ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2018, 12(2), jul-dic:243-259.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
COMPONENT COMMUNITY OF THE PARASITIC METAZOANS OF THE AFRO-AMERICAN
HOUSE GECKO HEMIDACTYLUS MABOUIA (MOREAU DE JONNÈS, 1818) (SQUAMATA:
GEKKONIDAE) FROM THE JUNGLE OF PERU
COMPONENTE COMUNITARIO DE LOS METAZOOS PARÁSITOS DEL GECKO-CASERO
TROPICAL HEMIDACTYLUS MABOUIA (MOREAU DE JONNÈS, 1818) (SQUAMATA:
GEKKONIDAE) DE LA SELVA DEL PERÚ
1 2 3 3
David Minaya-Angoma ; Carlos Mendoza-Vidaurre ;Jhon Chero-De la Cruz ; Gloria Saez-Flores ;
4 1,5
Reinaldo José da Silva & José Iannacone
ABSTRACT
The purpose of this study was to evaluate the component community of the parasitic metazoans of the
Afro-American house gecko Hemidactylus mabouia (Moreau de Jonnès, 1818) from the jungle of Peru.
Ninety-one specimens of H. mabouia from seven localities of San Martín and Huánuco were collected
from April to June 2015. The parasites were collected and processed according to standard protocols.
Eighty-five percent of the geckos were infected with at least one parasite species and a total of 1,120
parasite specimens were collected with a prevalence of 90%. The parasitic fauna of H. mabouia was
composed of 11 species, as follow: six species of nematodes - Oswaldocruzia aff. brasiliensis Lent et
Freitas, 1935, Spauligodon sp. Skrjabin, Schikhobalova & Lagodovskaja, 1960, Parapharyngodon sp.
Chatterji, 1933, Physaloptera sp. Rudolphi, 1819, Acuariidae gen. sp. Railliet, Henry & Sisoff, 1912, and
one species not identified of nematode; one cestode species - Oochoristica vanzolinii Rego & Rodrigues,
1965; two trematode species - Paradistomum sp.1 Kossack, 1910, Paradistomum sp.2 Kossack, 1910;
one pentastomid species - Raillietiella hebitihamata Self & Kuntz, 1960; and one mite species - Geckobia
hemidactyli Lawrence, 1936. The three parasites with the higher prevalence (P) and mean abundance
(MA) were G. hemidactyli (P = 45.05%, MA = 4.16), Spauligodon sp. (P = 37.36%, MA = 2.64), and
Raillietiella hebitihamata (P = 32.97%, MA = 2.3). Single and multiple parasitic infections with at least
one, two, three, four, and five species of parasites were observed in 25, 35, 15, 6, and 1 hosts, respectively.
Neotropical Helminthology
243
Volume12,Number2(jul-dec2018)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
1Laboratorio de Ecología y Biodiversidad Animal, Facultad de Ciencias Naturales y Matemática,
Universidad Nacional Federico Villarreal - UNFV. El Agustino, Lima, Perú.
2Universidad Alas Peruanas – UAP. Tarapoto, San Martín, Perú.
3Laboratorio de Parasitología General y Especializada, Facultad de Ciencias Naturales y Matemática,
Universidad Nacional Federico Villarreal - UNFV. El Agustino, Lima, Perú.
4São Paulo State University (Unesp), Institute of Biosciences, Department of Parasitology, Laboratory
of Parasitology of Wild Animals. Botucatu, São Paulo, Brasil.
5Laboratorio de Parasitología. Facultad de Ciencias Biológicas. Universidad Ricardo Palma. Santiago
de Surco, Lima, Perú. Corresponde Author: E-mail: joseiannacone@gmail.com
244
Neotropical Helminthology, 2018, 12(2), jul-dic
A positive association was observed between the prevalence of infection of R. hebitihamata and
Parapharyngodon sp. with the total length (TL) of the gecko. There was also a relationship between TL of
H. mabouia and MA and mean intensity of Spauligodon sp. The cestode O. vanzolinii and the pentastomid
R. hebitihamata are first geographical record for Peru. Non-metric multidimensional scaling (NMDS) and
the relationship between community composition and explanatory variables (host length, sex, and
locality) were examined by permutational analysis of variance (PERMANOVA) applied to species
abundances which showed high homogeneity among metazoan parasite communities of H. mabouia.
