Helmintofauna de Lithobates brownorum (Anura: Ranidae) en tres localidades del estado de Yucatán, México

Abstract

Between July 2004 and June 2005, 84 specimens of Lithobates brownorum (Sanders, 1973) were collected and examined for helminths. Hosts came from 3 localities in the state of Yucatán, Mexico: Celestún (n= 35), Lagunas de Yalahau (n= 33), and Ría Lagartos (n= 16). Twelve helminth taxa were found: 7 nematodes, 4 digeneans, and 1 acanthocephalan. With the exception of Haematoloechus floedae and Megalodiscus temperatus, all helminth taxa found have a Neotropical distribution. Our results differ from those obtained in previous studies dealing with amphibians in Mexico because we found higher richness and abundance of nematodes than digenean species. The relatively low mean intensity and mean abundance values reached by digenean species in this study may be related to the generalist host diet and with the vagility of frogs (from the aquatic to the terrestrial environment or vice versa).

Full text

Revista Mexicana de Biodiversidad 81: 191- 195, 2010
Recibido: 23 septiembre 2008; aceptado: 05 noviembre 2009
Research note
Helminth fauna of Lithobates brownorum (Anura: Ranidae) at three localities in
the state of Yucatán, Mexico
Helmintofauna de Lithobates brownorum (Anura: Ranidae) en tres localidades del estado de
Yucatán, México
Carlos A. Yáñez-Arenas and Sergio Guillén-Hernández*
Departamento de Biología Marina, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil,
Km 15.5. Apartado postal 4-116, Itzimná, Mérida, Yucatán, México.
*Correspondencia: ghernand@uady.mx
Abstract. Between July 2004 and June 2005, 84 specimens of Lithobates brownorum (Sanders, 1973) were collected
and examined for helminths. Hosts came from 3 localities in the state of Yucatán, Mexico: Celestún (n= 35), Lagunas
de Yalahau (n= 33), and Ría Lagartos (n= 16). Twelve helminth taxa were found: 7 nematodes, 4 digeneans, and 1
acanthocephalan. With the exception of Haematoloechus fl oedae and Megalodiscus temperatus, all helminth taxa found
have a Neotropical distribution. Our results differ from those obtained in previous studies dealing with amphibians in
Mexico because we found higher richness and abundance of nematodes than digenean species. The relatively low mean
intensity and mean abundance values reached by digenean species in this study may be related to the generalist host diet
and with the vagility of frogs (from the aquatic to the terrestrial environment or vice versa).
Key words: parasites, anurans, infection levels.
Resumen. Entre julio del 2004 y junio del 2005, se recolectaron y examinaron 84 ejemplares de Lithobates brownorum
(Sanders, 1973) en busca de helmintos en 3 localidades del estado de Yucatán: Celestún (n= 35), Lagunas de Yalahau (n=
33) y Ría Lagartos (n= 16). Los ejemplares estuvieron parasitados por 12 taxa de helmintos, 7 de nematodos, 4 digéneos
y 1 acantocefalo. Con excepción de Haematoloechus fl oedae y Megalodiscus temperatus, todos los taxa presentan
distribución neotropical. Nuestros resultados difi eren de los obtenidos por otros autores que han reportado más especies
de digéneos que de nematodos en este grupo de hospederos. Los bajos valores de intensidad y abundancia media de los
digéneos encontrados en este estudio pueden estar relacionados con la amplia dieta del hospedero y la vagilidad que éste
presenta entre el medio acuático y el terrestre.
Palabras clave: parásitos, anuros, niveles de infección.
In southern Mexico, Lithobates brownorum (Sanders,
1973) is a widely distributed frog that is commonly found
in and around water bodies throughout the Yucatán
Peninsula (Zaldívar-Riverón et al., 2004). However,
information concerning the helminth parasites associated
to this frog species in the Yucatán Peninsula (Moravec,
et al. 2002; León-Règagnon et al., 2005), or elsewhere in
Mexico (Paredes-León et al. 2008) is scarce. The present
work was aimed at characterizing the helminth fauna
present in L. brownorum specimens collected at 3 different
localities in Yucatán.
