Resumen
Abstract
RESEARCH NOTE/ NOTA CIENTÍFICA
HELMINTH FAUNA OF TWO GECKO LIZARDS, HEMIDACTYLUS AGRIUS AND
LYGODACTYLUS KLUGEI (GEKKONIDADE), FROM CAATINGA BIOME,
NORTHEASTERN BRAZIL
HELMINTOFAUNA DE DOS LAGARTOS GECONÍDEOS, HEMIDACTYLUS AGRIUS Y
LYGODACTYLUS KLUGEI (GEKKONIDADE), EN EL BIOMA CAATINGA, NORESTE
DEL BRASIL
§ § §
Luciano Alves dos Anjos*, Castiele Holanda Bezerra , Daniel Cunha Passos , Djan Zanchi & Conrado Aleksander Barbosa
§,†
Galdino
Depto de Biologia e Zootecnia – FEIS, UNESP, campus Ilha Solteira, SP, Brasil. CEP 15385000.
mabuyasp@yahoo.com.br,
§-Núcleo Regional de Ofiologia da Universidade Federal do Ceará - NUROF-UFC Centro de Ciências, Universidade Federal
do Ceará, Campus do Pici, Bloco 905, CEP 60.455-760, Fortaleza, Ceará, Brazil. Email: castieleholanda@gmail.com;
biologodanielpassos@gmail.com; djanzanchi@yahoo.com.br
† - Programa de Pós-graduação em Zoologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, Avenida Dom
José Gaspar, 290, Bairro Coração Eucarístico, Belo Horizonte, Minas Gerais, Brasil. CEP 30535-901. e-mail:
galdinoc@gmail.com
Suggested citation: Anjos, L.A., Bezerra, C.H., Passos, D.C., Zanchi, D. & Galdino, C.A.B. 2011. Helminth fauna of two
gecko lizards, Hemidactylus agrius and Lygodactylus klugei (Gekkonidade), from Caatinga biome, northeastern Brazil.
Neotropical Helminthology, vol 5, nº 2, pp. 285-290.
This study presented data on helminth fauna of two gecko lizards, Hemidactylus agrius and
Lygodactylus klugei, from Caatinga biome in northeastern Brazil. It was found four helminth species
parasitizing H. agrius, cistacanth of Centrorhynchidae (Acanthocephala) and the nematodes
Physalopteridae (larvae), Parapharyngodon alvarengai (Pharyngodonidae) and Skrjabinelazia sp.
(Seuratidade). The host Lygodactylus klugei presented two helminth species, one individual of
Mesocoelium monas (Trematoda: Mesocoeliidae) in the small intestine and one encysted larvae of
Physalopteridae (Nematoda: Physalopteridae) attached at stomach wall. The lizard species showed a
low prevalence and low richness of helminths. Moreover, H. agrius presented a low intensity of
infection. The foraging mode, arboreal habit and a restricted composition of diet could favoring the low
prevalence, low infection rates and low richness of helminths found in these geckonid host species.
Keywords: gastrointestinal tract - Gekkota – Hemidactylus – helminth.
Este estudio presenta datos sobre la fauna de helmintos de dos lagartos geconídeos, Hemidactylus
agrius y Lygodactylus klugei, en el bioma caatinga en el noreste del Brasil. Hay cuatro especies de
helmintos parásitos de H. agrius, cistacanto de Centrorhynchidae (Acanthocephala) y nematodos
Physalopteridae (estadios larvarios), Parapharyngodon alvarengai (Pharyngodonidae) y
Skrjabinelazia sp. (Seuratidade). El hospedador Lygodactylus klugei presentó dos especies de
helmintos, un individuo de Mesocoelium monas (Trematoda: Mesocoeliidae) en el intestino delgado y
una larva enquistada de Physalopteridae (Nematoda: Physalopteridae) adjunta a la pared del estómago.
Las especies de lagarto mostraron una baja prevalencia y baja riqueza de helmintos. Además, H. agrius
Neotrop. Helminthol., 5(2), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043
285
mostró una baja intensidad de infección. El modo de búsqueda de alimento, el hábito arbóreo y la
composición de una dieta restringida pudieran haber favorecido la baja prevalencia, las bajas tasas de
infección y riqueza baja de helmintos que se encontraron en las especies hospedadoras.
Palabras clave: Gekkota – Hemidactylus – helminth - tracto digestivo.
