin, 1972; Velikanov, 1992).

The oligochaetes Dero are diagnosed by a fossa around the anus, which usually contains gill filaments. Three subgenera--Aulophorus, Dero, and Allodero--are usually recognized. The first two are very similar; both have ventral setae that are longer and thinner on anterior segments than on posterior ones, a full complement of dorsal setae, and well developed branchial fossa and gills. All species are free-living and differ from each other in that Dero lacks the pair of elongate palps found on the posterior border of the Aulophorus fossa. By contrast, Allodero is mostly endocommensal in frogs; all ventral setae are similar and the dorsal setae and branchial organs are often reduced or absent (Pinder et al., 1998). However, it is a matter of controversy if the oligochaetes Dero (Allodero) recorded in the ureters, Wolffian ducts, and bladder of anurans--including many treefrogs from tropical regions in the Americas, Africa, Asia, and Australia--are parasites, endocommensals, or symbionts (Harman, 1971, 1973; Harman and Lawler, 1975; Pinder et al., 1998). Commensalism seems to be the term that best explains the relationship between these groups of species (e.g., Harman, 1971; Govedich et al., 2010; Pinder, 2010), since there are no visible adverse effects on the organs of the frogs (Harman, 1971; Harman and Lawler, 1975; Pinder et al., 1998). In fact, the presence of an incomplete alimentary canal in commensal individuals suggests that the worms do not feed in the frog (Pinder et al., 1998).

We do not know the route through which the oligochaetes reach organs of the treefrogs. Goodchild (1951) suggested that the invasion of the ureters by oligochaetes probably occurs through the cloaca rather than through ingestion or penetration during the tadpole stage, whereas Pinder et al. (1998) indicate that frogs can be infected in water when they enter to breed, and Serramo-Lopez et al. (2005) describe a phoretic behavior by Dero (Allodero) superterrenus on the skin of treefrogs inhabiting tank bromeliads. In Chamela, Jalisco (one of our study sites), individuals of the terrestrial cane toad, Rhinella marina, were found to host Dero (Allodero) (M. G. Velarde-Aguilar, pers. observ.), which supports that infection occurs in water during amplexus, laying of eggs, or both, or on wet dirt, but not on trees or shrubs. Thus, more studies are required on the interaction between Dero (Allodero) and treefrogs to understand the mechanism of infection, determine the type of biological interaction, evaluate the advantages or disadvantages for the involved species, and understand the evolution of these interactions.

The parasitic fauna in terrestrial anurans can be dominated by species of nematodes with direct life cycles that infect the host by skin penetration (such as C. diaglenae), or by direct consumption of eggs (such as Parapharyngodon). In contrast, larval cestodes and larval and adult trematodes can be dominant in aquatic and semiaquatic frogs as these can prey more frequently on aquatic intermediate hosts such as crustaceans, molluscs, or insects in larval stages (Yoder and Coggins, 2007). The information available about life cycles of species of the genus Parapharyngodon (the most prevalent and abundant taxa in this study) and physalopterins confirms the insectivorous dietary habits of D. spatulata indicated by Ordouez-Ifarraguerri (2012). The importance of these taxa suggests that the frogs prey mainly on adult insects rather than on aquatic larvae. On the other hand, the presence of proteocephalid cestodes, Dero (Allodero), Aplectana, and C. diaglenae suggests that activity in and around temporary water bodies during the breeding season is also important to explain the composition and abundance of species found in the shovel-headed treefrog. Finally, the presence of C. diaglenae, Parapharyngodon chamelensis, and Dero (Allodero) in localities from both Colima and Jalisco (see Mata-Lopez et al., 2008; Velarde-Aguilar et al., 2015; present work) is notable given that conditions, resources, and levels of disturbance vary among these sites. Such consistency may reflect a constant composition of species inhabiting D. spatulata in a relatively wide geographical area.