Keywords: gecko – helminths – Neotropic – parasitology – Peru
La finalidad de este estudio fue evaluar el componente comunitario de los metazoos parásitos del gecko-
casero tropical Hemidactylus mabouia (Moreau de Jonnès, 1818) de la selva del Perú. Se colectaron en
siete localidades de San Martín y de Huánuco, noventa y un especímenes de H. mabouia durante abril a
junio del 2015. Los parásitos fueron colectados y procesados siguiendo protocolos estándares. El 89% de
los geckos estuvieron infectados con al menos una especie de parásito, se colectaron un total de 1,120
especímenes parásitos. La fauna parasitaria de H. mabouia estuvo compuesta de 11 especies, como sigue:
Seis especies de nematodos Oswaldocruzia aff. brasiliensis Lent et Freitas, 1935, Spauligodon sp.
Skrjabin, Schikhobalova & Lagodovskaja, 1960, Parapharyngodon sp. Chatterji, 1933, Physaloptera sp.
Rudolphi, 1819, Acuariidae gen. sp. Railliet, Henry & Sisoff, 1912 y una especie no identificada de
nemátoda; una especie de cestodo Oochoristica vanzolinii Rego & Rodrigues, 1965, dos especies de
trematodos Paradistomum sp.1 Kossack, 1910, Paradistomum sp.2 Kossack, 1910; una especies de
pentastómido Raillietiella hebitihamata Self & Kuntz, 1960; y una especie de ácaro Geckobia hemidactyli
Lawrence, 1936. Los tres parásitos con la más alta prevalencia (P) y abundancia media (AM) fueron G.
hemidactyli (P = 45.05 %, AM = 4.16), Spauligodon sp. (P = 37.36 %, AM = 2.64) y R. hebitihamata (P=
32.97 %, AM = 2.3). Las infecciones parasitarias individuales y múltiples con al menos una, dos, tres,
cuatro y cinco especies de parásitos fueron observadas en 25, 35, 15, 6 y 1 hospederos, respectivamente.
Se observó asociación positiva entre la prevalencia de infección de R. hebitihamata y Parapharyngodon
sp. con la longitud total (LT) del gecko. También se observó relación entre la LT de H. mabouia y la AM e
intensidad media de Spauligodon sp. El cestodo O. vanzolinii y el pentastómido R. hebitihamata son
reportadas por primera vez a la composición de la fauna de parásitos de Perú. El escalamiento
multidimensional no métrico (NMDS) y la relación entre la composición de la comunidad y variables
explicativas (longitud, sexo del hospedero y localidad) fueron examinadas por el análisis de varianza de
permutación (PERMANOVA) aplicadas a la abundancia de especies y mostraron una alta homogeneidad
entre los parásitos metazoos de las comunidades de H. mabouia.
RESUMEN
Palabras clave: gecko – helmintos – Neotrópico – parasitología – Perú
The research focused on the study of parasite
communities in exotic reptiles is scarce both in
America and even more in Peru (Goldberg et al.,
1995; Hanley et al., 1995; Goldberg & Bursey,
INTRODUCTION 2000; Criscione & Font, 2001; Bursey et al., 2005).
However, parasitological studies focused on new
host records, localities, and descriptions of several
new species of helminths that infect reptiles in
South America have been increasing in recent years
(Goldberg et al., 2004; Ávila & Silva, 2010). Many
of these studies date back to 1920 when Lauro
Minaya-Angoma et al.
A total of 91 gecko specimens were collected from
April to Juny 2015, in the following locations: San
Martín Department, Bellavista Province
(Bellavista District: 7°02'25" S 76°34'23" W, n =
5), province of Lamas (districts of Barranquita:
6°14'35" S 76°02'08" W, n = 11, and Lamas:
6°25'06" S 76°31'14" W, n = 7), province of San
Martín (districts of Morales: 6°28'45" S 76°24'09"
W, n = 8; of Tarapoto: 6°29'49" S 76°23'53" W, n =
51, and of the Banda de Shilcayo: 6°29'46" S
76°21'47" W, n = 1), and finally in the Department
of Huánuco, Province Leoncio Prado (9°17'02" S
75°59'05" W, n = 8), Peru. The technique of direct
detection or search by visual encounter was used.