INTRODUCTION
Knowledge on the aspects of parasitism by
helminths of neotropical lizards had increased in
last decade (e.g. Vrcibradic et al., 2000; Rocha et
al., 2003; Ávila & Silva, 2010). However, despite
the great diversity of the neotropical gekkotans
relatively few species have been surveyed for
parasites; two species of Gekkonidae (Anjos et al.,
2005; Anjos et al., 2007; Anjos et al., 2008; Ávila et
al., in press), one species of Sphaerodactylidae
(Ávila & Silva, 2010) and 12 species of
Phyllodactylidae (Ávila & Silva, 2010; Ávila et al.,
in press).
Recently the taxonomy and systematic of geckos
was revised (Gamble et al., 2008a; 2008b) and the
Gekkota infraorder now compriese seven lizards'
families. In South America three families are most
r e p r e s e n t a t i v e s , G e k k o n i d a d e ,
Spaherodactylidade and Phyllodactylidae
(Gamble et al., 2008b). Hemidactylus agrius
Vanzolini, 1978 (Gekkonidae) is a nocturnal lizard
associated to pristine environments (Rodrigues,
2003). This lizard was first considered to be
endemic to the Caatinga Biome (Vanzolini, 1978),
however recently Andrade et al. (2004) extended
the species range to the cerrado of Maranhão State.
Information on the species is scarce (Bezerra et al.,
2011; Passos & Borges-nojosa, in press).
Lygodactylus klugei (Smith et al., 1977)
(Gekkonidae) is a small-bodied diurnal and
arboreal lizard with a wide distribution along the
Caatinga (Vitt, 1995).
Herein we present data on helminth fauna of two
geckonid lizards, H. agrius and L. klugei from
Caatinga (Savanna-Like vegetation) from
Northeastern Brazil.
MATERIAL AND METHODS
Lizards were sampled at “Fazenda Experimental
do Vale do Curu (FEVC)” (03°49'0.03”S,
39°20'16.7”W, 45 msnm), Pentecoste municipality,
Ceará State, northeastern Brazil, between February
and March 2010. The FEVC covers 142 ha of
caatinga vegetation, characterized by a xerophytic,
deciduous, thornscrubland forest, typical of the
northeastern Brazil (Leal et al., 2005). This semi-
arid biome can experience in some years up to 11
month of dry condition.
Lizards were searched from ca. 0700h to ca. 1600h.
After capture lizards were euthanized with a lethal
injection of sodium thiopental, fixed in 10%
formalin and stored in 70% alcohol. In the
laboratory, lizards were necropsied and their body
cavity and digestive tract were checked under a
stereomicroscope for endoparasites.
Nematodes were cleared in lactophenol;
trematodes and cistacanth were stained with
hydrochloric carmine, dehydrated and cleared with
creosote. Helminths were mounted on temporary
slides, identified and deposited in the Coleção
Helmintológica do Instituto de Biociências
Botucatu, São Paulo State, Brazil, under the
acronym CHIBB 6724-6730. Parasitological
terminology used throughout and values of means
± 1 standard error follows that of Bush et al. (1997).
RESULTS
It was collected 56 H. agrius (19 adult male, 19
adult female and 18 juveniles) and 22 L. klugei.
For H. agrius were found four taxa of infecting
helminths: cistacanth of Centrorhynchidae
(Acanthocephala), larvae of Physalopteridae
(Nematoda), Parapharyngodon alvarengai
Freitas, 1957 (Nematoda: Pharyngodonidae), and
Skrjabinelazia sp. Sypliaxov, 1930 (Nematoda:
Seuratidae). Cistacanth were found only in lizards'
body cavity. Among nematodes Physalopteridae
larvae were found only in the small intestine, P.
alvarengai in the small and large intestine while
Skrjabinelazia sp. were found exclusively in the
large intestine.
Helminth fauna of two gecko lizards from brazil Anjos et al.
286
From the 56 individuals of H. agrius analyzed eight
lizards were infected by at least one parasite
(overall prevalence of 14.3%). Prevalence on the
adult male host were 26.3% (n = 5) and on adult
females were 15.8% (n = 3). There was no
significant difference in the overall prevalence
between females and males (Test Z for proportions;
Z = 0.40; P = 0.70). No juvenile lizard was
parasitized. The mean intensity of infection was
1.9 ± 0.3 parasites per host. Nematode P.
alvarengai was the most prevalent (5/8, P =
62.5%), with all other helminths present in a single
lizard host.
