1 Introduction
The leiuperid genus Pleurodema (Tshudi, 1838) currently comprises 15 species widely distributed in the Neotropical region (Frost, 2011Frost, DR., 2011. Amphibian Species of the World 5.5, an Online Reference. Electronic Database. New York: American Museum of Natural History. Available from: <http://research.amnh.org/vz/herpetology/amphibia>.), mainly in dry forests and open areas (Ferraro and Casagranda, 2009FERRARO, DP. and CASAGRANDA, MD., 2009. Geographic distribution of the genus in Argentina (Anura: Leiuperidae). PleurodemaZootaxa, vol. 2024, p. 33-55.; Kolenc et al., 2009KOLENC, F., BORTEIRO, C., BALDO, D., FERRARO, DP. and PRIGIONI, C. 2009. The tadpoles of (Müller), with notes on their advertisement calls, natural history and conservation status (Amphibia, Anura, Leiuperidae). Pleurodema bibroni Tschudi and Pleurodema kriegiZootaxa, vol. 1969, p. 1-35.). Pleurodema diplolister (Peters, 1870) is the only species in the genus known to inhabit the Caatinga biome (shrub-like vegetation) (Cardoso and Arzabe, 1993Cardoso, AJ. and Arzabe, C., 1993. Corte e desenvolvimento larvário de (Anura: Leptodactylidae). Pleurodema diplolistrisRevista Brasileira de Biologia = Brazilian Journal of Biology, vol. 53, no. 4, p. 561-570.). The species is also found in the Brazilian Cerrado and Cerrado-Caatinga transition zones (Andrade and Vaz-Silva, 2012Andrade, SP. and Vaz-Silva, W., 2012. First state record and distribution extension of (Peters 1870) (Anura: Leiuperidae) from state of Goiás, Brazil. Pleurodema diplolisterCheck List, vol. 8. no. 4, p. 149-151.).
Pleurodema diplolister is a fossorial and omnivorous frog, and its
explosive reproduction shows greater specialization between the anuran communities
of the Caatinga (Hödl, 1992HÖLD, W., 1992. Reproductive behavior in the neotropical
foam-nesting frog (Leptodactylidae). Pleurodema
diplolistrisAmphibia-Reptilia, vol. 13, no. 3, p. 263-274.
http://dx.doi.org/10.1163/156853892X00472.
http://dx.doi.org/10.1163/156853892X0047...
; Cardoso and Arzabe, 1993Cardoso, AJ. and Arzabe, C., 1993. Corte e desenvolvimento larvário
de (Anura: Leptodactylidae). Pleurodema diplolistrisRevista
Brasileira de Biologia = Brazilian Journal of Biology, vol. 53, no. 4, p.
561-570.; Santos et al., 2003Santos, JWA., Damasceno, RP. and Rocha, PLB., 2003. Feeding habits
of the frog (Anura, Leptodactylidae) in quaternary sand dunes of the Middle Rio
São Francisco, Bahia, Brazil. Pleurodema
diplolistrisPhyllomedusa, vol. 2, no. 2, p. 83-92.
http://dx.doi.org/10.11606/issn.2316-9079.v2i2p83-92.
http://dx.doi.org/10.11606/issn.2316-907...
).
Parasitological studies are important to understand host population dynamics, as well
behavioral, morphological and dietary shifts, especially within highly specialized
anurans such as P. diplolister. To date, only two records of
parasitism in the genus Pleurodema are available, all of these by
nematodes of the family Cosmocercidae: Aplectana meriodionalis Lent
and Freitas, 1948 infecting Pleurodema borellii Peracca, 1895
(Baker, 1980BAKER, MR., 1980. Revision of old World species of the genus
Aplectana Railliet & Henry, 1916 (Nematoda, Cosmocercidae). Bulletin du
Museum National d’Histoire Naturelle, vol. 2, p. 955-998.) and Oxyascaris
oxyascaris Travassos, 1920 in P. diplolister (Vicente et al., 1990Vicente, JJ., Rodrigues, HO., Gomes, DC. and Pinto, RM., 1990.