The individuals were captured and euthanized in
the lethal chamber with chloroform. The
identification was made by the Department of
Herpetology of the Natural History Museum of San
Marcos. Data of total length (TL) in cm and sex (S)
were taken for all studied individuals. The
collection was authorized by Directorial
Resolution N°024-2014-SERFOR-DGGSPFFS.
Collection, fixation, and identification of
parasites
For the collection of the endoparasites, coelomic
cavity, lungs, stomach, small intestine, large
intestine, gonads, heart, gallbladder, liver, and
spleen were surveyed. The nematodes were fixed
in 70% hot ethyl alcohol; the pentastomids,
cestodes and trematodes were fixed under slight
pressure of coverslip for 24 h. After, they were
preserved in 70% ethyl alcohol and placed in
labeled vials for transfer to the Laboratory
(Lamothe, 1997). For the collection of
ectoparasites, the skin of the geckos was checked.
All the mites were stored in 70% ethyl alcohol for
later identification.
For their taxonomic study, cestodes and trematodes
were stained in Semichon acetic carmine and
mounted in balsam of Canada; the nematodes were
cleared in a mixture of alcohol-phenol to observe in
detail structures of taxonomic importance; the
pentastomids were mounted on slides and treated
with a Hoyer medium (Lamothe, 1997). The
photographs and measurements were made with
the help of a Leica DM500 microscope with Leica
Application Suite software version 3.1.0.
The nomenclature and classification of parasite
Travassos and collaborators presented important
contributions to this field (Travassos, 1920;
Travassos, 1931; Ávila & Silva, 2010).
In Peru, the first studies related to the parasitology
of reptiles start with the work of Baylis (1926) who
described for the first time the nematode
Thubunaea parkeri Baylis 1926 parasitizing the
lizards Microlophus occipitalis (Peters, 1871) and
Dicrodon heterolepis (Baylis, 1926).
Hemidactylus mabouia (Moreau de Jonnès, 1818)
(Squamata: Gekkonidae) is a species of exotic
gecko of African origin that is well established and
widely distributed in South America (Ávila-Pires,
1995). Hemidactylus mabouia is very common in
Brazil, where it is usually associated with man-
made structures and is frequently found around
human dwellings, both in rural areas and urban
areas (Vanzolini, 1978; Ávila-Pires, 1995). In
relation to its conservation status, it is not cataloged
by the IUCN (International Union for the
Conservation of Nature) and nor by CITES
(Convention on International Trade in Endangered
Species of Wild Fauna and Flora). GISS (2018)
cited as an invasive exotic species that displaces
and feeds on native geckos.
Many of the studies related to the parasitic fauna of
this reptile have been carried out in Brazil where
fifteen taxa of parasitic helminths have been
reported (two species of trematodes, one of
cestode, eleven of nematodes and one of
acanthocephalan), pentastomids, and a mite
species (Martínez-Rivera et al., 2003; Anjos et al.,
2005; Anjos et al., 2008; Ávila & Silva, 2010;
Ávila & Silva, 2011; Sousa et al., 2014).
The objective of this study was to evaluate the
component community of the parasitic metazoans
of the Afro-American house gecko H. mabouia of
the jungle of Peru, as well as to determine the
association between the main parasitic indexes
with some biometric parameters of this host.
Area of study, capture, and identification of
lizards
245
Neotropical Helminthology, 2018, 12(2), jul-dic
MATERIAL AND METHODS
Metazoans of the Afro-American house gecko
was used to determine the ratio of the TL of the host
to the MA and MI of each parasitic species. In all
cases, the normality of the data was verified using
the Kolmogorov-Smirnov test with the Lillierfors
modification and the variance homocentricity
based on the Levene test (Zar, 2014).
2 x 2 contingency tables were used to calculate the
degree of association between the sex of the host
and the prevalence of each parasite using Chi-
2
squared (X ) and the Likelihood Ratio test. The
Student t-test was used to compare the MA and MI
of each parasite and the sex of the host. The
analysis of the parasites in relation to the size and
sex of the host was made only for the species with
prevalence greater than 10% (Esch et al., 1990).
Dendrograms were performed with the qualitative
Jaccard similarity index and the Morisita-Horn
quantitative index for paired association data
between the H. mabouia parasites of the San
Martin and Huánuco regions, Peru. The level of
significance was evaluated at a level of alpha =
0.05. For the determination of descriptive and
inferential statistics, the statistical package IBM
SPSS Statistics 20 was used.