From the 22 individuals of L. klugei, just two
lizards were found harboring helminths (overall
prevalence of 9.1%). It was found two helminth
species, one individual of Mesocoelium monas
(Rudolphi, 1819) (Trematoda: Mesocoeliidae) in
the small intestine and one encisted larvae of
Physalopteridae (Nematoda: Physalopteridae)
attached at stomach wall.
DISCUSSION
The helminth fauna of H. agrius from FEVC had
been also found infecting other neotropical lizards
species, and such infections are not restricted to the
gekkotans. Cistacanth of Centrorhynchidae was
found parasitizing the gekkonid H. mabouia, in that
case with a high prevalence and intensity of
infection (Anjos et al., 2005). Larvae of
Physaloptera have been found in many lizards
from different families (Ávila et al., 2010), usually
these lizards act as intermediate host (Anderson,
2000). Parapharyngodon alvarengai have been
found in lizards Trachylepis atlantica, Ameiva
ameiva and in Amphisbaena ridleyi (Ávila & Silva,
2010). Species of the genus Skrjabinelazia is a
common parasite of gekkotan lizards from Old
World (Lhermitte et al., 2008; Goldberg et al.,
2011). Nonetheless, species of Skrjabinelazia
were found also parasitizing the neotropical
Gonatodes humeralis (Phyllodactylidade) in North
Brazil (Vicente et al., 1993).
Additionally, Skrjabinelazia intermedia was found
infecting the teiid Cnemidophorus nativo in the
northeast Brazil (Menezes et al., 2004). Since
there is no previous study addressing the helminth
parasitism for H. agrius this lizard species is here
reported as a new host for Centrorhynchidae
c i s t a c a n t h , P h y s a l o p t e r i d a e l a r v a ,
Parapharyngodon alvarengai, and Skrjabinelazia
sp.
The existing information on parasitic aspects from
Neotropical gecko lizards (Gekkonidae,
Sphaerodactylidae and Phyllodactylidae) accounts
for a relatively low overall prevalence and richness
of helminth supracommunity ranging from one to
four species of parasite (Vicente et al., 1993; Ávila
& Silva, 2010). The exception occurs in H.
mabouia an exotic invader species, which acquired
helminth fauna of native host lizards (Anjos et al.,
2005; Anjos et al., 2007).
Several aspects of the biology and the ecology of
lizards such as, foraging mode, use of microhabitat,
body size, pregnancy, diet composition and
ontogeny (Aho, 1990; Combes, 2005; Poulin,
2007) play a key role in the acquisition of the
associated helminth fauna. The low richness of
helminths and the low prevalence and infection
rates found for H. agrius might be related to the
species foraging mode and also to intrinsic features
of each lizard species.
In spite of H. agrius has a generalist diet in terms of
prey composition; orthopterans were the
predominant food item ingested by the individuals
from FEVC (C. Galdino, in prep.). Thereby, such
bias in the specialization on prey consumption
should be a factor contributing to the low rate of
parasites acquisition in the population. Is also
important to point out that the composition of the
helminth fauna of H. agrius was dominated by
monoxenic life-cycle parasites (Anderson, 2000).
Thus, behavioral components as the selection of
foraging sites with low occurrence of parasites
might be of importance in determining low
infection in the species, as pointed by the theory of
Combe's filter (Combes, 2005).
Lygodactylus klugei is an arboreal lizard, and this
trait could reduce their chances to be infected by
helminths. The cestode M. monas have been
registered in more than a hundred species of
reptiles and amphibians (Travassos et al., 1969;
Goldberg et al., 2005; Ávila & Silva, 2010) in
almost all continents and this study found a new
host species for the parasite.
Neotrop. Helminthol., 5(2), 2011
287
The low prevalence and intensity of infection of
these geckonid lizards are according to other
studies focusing on helminth fauna of gekkotans
(except H. mabouia). The movement rate, arboreal
habit and a trend of specialization on prey
consumption usually reflect on their depauperated
helminth fauna, composed primarily by species
monoxenic and commons.
ACKNOWLEDGEMENTS
We thank the administrative staff of the Fazenda
Experimental do Vale do Curu for logistical
support and for the permission to work at the area.