Nematóides do Brasil 2 parte: nematóides de Anfíbios. Revista Brasileira de
Zoologia, vol. 7, no. 4, p. 549-626.
http://dx.doi.org/10.1590/S0101-81751990000400015.
http://dx.doi.org/10.1590/S0101-81751990...
).
Herein, we present data on helminth infection of the frog P. diplolister in the Caatinga of Pernambuco State, Brazil.
2 Material and Methods
The study was conducted onAngico Farm (08° 07’ 55.7” S 40° 05’ 3.2” W), located in the rural zone of the municipality of Ouricuri, in the Caatinga of Pernambuco State. The vegetation is characterized mainly by deciduous forest and hypoxerophytic Caatinga (CPRM, 2005CPRM, 2005. Diagnóstico do município de Ouricuri. Brasília. Available from: <http://www.cprm.gov.br>. Access in: 12 Apr. 2012.).
Pleurodema diplolister specimens were collected in February 2012, using pitfall traps with drift fence or by hand, in a gallery forest near a temporary river after one of the few rains occurring that year. The specimens were euthanatized with a lethal injection of lidocaine, fixed in 10% formalin and then stored in 70% ethanol. The snout-vent length was measured with a digital caliper (± 0.01 mm). Sex was assigned by the direct examination of the gonads. Voucher specimens were deposited at Coleção Herpetológica da Universidade Regional do Cariri, Crato municipality, Ceará State (URCA-H: 2855-2858, 2866-2870).
Lungs, gall bladder and digestive tract were examined under a stereomicroscope for parasites. For identification, nematodes were cleared in lactophenol, and the cestodes were stained with carmine, dehydrated in an increasing alcohol series and cleared in creosote, where they were subsequently mounted on temporary slides and identified under a light microscope. All parasites were counted and stored in 70% ethanol. Voucher specimens were deposited in the Coleção Parasitológica da URCA (URCA-P: 357-359, 379-381).
Prevalence and mean intensity of infection were calculated according to Bush et al. (1997)Bush, AO., Lafferty, KD., Lotz, JM. and Shostak, AW., 1997.
Parasitology meets ecology on its own terms: Margolis et al. revisited. The
Journal of Parasitology, vol. 83, no. 4, p. 575-583.
http://dx.doi.org/10.2307/3284227. PMid:9267395
http://dx.doi.org/10.2307/3284227...
. A Pearson correlation
(R) was conducted to determine the relationship between
snout-vent length (SVL) and number of parasites using R software (R Development Core Team, 2013R Development Core Team, 2013. R: a language and environment for
statistical computing. Vienna: R Foundation for Statistical Computing.
http://www.R-project.org/.
http://www.R-project.org/...
). The
discrepancy index (D) was used to measure the level of aggregation of each helminth
species, as suggested by Poulin (1993)Poulin, R., 1993. A cleaner perspective on cleaning symbiosis.
Reviews in Fish Biology and Fisheries, vol. 3, no. 1, p. 75-79.
http://dx.doi.org/10.1007/BF00043298.
http://dx.doi.org/10.1007/BF00043298...
. This
index was calculated with the software Quantitative Parasitology 3.0 (Rozsa et al., 2000Rózsa, L., Reiczigel, J. and Majoros, G., 2000. Quantifying
parasites in samples of hosts. The Journal of Parasitology, vol. 86, no. 2, p.
228-232. http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2.
PMid:10780537
http://dx.doi.org/10.1645/0022-3395(2000...
).
3 Results
A total of 32 specimens of P. diplolister were examined, which included 11 males (33.04 ± 1.29 mm SVL) and 21 females (34.6 ± 1.71 mm SVL). Two helminth species were found infecting the intestines of P. diplolister from the Caatinga of Pernambuco State: Raillietnema spectans Gomes, 1964 (Nematoda: Cosmocercidae) and Plerocercoid larvae of the family Proteocephalidae (Cestoda). These larvae could not be identified due to the immature condition.