The non-metric multi-dimensional scaling
(NMDS), an ordination technique, was used to
study pattern in the parasite community structure
based on the abundance of parasite species. A
similarity matrix was constructed based on the
Bray–Curtis measure. The abundance of infection
of each parasite species in each host and its relation
to length, sex, and locality of the host were
analyzed through one-way analysis of variance
with a non-parametric permutational ANOVA
(PERMANOVA) test (Anderson, 2001; Míguez-
Lozano et al., 2012).
Ethical aspects
The procedures for collecting the diversity of
parasitic fauna in the gecko followed the guidelines
of the "Institutional Animal Care and Use
Committee" (IACUC) (APA, 2012), minimizing
the number of organisms used, repetitions and
using the three Rs "Rs-replacement, reduction, and
refinement", and resolution 2558-2018-CU-UNFV
that includes the code of ethics for research at the
National University Federico Villarreal (UNFV).
For the management of the parasitic fauna, the
guidelines of the protection and animal welfare law
246
Neotropical Helminthology, 2018, 12(2), jul-dic
species were carried out following the taxonomic
keys of Gibson et al. (2008) for trematodes, Khalil
et al. (1994) for cestodes, Anderson (2000) for
nematodes, and Krantz (1978) for the mites. The
specimens of the parasite species were deposited in
the Helminthological Collection of the Institute of
Biosciences (CHIBB) of São Paulo State
University (UNESP), municipality of Botucatu
under registration numbers CHIBB 7813-7818.
Statistical analysis
The data of total length (TL, in cm) and sex (S)
were plotted in a Box plot. Ecological
parasitological indexes: prevalence (P, %), mean
abundance (MA), and mean intensity (MI) of
infection were calculated following the indications
of Bush et al. (1997) and Bautista-Hernández et al.
(2015). The P, MA, and MI were determined for
each of the parasites registered in the geckos. The
index of specific importance (ISI) calculated as the
importance of each parasitic species in the
ecological assembly was used. ISI = P + (MA x
100) in order to obtain an integrated infection index
of both ecological descriptors (Bursey et al., 2001;
Iannacone & Alvariño, 2013).
The frequency of dominance was determined as the
number of times a parasitic species is dominant in
all the hosts examined and the frequency of relative
dominance as the number of individuals of a taxon
on the total number of individuals of all the taxa in
the parasitic infracomunity (Rohde et al., 1995).
Individual (monospecific) and multiple parasitic
infections (two to three parasite species) were
determined.
For the case of parasitic species with prevalence
greater than 10% (Esch et al., 1990), three
aggregation indices were applied: Dispersion (Id),
Poulin Discrepancy Index (PDI), and K of the
negative binomial equation with its respective
2
value of X (Bego & Von Zuben, 2010). The
Quantitative Parasitology 3.0 package was used
(Rózsa et al., 2000). These indices were calculated
in order to show if parasitic helminths had a
distribution: (1) contagious, aggregated or
conglomerate; (2) uniform-regular or (3)
randomized.The Pearson correlation coefficient
was used to evaluate the association between the
TL versus the P of infection, previously
transforming the values of P to the square root of
arcosene. The Spearman correlation coefficient
Minaya-Angoma et al.
parasites collected in H. mabouia were presented in
Table 1.
A total of 1,120 parasites was recovered. Species
richness was represented mostly by nematodes (n =
6) which were collected from the intestine of the
geckos. Geckobia hemidactyli is the ectoparasite
with the highest abundance (379 individuals),
which was found infecting 41 hosts (P = 45.05%)
followed by the nematode Spauligodon sp (N = 240
individuals, n = 34 hosts, P = 37.36%).
The percentage of parasitized geckos with at least
one parasite species was 90.11% (n = 82). In the
case of specific infections, 27.47% (n = 25) was
infected with a single species of parasite, 38.46%
(n = 35) with two species, 16.48% (n = 15), with
three species, 6.59% (n = 6), with four species, and
1.11% (n = 1) with five species (Table 2).
The highest specific importance, frequency of
dominance and relative dominance were also for G.
hemidactyli and Spauligodon sp. (Table 3).
Aggregation indices: Dispersion (Id), Poulin
Discrepancy Index (PDI) and K of the negative
binomial equation indicate a conglomerate or
contagious type distribution for parasites with
prevalence greater than 10% (Table 3).