From July 2004 to June 2005, L. brownorum
specimens were collected from the following localities: 1),
Celestún, located on the northwest coast of the Yucatán
Peninsula (20°46´, 21°06´ N; 90°11´, 90°25´ W); 2),
Yalahau, an inland lagoon found in the central portion
of the state (20°40´37.3´´, 20°34´59.7´´N, 89°10´49.6´´,
89°15´00.5´´W); and 3), Ría Lagartos (21°32´, 21°34´N;
87°35´, 88°15´W) found on the northeast coast of the
Yucatán Peninsula.
Frogs were captured either by hand or with seine
nets, and specimens were kept alive until parasitological
examination was conducted. Specimens were sacrifi ced
with an overdose of sodium pentobarbital. All organs

192 Yáñez-Arenas and Guillén-Hernández.- Helminths of Lithobates brownorum
were examined under a stereo-microscope, and helminths
were removed, counted, and identifi ed. Standard
techniques were employed to prepare parasite specimens
for microscopic examination (see Lamothe-Argumedo,
1997). Parasite voucher specimens were deposited in the
Colección Nacional de Helmintos (CNHE) of the Instituto
de Biología, Universidad Nacional Autónoma de México
(UNAM), Mexico City. Ecological parameters such as
prevalence, mean intensity, and mean abundance were
calculated following Bush et al. (1997).
A total of 84 L. brownorum specimens were collected
and examined (Celestún, n= 35; Yalahau, n= 33; and Ría
Lagartos, n= 16). Four hundred and forty helminths (296
nematodes, 139 digeneans, and 5 acanthocephalans) were
found, representing 12 taxa (3 of them in larval stage). Seven
taxa were nematodes, 4 digeneans, and 1 acanthocephalan.
Nine of these taxa are recorded for the fi rst time in Yucatán
(Table 1), and 9 represent new records for L. brownorum
(Langeronia macrocirra Caballero y Bravo-Hollis, 1949,
Megalodiscus temperatus (Stafford, 1923), Aplectana
incerta Caballero, 1949, Foleyellides striatus (Ochoterena
and Caballero, 1932), Rhabdias füelleborni Travassos,
1926, Subulascaris falcaustriformis Texeira de Freitas and
Dobbin, 1957, Contracaecum sp., Physalopteridae gen.
sp., and Oncicola sp.).
The greatest number of helminth taxa was found in
specimens from Celestún, while the lowest numbers of
parasites were found in specimens from Ría Lagartos.
Overall, more nematode species were found than any other
helminth taxonomic group. The greatest prevalence and
mean abundance values were observed for the nematodes
S. falcaustriformis and A. incerta in specimens from
Celestún and Yalahau, respectively. On the other hand,
the digenean L. macrocirra showed the highest prevalence
and mean abundance values for specimens in Ría Lagartos.
Finally, the digeneans G. brownorumae and again L.
macrocirra showed the highest mean intensity values for
specimens from Ría Lagartos; Glypthelmins brownorumae
also was the species with the highest mean intensity value
for specimens from Celestún, and L. macrocirra had
the greatest value for this parameter for specimens from
Yalahau (Table 2).
Previous to this work, only 2 helminth species had
been recorded for L. brownorum in Yucatán (Moravec et
al., 2002; León-Règagnon et al., 2005, Paredes-León et al.,
2008); our study increased this number to 13. Except for
H. fl oedae and M. temperatus, all helminth species found
have Neotropical distribution. The presence of H. fl oedae
Table 1. Helminth parasites found in L. brownorum specimens (n= 84) collected at 3 localities in Yucatán, Mexico. RBC= Reserva de
la Biosfera de Celestún, PELY= Parque Estatal Lagunas de Yalahau, RBRL= Reserva de la Biosfera de Ría Lagartos
Helminth RBC PELY RBRL Distribution Hábitat
DIGENEA
Glypthelmins brownorumae Razo-Mendivil, et al. 2004† XX
Neotropical Intestine
Haematoloechus fl oedae Harwood, 1932 XNearctic Lungs
Langeronia macrocirra Caballero y Bravo-Hollis, 1949* † XXX
Neotropical Intestine
Megalodiscus temperatus (Stafford, 1923)*† XNearctic Intestine
ACANTHOCEPHALA
Oncicola sp.* XX
Neotropical Mesentery
NEMATODA
Aplectana incerta Caballero, 1949 *† XXX
Neotropical Intestine
Contracaecum sp. * † XXX ? Body cavity
Foleyellides striatus (Ochoterena and Caballero, 1932)* †
Caballero, 1935* †
XXX
Neotropical Body cavity
Oswaldocruzia subauricularis (Rudolphi 1819) * XNeotropical Intestine
Physalopteridae gen. sp. * †XX Body cavity
Rhabdias fülleborni Travassos, 1926 *† XX Neotropical Lungs
Subulascaris falcaustriformis Texeira de Freitas y Dobbin,
1957 * † XXX
Neotropical Intestine
* New host record
† New record in the state of Yucatán.