Of the total anuran hosts examined, six of them harbored at least one helminth species (overall prevalence of 18.75%; mean intensity of infection of 10 ± 13.59). For R. spectans, the prevalence was 15.6% and for the plerocercoid cestode larvae 3.1%. The prevalence was 19.4% for female hosts and 18.2% for males. Mean intensity of infection was 14.3 for females and 1 for males. Discrepancy index (D) was 0.901 for R. spectans and 1 for the cestode larvae.
4 Discussion
Helminth communities of amphibians are characterized by generalist species (Aho, 1990Aho, JM., 1990. Helminth communities of amphibians and reptiles:
comparative approaches to understanding patterns and process. In ESCH, GW.,
BUSH, AO. and AHO, JM. (Eds.). Parasite communities: patterns and process.
London: Chapman and Hall. p. 157-199.
http://dx.doi.org/10.1007/978-94-009-0837-6_7.
http://dx.doi.org/10.1007/978-94-009-083...
). The low host specificity, allied
to the general lack of studies with Neotropical frog species, frequently are the
main causes of new host records. In Brazil, species of Leptodactylidae and Bufonidae
may be considered as hosts for a generalist helminth fauna, in view of studies
conducted so far (Vicente et al., 1990Vicente, JJ., Rodrigues, HO., Gomes, DC. and Pinto, RM., 1990.
Nematóides do Brasil 2 parte: nematóides de Anfíbios. Revista Brasileira de
Zoologia, vol. 7, no. 4, p. 549-626.
http://dx.doi.org/10.1590/S0101-81751990000400015.
http://dx.doi.org/10.1590/S0101-81751990...
,
Goldberg et al., 2007Goldberg, SR., Bursey, CR., Caldwell, JP., Vitt, LJ. and Costa, GC.,
2007. Gastrointestinal helminths from six species of frogs and three species of
lizards, sympatric in Pará State, Brazil. Comparative Parasitology, vol. 74, no.
2, p. 327-342. http://dx.doi.org/10.1654/4268.1.
http://dx.doi.org/10.1654/4268.1...
, 2009Goldberg, SR., Bursey, CR., Caldwell, JP. and Shepard, DB., 2009.
Gastrointestinal Helminths of Six Sympatric Species of Leptodactylus from
Tocantins State, Brazil. Comparative Parasitology, vol. 76, no. 2, p. 258-266.
http://dx.doi.org/10.1654/4368.1.
http://dx.doi.org/10.1654/4368.1...
; Luque
et al., 2005Luque, JL., Martins, AN. and TAVARES, LER., 2005. Community
structure of metazoan parasites of the yellow Cururu toad, (Anura, Bufonidae)
from Rio de Janeiro, Brazil. Bufo ictericusActa Parasitologica,
vol. 50, no. 1, p. 215-220.). Regarding others amphibians taxa, further studies is still
required to have any conclusion about the host specificity.
The leiuperid P. diplolister is a new host record for the
cosmocercid R. spectans and for the proteocephalidean cestode. In
Brazil, R. spectans is known to infect the bufonids
Rhinella crucifer (Wied-Neuwied, 1821), Rhinella
icterica (Spix, 1824), and Rhinella schneideri
(Werner, 1894) and the leptodactylid Leptodactylus latrans
(Steffen, 1815) (Vicente et al., 1990Vicente, JJ., Rodrigues, HO., Gomes, DC. and Pinto, RM., 1990.
Nematóides do Brasil 2 parte: nematóides de Anfíbios. Revista Brasileira de
Zoologia, vol. 7, no. 4, p. 549-626.
http://dx.doi.org/10.1590/S0101-81751990000400015.
http://dx.doi.org/10.1590/S0101-81751990...
).