We thank L. Garcia-Prieto for technical support, B. Mendoza Garfias for taking scanning electron microscope pictures of specimens, and D. Osorio-Sarabia for taxonomic advice. This paper was partially supported by the projects 54475 from Consejo Nacional de Ciencia y Tecnologia (CONACyT, Mexico), to VLR and DEB0102383 to J. Campbell (University of Texas). Specimens were collected under permit FAUT0056 from SEMARNAT to VLR. MGVA was awarded with a scholarship from the project CONABIO HB026. LGO and ECG thank the postdoctoral fellowship program from CONACyT for support during the writing of this paper.


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Submitted 17 March 2014.

Acceptance recommended by Associate Editor, Jesse M. Meik, 18 February 2015.


Laboratorio de Biologia Acuatica, Facultad de Biologia, Universidad Michoacana de San Nicolas de Hidalgo. Ciudad Universitaria, Morelia, Michoacan, Maxico (LGO)

Department of Wetland Ecology, Estacian Biolagica de Donana, CSIC. Avenida Amarico Vespucio, Seville, Spain (ECG)

Estacian de Biologia Chamela, Instituto de Biologia, Universidad Nacional Autanoma de Maxico. San Patricio, Jalisco, Maxico (MGVA, VLR)

* Correspondent:
TABLE 1--Parasites and commensals of the shovel-headed treefrog,
Diaglena spatulata, from Colima and Jalisco, Mexico. (a)

Parasite/commensal species        Habitat             CNHE
  Proteocephalidea genus          Intestine           7774
    species, P *
  Aplectana species, A *          Cloaca, intestine   5687-5689
  Cosmocercella diaglenae, A **   Cloaca, intestine   5690-5692
  Parapharyngodon chamelensis,    Intestine           5693-5696, 8669
    A **
  Physalopteroides bahamensis,    Stomach             5697-5698
    A * **
  Dero (Allodero) species,        Ureters, oviduct    5699, 8500
    J* **

                                  Colima Site 1     Colima Site 2
                                  (n = 5) (b)       (n = 11) (c)

Parasite/commensal species          %        MA       %        MA
  Proteocephalidea genus          -- (e)     --       --       --
    species, P *
  Aplectana species, A *            40      1.8      45.4     1.5
  Cosmocercella diaglenae, A **     40     190       18.2     1.4
  Parapharyngodon chamelensis,      20      2.6      72.7     14.1
    A **
  Physalopteroides bahamensis,      --       --      27.3     1.3
    A * **
  Dero (Allodero) species,          --       --      36.4     0.81
    J* **

                                  (n = 5) (d)

Parasite/commensal species          %        MA
  Proteocephalidea genus            20      0.2
    species, P *
  Aplectana species, A *            --       --
  Cosmocercella diaglenae, A **     --       --
  Parapharyngodon chamelensis,     100      141
    A **
  Physalopteroides bahamensis,      --       --
    A * **
  Dero (Allodero) species,          60      6.4
    J* **

(a) P = plerocercoid, A = adult, J = juvenile. * = new host record,
** = new locality record, CNHE = Coleccion Nacional de Helmintos
accession number, n = sample size, % = prevalence (number of
infected hosts with one or more individuals of a species, or taxa,
divided by the number of examined hosts), MA = mean abundance (total
number of individuals of a particular parasite in a sample divided
by the number of examined hosts).

(b) Colima Site 1, temporary pond beside a road near Highway 98
between Minatitlan and Manzanillo.

(c) Colima Site 2, pond with a breeding chorus next to a road beside
Highway 54 near Ixtlahuacan.

(d) Jalisco, on vegetation and in water from a breeding chorus in a
temporary pond at a pristine tropical dry forest in the
Chamela-Cuixmala Biosphere Reserve.

(e) Dash indicates no data.
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Author:Garrido-Olvera, Lorena; Cabrera-Guzman, Elisa; Velarde-Aguilar, Maria G.; Leon-Regagnon, Virginia
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Jun 1, 2015
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