Revista Mexicana de Biodiversidad 81: 191- 195, 2010 193
Table 2. Helminth infection levels from L. brownorum specimens collected at 3 localities in Yucatán, Mexico. RBC= Reserva de la
Biosfera de Celestún, PELY= Parque Estatal Lagunas de Yalahau, RBRL= Reserva de la Biosfera de Ría Lagartos. %= Prevalence,
MI= Mean Intensity ± SD, MA=Mean Abundance ± SD
Locality RBC (n=35) PELY (n=33)
DIGENEA % MA (± SE) MI (± SD) % MA (± SD MI (± SD)
Megalodiscus temperatus 2.0 0.02 ( ± 0.16 ) 1 ( ± 0 ) 0.0 0.0 0.0
Haematoloechus fl oedae 0.0 0.0 0.0 3.0 0.03 ( ± 0.17 ) 1.0 ( ± 0.0 )
Langeronia macrocirra 14.0 0.54 ( ± 1.54 ) 3.80 ( ± 2.16 ) 15.0 1.42 ( ± 6.13 ) 9.40 ( ± 14.39 )
Glypthelmins brownorumae 20.0 1.17 ( ± 3.61 ) 5.85 ( ± 6.49 ) 0.0 0.0 0.0
ACANTHOCEPHALA
Oncicola sp. 8.0 0.11 ( ± 0.40 ) 1.33 ( ± 0.57 ) 0.0 0.0 0.0
NEMATODA
Rhabdias fülleborni 20.0 0.80 ( ± 2.38 ) 4.14 ( ± 4.017) 9.0 0.24 ( ± 0.86 ) 2.66 ( ± 1.52 )
Aplectana incerta 5.0 0.14 ( ± 0.69 ) 2.50 ( ± 2.12 ) 39.0 1.54 ( ± 2.39 ) 3.92 ( ± 2.28 )
Foleyellides striatus 14.0 0.42 ( ± 1.24 ) 3.0 ( ± 1.87 ) 6.0 0.09 ( ± 0.38 ) 1.50 ( ± 0.70 )
Subulascaris falcaustriformis 25.0 1.48 ( ± 3.95 ) 5.77 ( ± 6.22 ) 18.0 0.96 ( ± 3.03 ) 5.33 ( ± 5.57 )
Contracaecum sp. 2.0 0.02 ( ± 0.16 ) 1.0 ( ± 0 ) 6.0 0.06 ( ± 0.24 ) 1.0 ( ± 0 )
Oswaldocruzia subauricularis 0.0 0.0 0.0 18.0 0.57 ( ± 1.41 ) 3.16 ( ± 1.72 )
Physalopteridae gen. sp. 8.0 0.20 ( ± 0.75 ) 2.33 ( ± 1.52 ) 15.0 1.27 ( ± 5.41 ) 8.40 ( ± 12.64 )
Locality RBRL (n=16)
DIGENEA % MA (± SD) MI (± SD)
Megalodiscus temperatus 0.0 0.0 0.0
Haematoloechus fl oedae 0.0 0.0 0.0
Langeronia macrocirra 25.0 1.50 ( ± 2.96 ) 6.0 ( ± 2.82 )
Glypthelmins brownorumae 6.0 0.37 ( ± 1.5 ) 6.0 ( ± 0 )
ACANTHOCEPHALA
Oncicola sp. 6.0 0.06 ( ± 0.25 ) 1.0 ( ± 0.0 )
NEMATODA
Rhabdias fülleborni 0.0 0.0 0.0
Aplectana incerta 18.0 0.75 ( ± 2.04 ) 4.0 ( ± 3.46 )
Foleyellides striatus 12.0 0.43 ( ± 1.31 ) 3.50 ( ± 2.12 )
Subulascaris falcaustriformis 6.0 0.12 ( ± 0.5 ) 2.0 ( ± 0 )
Contracaecum sp. 12.0 0.56 ( ± 1.99 ) 4.50 ( ± 4.94 )
Oswaldocruzia subauricularis 0.0 0.0 0.0
Physalopteridae gen. sp. 0.0 0.0 0.0

194 Yáñez-Arenas and Guillén-Hernández.- Helminths of Lithobates brownorum
in native amphibian species in Yucatán may be due to the
introduction of Lithobates catesbeiana (Shaw, 1802) in the
region for culture purposes (León-Règagnon, et al., 2005).