We also thank R. J. da Silva and people from
LAPAS (Laboratory of Wildlife Parasitology) for
the facilities at the lab. This Study were supported
by grant from Conselho Nacional de
Desenvolvimento Científico e Tecnológico
(CNPQ) proc. 35.0241/2008-2 and from Fundação
Cearense de Apoio ao Desenvolvimento Científico
e Tecnológico conv. 22/2007 to C. A. B. Galdino.
Currently C.A.B. Galdino benefits from a grant
from CNPq (postdoctoral fellowship proc.
151663/2010-6). LA Anjos received grants from
FAPESP (postdoctoral fellowship, proc.
20.08/50417-7). D Zanchi is grateful to Fundação
Cearense de Apoio ao Desenvolvimento Científico
e Tecnológico for the grant BMD-0008-
00060.01.14/10 and from Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior. We
also thank Instituto Chico Mendes de Conservação
da Biodiversidade (ICMBio) for collecting
permission (license nº 21551-1).
BIBLIOGRAPHIC REFERENCES
Aho, J. 1990.
Anderson, R (ed.). 2000.
Andrade, GV, Gomes, JO, Freire, P C & Cruz, LD.
2 0 0 4 .
Helminth communities of amphibians
and reptiles: Comparative approaches to
understanding patterns and processes.
p.157 - 195. In: Esch, G W, Bush, A O &
Aho, J M (eds.). Parasite communities:
patterns and processes. New York, USA.
Chapman and Hall.
Nematode parasites of
vertebrates: Their development and
transmission. CABI.
G e o g r a p h i c D i s t r i b u t i o n .
Hemidactylus agrius. Herpetological Review,
vol.35, pp. 287.
The alien and
native pentastomids fauna of an exotic lizard
population from Brazilian Northeast.
Parasitology Research, vol.101, pp. 627-
628.
A
Pentastomids
infecting an invader lizard, Hemidactylus
mabouia (Gekkonidae) in northeastern
Brazil. Brazilian Journal of Biology, vol.68,
pp. 611-615.
Helminths of the exotic lizard
Hemidactylus mabouia from a rock outcrop
area in southeastern Brazil. Journal of
Helminthology, pp. 307-313.
Helminths
from seven species of Lizards (Reptilia:
Squamata) at the Cerrado of Mato Grosso
do Sul State, Brazil. Comparative
Parasitology, vol.77, pp. 67-71.
Nematodes
of lizards (Reptilia: Squamata) from
Caatinga Biome, Northeastern Brazil.
Comparative Parasitology.
Checklist of
helminths from lizards and amphisbaenians
(Reptilia, Squamata) of South America.
Journal of Venomous Animals and Toxins
including Tropical Diseases, vol.16, pp.
543-572.
Hemidactylus
agrius (Country-leaf t oa d g ec ko )
reproduction. Herpetological Review,
vol.42, pp. 274-275.
Parasitology meets ecology on its own
terms: Margolis et al. revisited. The Journal
of parasitology, vol.83, pp. 575-583.
Anjos, LA, Almeida, WO, Vasconcellos, A, Freire,
EMX & Rocha, CFD. 2007.
njos, LA, Almeida, WO, Vasconcellos, A, Freire,
EMX & Rocha, CFD. 2008.
Anjos, LA, Rocha, CFD, Vrcibradic, D & Vicente,
J J. 2005.
Ávila, R, Souza, F & da Silva, R. 2010.
Ávila, RW, Anjos, L A, Ribeiro, SC, Morais, DH,
Silva, RJ & Almeida, WO 2011.
Ávila, RW & Silva, RJ. 2010.
Bezerra, CH, Passos, DC, Mesquita, PCMD &
Borges-nojosa, DM. 2011.
Bush, A, Lafferty, K, Lotz, J & Shostak, A. 1997.
Helminth fauna of two gecko lizards from brazil Anjos et al.
288
Combes, C (ed.). 2005
Gamble, T, Bauer, A M, Greenbaum, E & Jackman,
TR. 2008a.
Gamble, T, Bauer, AM, Greenbaum, E & Jackman,
TR. 2008b.
Goldberg, SR, Bursey, CR, Bauer, AM, de Silva, A
& Austin, CC. 2011.
Goldberg, SR, Bursey, CR & Telford, SR. 2005.
Leal, I R, Silva, J M C, Tabarelli, M & Lacher, T E J.
2005.