Cestodes of the family Proteocephalidae are endoparasites of vertebrates, infecting
mainly freshwater fishes (Pavanelli and Santos,
1991Pavanelli, GC. and Santos, MHM., 1991. Proteocefalídeos parasitos de
peixes, em especial pimelodídeos do rio Paraná, Paraná. Revista Unimar, vol. 13,
no. 2, p. 147-162.). It is also found in anurans of the families Leptodactylidae in
Chile and Peru (Olmos and Muñoz, 2006Olmos, V. and Muñoz, G., 2006. Estado de conocimiento de los
parasitos eumetazoos de organismos dulceacuicolas de Chile. Gayana Zoologica,
vol. 70, no. 1, p. 122-139.; Iannacone, 2003IANNACONE, J., 2003. Helminth parasites of . Telmatobius
jelskii (Peters) (Anura, Leptodactylidae) from Lima, PeruRevista
Brasileira de Zoologia, vol. 20, no. 1, p. 131-134.), Bufonidae in Peru (Tantaleán and Garcia, 1989TANTALEÁN, MV. and GARCÍA, L., 1989. Contribución al estudio de los
helmintos parásitos de anfibios del Perú. Boletín de Lima, vol. 64, p.
69-78.), Hylidae in
Ecuador (Dyer and Altig, 1977Dyer, WG. and Altig, R., 1977. sp. n. (Cestoda: Proteocephalidae)
from Spix 1824 in Ecuador. OphiotaeniaolseniHyla
geographicaThe Journal of Parasitology, vol. 63, no. 5, p. 790-792.
http://dx.doi.org/10.2307/3279879.
http://dx.doi.org/10.2307/3279879...
), and Ranidae
in Costa Rica (Bursey and Goldberg, 2006BURSEY, CR. and GOLDBERG, SR., 2006. New species of
Raillietnema (Nematoda: Cosmocercidae) and other helminths
in (Ranidae) from Costa Rica. Rana vibicariaComparative
Parasitology, vol. 73, no. 2, p. 193-200.)
and Papua New Guinea (Bursey et al.,
2008BURSEY, CR., GOLDBERG, SR. and KRAUS, F., 2008. A new species of
(Cestoda: Proteocephalidae), description of the male of (Nematoda:
Quimperiidae), and other endoparasites in .
ProteocephalusDesmognathinema
papuensisSylvirana supragrisea (Anura:Ranidae)
from Papua New GuineaComparative Parasitology, vol. 75, no. 1, p. 33-48.
http://dx.doi.org/10.1654/4291.1.
http://dx.doi.org/10.1654/4291.1...
).
Brazil harbors a high diversity of amphibians with 946 species (Segalla et al., 2012Segalla, MV., Caramaschi, U., Cruz, CAG., Garcia, PCA. and Grant,
T., HADDAD, CFB. and LANGONE, J., 2012. Brazilian amphibians: list of species.
São Paulo. Available from: <http://www.sbherpetologia.org.br>. Access in:
6 Apr. 2013.). Despite this great diversity,
parasitological studies focusing on ecological aspects, such as helminth community
structure are scarce. Although there has been an increase in such studies in the
past few years (Luque et al., 2005Luque, JL., Martins, AN. and TAVARES, LER., 2005. Community
structure of metazoan parasites of the yellow Cururu toad, (Anura, Bufonidae)
from Rio de Janeiro, Brazil. Bufo ictericusActa Parasitologica,
vol. 50, no. 1, p. 215-220.; Campião et al., 2009Campião, KM., Silva, RJ. and Ferreira, VL., 2009. Helminth parasites
of Leptodactylus podicipinus (Anura: Leptodactylidae) from south-eastern
Pantanal, State of Mato Grosso do Sul, Brazil. Journal of Helminthology, vol.
83, no. 4, p. 345-349. http://dx.doi.org/10.1017/S0022149X09289358.
PMid:19422730
http://dx.doi.org/10.1017/S0022149X09289...
), further efforts are
still necessary to understand the influence of parasites in the structure and
dynamics of Brazilian anuran populations.
Acknowledgements
We thank Pró-Reitoria de Pós Graduação e Pesquisa da Universidade Regional do Cariri for financial support (Chamada Pública PRPGP-URCA 03/2013). To Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico – FUNCAP for the research grant awarded to RWA (BPI-0067-00006.01.00/12) and fellowship to JGGS. To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for the fellowship to DAT and MRMS, such as by Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (permit 29613-1) for support. We are grateful to João A. Araujo-Filho for laboratory assistance. Dr. A. Leyva helped with English editing of the manuscript.