On the other hand, M. temperatus has a wide distribution
and has been recorded from the southern United States
of America to Costa Rica, where it is a common parasite
of several genera of anurans (Yamaguti, 1971; Bursey
and Golberg, 2005). The widespread distribution of fi nal
hosts of M. temperatus suggests the presence of a species
complex which needs further research.
Numerous studies have shown that in general more
digeneans species are found in amphibians with either
aquatic or semiaquatic habits, while nematode species
are more common in terrestrial amphibians (Aho, 1990;
Guillén-Hernández et al., 2000; Pérez-Ponce de León et
al., 2000; Paredes-Calderón, et al., 2004; Espínola-Novelo
and Guillén-Hernández, 2008). Overall, results from this
work contradict these fi ndings; nematode species richness
and mean abundance in L. brownorum were greater
compared to that of digeneans in 2 of the localities (Table
2). This difference in the number of nematode and digenean
species and their relative abundances in L. brownorum
may be due to the specifi c biotic and abiotic conditions
present in those localities. A low richness of suitable
invertebrate species acting as intermediate hosts (e.g.,
snails and insects) throughout the life cycle of digeneans
at those localities may explain our results. Nematode
species collected in this study are monoxenous and most
of them infect their host via skin penetration. Amphibians
are generally considered generalist feeders and their diets
usually refl ect the availability of suitable prey (Duellman
and Trueb, 1994). In particular, L. brownorum has been
shown to feed on a wide variety of terrestrial and aquatic
arthropods, although it does not show a special preference
for any given item (Ramírez-Bautista and Lemos-Espinal,
2004). Digeneans usually require an aquatic intermediate
host species in addition to a snail species in their life cycle.
The presence of M. temperatus and G. brownorum in this
amphibian species suggests the possibility that it feeds on
its own skin after molting since larval stages (metcercariae)
of these parasites occur in amphibian skin (Smith, 1980);
another possibility is that adults prey on tadpoles.
The relatively low mean intensity and mean abundance
values found for digeneans in this study may be related
to this amphibian’s generalist diet, as well as its mobility
between aquatic and terrestrial habitats. The high
prevalence values observed for nematodes relative to
digeneans suggests that L. brownorum spends a signifi cant
amount of time out of the water, resulting in high rates of
nematode recruitment via skin penetration.
Results for L. brownorum, the mostly aquatic host
that we examined in this study and those reported for the
terrestrial hosts C. marinus and C. valliceps in Yucatán
(Espinola-Novelo and Guillén-Hernández, 2008) strongly
differ from results reported in a study which examined
specimens of both terrestrial species and 2 aquatic (L.
berlandieri and L. vaillanti) species closely related to
L. brownorum from Los Tuxtlas, Veracruz (Guillén-
Hernández, 1992; Guillén-Hernández, et al. 2000). These
fi ndings suggest that digeneans species are an important
component which structures the parasite community of
amphibians in Veracruz, while in Yucatán nematodes
appear to take their place as we found them to be more
species-rich and abundant. Further studies which record
helminth species for other species of amphibians in the
Yucatan Peninsula are necessary to provide insight on this
issue.
We thank Jorge Cerón, Alfredo Barrera, Karla
Rodríguez, Juan Espínola, and Mara Bravo for fi eld
assistance. The authors also thank Rosario Mata,
David Osorio, and Elizabeth Martínez (Laboratorio
de Helmintología, UNAM) for their assistance in the
identifi cation of some helminth species. Financial support
for this study was granted by CONACYT (FOMIX-YUC-
2003-CO3-036) as part of the project titled “Valoración
de la diversidad de helmintos en anfi bios de tres áreas
protegidas del estado de Yucatán”
Literature cited
Aho, J. M. 1990. Helminth communities of Amphibians and
Reptiles: comparative approaches to understanding patterns
and processes. In Parasites communities: patterns and
processes, G. Esch, A. Bush and J. Aho (eds.). Chapman and
Tall, London. p. 157-196.
Brooks, D., V. León-Règagnon, D. Mclennan and D. Zelmer.