Lhermitte, N, Bain, O & Virga, A. 2008.
Skrjabinelazia rizzoi n. sp.
Menezes, VA, Vrcibradic, D, Vicente, JJ, Dutra, G
F& Rocha, CFD. 2004.
. The art of being a parasite.
University of Chicago Press, Chicago.
Evidence for Gondwanan
vicariance in an ancient clade of gecko
lizards. Journal of Biogeography, vol.35, pp.
88-104.
Out of the blue: a novel, trans-
Atlantic clade of geckos (Gekkota,
Squamata). Zoologica Scripta, vol.37, pp.
355-366.
Helminths from 9
Species of Geckos (Squamata: Gekkonidae)
from Sri Lanka. Comparative Parasitology,
vol.78, pp. 359-366.
Metazoan endoparasites of four species of
lizards, Gehyra mutilata, Hemidactylus
frenatus (Gekkonidae), Mabuya cumingi,
Mabuya multifasciata (Scincidae), and one
species of snake, Ramphotyphlops braminus
(Typhlopidae), from the Philippine Islands.
Comparative Parasitology, vol.72, pp. 88-
101.
Changing the course of biodiversity
conse rvati on in t he Caa ti nga o f
Northeastern Brazil. Conservation Biology,
vol.19, pp. 701-706.
(Nematoda:
Seuratoidea) from a Sicilian lacertid, with
comments on specific and biological
diversity in the genus. Parasite, vol.15, pp.
45-52.
Helminths infecting
the parthenogenetic whiptail lizard
Cnemidophorus nativo in a restinga habitat
of Bahia State, Brazil. Journal of
Helminthology, vol.78, pp. 323-328.
Passos, DC & Borges-nojosa, DM in press.
Poulin, R (ed.). 2007.
Rocha, CFD, Vrcibradic, D, Vicente, JJ & Cunha-
Barros, M. 2003.
Rodrigues, MT. 2003.
Travassos, L, Freitas, JFT & Kohn, A. 1969.
Vanzolini, PE. 1978.
Vicente, J J, Rodrigues, HDO, Gomes, DC & Pinto,
R M. 1993.
Vitt, L J. 1995.
Vrcibradic, D, Cunha-Barros, M, Vicente, JJ,
Galdino, CAC, Hatano, F H, Van Sluys, M &
Rocha, CFD. 2000.
Morphometry of hatchlings of the gecko
H e m i d a c t y l u s a g r i u s
(Squamata:Gekkonidae) from a semi-arid
area of northeastern Brazil. Herpetology
Notes.
Evolutionary ecology of
parasites. Princeton UP, Princeton, NJ.
Helminths infecting
Mabuya dorsivittata (Lacertilia, scincidae)
from a high-altitude habitat in Itatiaia
National Park, Rio de Janeiro State,
southeastern Brazil. Brazilian Journal of
Biology, vol.63, pp. 129-132.
Herpetofauna da caatinga.
p.181-236. In: Leal, I R, Tabarelli, M &
Silva, J M C (eds.). Ecologia e conservação
da Caatinga. UFPE. 181-236.
Trematódeos do Brasil. Memorias do
Instituto Oswaldo Cruz, vol.67, pp. 1 - 886.
On South American
Hemidactylus (Sauria, Gekkonidae). Papéis
Avulsos de Zoologia, vol.31, pp. 307-343.
Nematóides do Brasil. Parte III:
nematóides de répteis. Revista Brasileira de
Zoologia, vol.10, pp. 19-168.
The ecology of tropical lizards in the
caatinga of northeast Brazil. Occasional
Papers of the Oklahoma Museum of Natural
History, vol.1, pp. 1-29.
Nematode infection
patterns in four sympatric lizards from a
restinga habitat (Jurubatiba) in Rio de
Janeiro state, southeastern Brazil.
Amphibia-Reptilia, vol.21, pp. 307-316.
Neotrop. Helminthol., 5(2), 2011
289
Correspondence to author /Autor para
correspondência:
Luciano Alves dos Anjos.
Depto de Biologia e Zootecnia – FEIS, UNESP,
campus Ilha Solteira, SP, Brasil. CEP 15385000.
E-mail/ correo electrónico:
mabuyasp@yahoo.com.br
Received October 14, 2011.
Accepted October 31, 2011.
Helminth fauna of two gecko lizards from brazil Anjos et al.
290