References
- Aho, JM., 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and process. In ESCH, GW., BUSH, AO. and AHO, JM. (Eds.). Parasite communities: patterns and process. London: Chapman and Hall. p. 157-199. http://dx.doi.org/10.1007/978-94-009-0837-6_7.
» http://dx.doi.org/10.1007/978-94-009-0837-6_7 - Andrade, SP. and Vaz-Silva, W., 2012. First state record and distribution extension of (Peters 1870) (Anura: Leiuperidae) from state of Goiás, Brazil. Pleurodema diplolisterCheck List, vol. 8. no. 4, p. 149-151.
- BAKER, MR., 1980. Revision of old World species of the genus Aplectana Railliet & Henry, 1916 (Nematoda, Cosmocercidae). Bulletin du Museum National d’Histoire Naturelle, vol. 2, p. 955-998.
- Bush, AO., Lafferty, KD., Lotz, JM. and Shostak, AW., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, vol. 83, no. 4, p. 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395
» http://dx.doi.org/10.2307/3284227 - BURSEY, CR. and GOLDBERG, SR., 2006. New species of Raillietnema (Nematoda: Cosmocercidae) and other helminths in (Ranidae) from Costa Rica. Rana vibicariaComparative Parasitology, vol. 73, no. 2, p. 193-200.
- BURSEY, CR., GOLDBERG, SR. and KRAUS, F., 2008. A new species of (Cestoda: Proteocephalidae), description of the male of (Nematoda: Quimperiidae), and other endoparasites in . ProteocephalusDesmognathinema papuensisSylvirana supragrisea (Anura:Ranidae) from Papua New GuineaComparative Parasitology, vol. 75, no. 1, p. 33-48. http://dx.doi.org/10.1654/4291.1.
» http://dx.doi.org/10.1654/4291.1 - Campião, KM., Silva, RJ. and Ferreira, VL., 2009. Helminth parasites of Leptodactylus podicipinus (Anura: Leptodactylidae) from south-eastern Pantanal, State of Mato Grosso do Sul, Brazil. Journal of Helminthology, vol. 83, no. 4, p. 345-349. http://dx.doi.org/10.1017/S0022149X09289358. PMid:19422730
» http://dx.doi.org/10.1017/S0022149X09289358 - Cardoso, AJ. and Arzabe, C., 1993. Corte e desenvolvimento larvário de (Anura: Leptodactylidae). Pleurodema diplolistrisRevista Brasileira de Biologia = Brazilian Journal of Biology, vol. 53, no. 4, p. 561-570.
- CPRM, 2005. Diagnóstico do município de Ouricuri. Brasília. Available from: <http://www.cprm.gov.br>. Access in: 12 Apr. 2012.
- Dyer, WG. and Altig, R., 1977. sp. n. (Cestoda: Proteocephalidae) from Spix 1824 in Ecuador. OphiotaeniaolseniHyla geographicaThe Journal of Parasitology, vol. 63, no. 5, p. 790-792. http://dx.doi.org/10.2307/3279879.
» http://dx.doi.org/10.2307/3279879 - FERRARO, DP. and CASAGRANDA, MD., 2009. Geographic distribution of the genus in Argentina (Anura: Leiuperidae). PleurodemaZootaxa, vol. 2024, p. 33-55.
- Frost, DR., 2011. Amphibian Species of the World 5.5, an Online Reference. Electronic Database. New York: American Museum of Natural History. Available from: <http://research.amnh.org/vz/herpetology/amphibia>.
- Goldberg, SR., Bursey, CR., Caldwell, JP., Vitt, LJ. and Costa, GC., 2007. Gastrointestinal helminths from six species of frogs and three species of lizards, sympatric in Pará State, Brazil. Comparative Parasitology, vol. 74, no. 2, p. 327-342. http://dx.doi.org/10.1654/4268.1.