2006. Ecological fi tting as a determinant of the community
structure of platyhelminth parasites of anurans. Ecology 87:
S76-S85.
Bursey, C. R. and S. R. Golberg. 2005. New species of
Oswaldocruzia (Nematoda: Molineoidea), new species of
Rhabdias (Nematoda: Rhabdiasidae), and other helminthes
of Rana cf. forreri (Anura: Ranidae) from Costa Rica.
Journal of Parasitology 91:600-6005.
Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997.
Parasitology Meets Ecology on its own terms: Margolis et al.
Revisited. Journal of Parasitology 83:575-583.
Duellman, W. E. and L. Trueb. 1986. Biology of amphibians.
The Johns Hopkins University Press. Baltimor and London.
670 p.
Espínola-Novelo, J. F. and S. Guillén-Hernández. 2008.
Helminth parasites in C. marinus and C. valliceps (Anura:
Bufonidae) from Lagunas Yalahau, Yucatán, Mexico.
Journal of Parasitology 94:672-674.
Guillén-Hernández, S. 1992. Comunidades de helmintos de
algunos anuros de “Los Tuxtlas”, Veracruz. Thesis, Facultad

Revista Mexicana de Biodiversidad 81: 191- 195, 2010 195
de Ciencias, UNAM. 90 p.
Guillén-Hernández, S., G. Salgado-Maldonado and R. Lamothe-
Argumedo. 2000. Digeneans (Platyhelminthes: Trematoda)
of seven sympatric species of anurans from Los Tuxtlas,
Veracruz, México. Studies of Neotropical Fauna and
Environment 35:10-13.
Lamothe-Argumedo, R. 1997. Manual de técnicas para preparar
y estudiar los parásitos de animales silvestres. AGT, México,
D.F. 43 p.
León-Règagnon, V., S. Guillén-Hernández and M. A. Arizmendi-
Espinosa. 2005. Intraespecifi c variation of Haematoloechus
fl oedae Harwood, 1932 (Digenea: Plagiorchiidae), from Rana
spp. in North and Central America. Journal of Parasitology
91:915-921.
Moravec, F., E. Mendoza-Franco, C. Vivas-Rodríguez, J.
Vargas-Vázquez and D. González-Solís. 2002. Observations
on seasonal changes in the occurrence and maduration of
fi ve helminth species in the Pimelodid catfi sh, Rhamdia
guatemalensis, in the cenote (=sinkhole) Ixin-há, Yucatán,
Mexico. Acta Societae Zoologicae Bohemia 66:121-140.
Paredes-Calderón, E. L., V. León-Regagnon and L. Garcıía-
Prieto. 2004. Helminth infracommunities of Rana vaillanti
Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico.
Journal of Parasitology 90:692-696.
Paredes-León, R., L. García-Prieto, C. Guzmán-Cornejo, V.
León-Regagnon and T. M. Pérez. 2008. Metazoan parasites
of Mexican amphibians and reptiles. Zootaxa 1904:1-166.
Pérez-Ponce de León, G., V. León-Règagnon, L. García-Prieto,
U. Razo Mendivil and A. Sánchez-Álvarez. 2000. Digenean
fauna of amphibians from Central Mexico: Nearctic and
Neotropical Infl uences. Comparative Parasitology 67:92-
106.
Ramírez-Bautista, A. and J. A. Lemos-Espinal. 2004. Diets of
two syntopic populations of frogs, Rana vaillanti and Rana
brownorum, from a tropical rain forest in southern Veracruz,
México. Southwestern Naturalist 49:316-320.
Razo-Mendivil, U., V. León-Règagnon and G. Pérez-Ponce
de León. 2006. Monophyly and systematic position of
Glypthelmins (Digenea), based on partial lsrDNA sequences
and morphological evidence. Organisms, Diversity &
Evolution 6:308-320.
Smith, J. D. and M. M. Smith. 1980. Frogs as host-parasites
system I. The MacMillan Press LTD, London. 101 p.
Yamaguti, S. 1971. Synopsis of Digenetic Trematodes of
Vertebrates. Vol. I and III. Keigaku Publishing Co. Tokyo,
Japan. 1974 p.
Zaldívar-Riverón, A., V. León-Règagnon and A. Nieto-Montes
de Oca. 2003. Phylogenetic relationships of Mexican coastal
frogs (Rana berlandieri group) based on mtDNA sequences.
Molecular Phylogenetics and Evolution 26:38-49.