» http://dx.doi.org/10.1654/4268.1 - Goldberg, SR., Bursey, CR., Caldwell, JP. and Shepard, DB., 2009. Gastrointestinal Helminths of Six Sympatric Species of Leptodactylus from Tocantins State, Brazil. Comparative Parasitology, vol. 76, no. 2, p. 258-266. http://dx.doi.org/10.1654/4368.1.
» http://dx.doi.org/10.1654/4368.1 - HÖLD, W., 1992. Reproductive behavior in the neotropical foam-nesting frog (Leptodactylidae). Pleurodema diplolistrisAmphibia-Reptilia, vol. 13, no. 3, p. 263-274. http://dx.doi.org/10.1163/156853892X00472.
» http://dx.doi.org/10.1163/156853892X00472 - IANNACONE, J., 2003. Helminth parasites of . Telmatobius jelskii (Peters) (Anura, Leptodactylidae) from Lima, PeruRevista Brasileira de Zoologia, vol. 20, no. 1, p. 131-134.
- KOLENC, F., BORTEIRO, C., BALDO, D., FERRARO, DP. and PRIGIONI, C. 2009. The tadpoles of (Müller), with notes on their advertisement calls, natural history and conservation status (Amphibia, Anura, Leiuperidae). Pleurodema bibroni Tschudi and Pleurodema kriegiZootaxa, vol. 1969, p. 1-35.
- Luque, JL., Martins, AN. and TAVARES, LER., 2005. Community structure of metazoan parasites of the yellow Cururu toad, (Anura, Bufonidae) from Rio de Janeiro, Brazil. Bufo ictericusActa Parasitologica, vol. 50, no. 1, p. 215-220.
- Olmos, V. and Muñoz, G., 2006. Estado de conocimiento de los parasitos eumetazoos de organismos dulceacuicolas de Chile. Gayana Zoologica, vol. 70, no. 1, p. 122-139.
- Pavanelli, GC. and Santos, MHM., 1991. Proteocefalídeos parasitos de peixes, em especial pimelodídeos do rio Paraná, Paraná. Revista Unimar, vol. 13, no. 2, p. 147-162.
- Poulin, R., 1993. A cleaner perspective on cleaning symbiosis. Reviews in Fish Biology and Fisheries, vol. 3, no. 1, p. 75-79. http://dx.doi.org/10.1007/BF00043298.
» http://dx.doi.org/10.1007/BF00043298 - R Development Core Team, 2013. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/.
» http://www.R-project.org/ - Rózsa, L., Reiczigel, J. and Majoros, G., 2000. Quantifying parasites in samples of hosts. The Journal of Parasitology, vol. 86, no. 2, p. 228-232. http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. PMid:10780537
» http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2 - Santos, JWA., Damasceno, RP. and Rocha, PLB., 2003. Feeding habits of the frog (Anura, Leptodactylidae) in quaternary sand dunes of the Middle Rio São Francisco, Bahia, Brazil. Pleurodema diplolistrisPhyllomedusa, vol. 2, no. 2, p. 83-92. http://dx.doi.org/10.11606/issn.2316-9079.v2i2p83-92.
» http://dx.doi.org/10.11606/issn.2316-9079.v2i2p83-92 - Segalla, MV., Caramaschi, U., Cruz, CAG., Garcia, PCA. and Grant, T., HADDAD, CFB. and LANGONE, J., 2012. Brazilian amphibians: list of species. São Paulo. Available from: <http://www.sbherpetologia.org.br>. Access in: 6 Apr. 2013.
- TANTALEÁN, MV. and GARCÍA, L., 1989. Contribución al estudio de los helmintos parásitos de anfibios del Perú. Boletín de Lima, vol. 64, p. 69-78.
- Vicente, JJ., Rodrigues, HO., Gomes, DC. and Pinto, RM., 1990. Nematóides do Brasil 2 parte: nematóides de Anfíbios. Revista Brasileira de Zoologia, vol. 7, no. 4, p. 549-626. http://dx.doi.org/10.1590/S0101-81751990000400015.
» http://dx.doi.org/10.1590/S0101-81751990000400015
Publication Dates
-
Publication in this collection
Jan-Mar 2015
History
-
Received
22 May 2013 -
Accepted
12 Dec 2013