Table 4 shows a positive correlation between the
prevalence of R. hebitihamata and the length of its
hosts. The same degree of association is observed
between the P% of Parapharyngodon sp. and the
TL of H mabouia. The MA and MI of O. vanzolinii
and Spauligodon sp. were also positively related to
the gecko TL. In relation to the sex of the host, this
was only associated with the P and AM of the
nematode Parapharyngodon sp., not finding
females parasitized with this parasite.
The level of similarity between the parasitic
species is observed in Figure 2, which indicates
that there is a low similarity (below 50%) among
the parasites associated with H. mabouia. The
highest similarity at a qualitative level (presence
and absence) is between G. hemidactyli and R.
hebitihamata and at quantitative levels between G.
hemidactyli and Spauligodon sp. Paradistomum
geckonum and Paradistomum sp. are the second
group that forms most similarly, which show
similar similarities at a quantitative and qualitative
level.
of Peru were followed (Law No. 30407: Article
19). The collection of the parasitic fauna is
indicated by the SERFOR (National Forestry and
Wildlife Service) of Peru that establishes the
guidelines for the scientific investigation of flora
and/or wild fauna (Resolution of Executive
Direction Nº060-2016 SERFOR-DE). For the field
collection of the geckos, the impact on the
abundance of species was minimized so that it is
minimal (Costello et al., 2016).
Conflicts of interest
The authors declare that they do not present any
conflict of interest.
Ninety-one specimens of H. mabouia were
examined, of which 20.9% (n = 19) were females
and 79.1% (n = 72) were males. The individuals
showed an average total length (TL) of 11.54 ± 2.09
cm; the males showed a TL of 11.96 ± 1.96 cm and
the females a TL of 9.95 ± 1.84 cm (Fig. 1). The t-
test for independent samples accepts the null
hypothesis assuming the equality of variances and
in which the averages of the TL of the male and
female geckos do not have significant differences
(F = 0.031, p = 0.86, t = 4, 02, n = 91).
Levene
The component community was composed of 11
parasite species: the nematodes Oswaldocruzia aff.
b r a s i l i e n s i s L e n t & F r e i t a s , 1 9 3 5
(Diaphanocephalidae), Spauligodon sp. Skrjabin,
S c h i k h o b a l o v a & L a g o d o v s k , 1 9 6 0
(Pharyngodonidae), Parapharyngodon sp.
Chatterji, 1933 (Pharyngodonidae), Physaloptera
sp. Rudolphi, 1819 (Physalopteridae), a larval
nematode of the family Acuariidae Railliet, Henry
& Sisoff, 1912, and a nematode cyst in Liver; the
trematodes Paradistomum sp.1 Kossack, 1910
(Dicrocoeliidae),and Paradistomum sp.2 Kossack,
1910 (Dicrocoeliidae); the cestode Oochoristica
v a n z o l i n i i R ego & Rod rig u es , 1 9 65
(Linstowiidae); the pentastomid Raillietiella
h e b i t i h a m a t a S e l f & K u n t z , 1 9 6 0
(Cephalobaenidae); and the mite Geckobia
hemidactyli Lawrence, 1936 (Pterygosomatidae),
which was the only ectoparasite species. The site of
infection/infestation, stage, prevalence, mean
abundance and mean intensity of infection of the
247
Neotropical Helminthology, 2018, 12(2), jul-dic
RESULTS
Metazoans of the Afro-American house gecko
PERMANOVA analysis confirmed the low
heterogeneity among metazoan parasites
communities of H. mabouia (Table 5).
Figure 5, 6 and 7 display the NMDS ordination plot
of the 91 metazoan parasites communities from H.
mabouia. The NMDS ordination suggests a high
degree of homogeneity across communities. The
248
Neotropical Helminthology, 2018, 12(2), jul-dic
Figure 1. Box plot diagram for the total length (in cm) of the total of Geckos, males, and females of Hemidactylus mabouia
collected in the region of San Martin and Huanuco, Peru.
Figure 2. Dendrogram with the Jaccard similarity index (left) and the Morisita-Horn quantitative index (right) for paired data of
association between Hemidactylus mabouia parasites of San Martin and Huánuco, Peru. GH=Geckobia hemidactyli,
RF=Raillietiella hebitihamata, PG=Paradistomum sp1., Psp=Paradistomum sp2., OV=Oochoristica vanzolinii,
OB=Oswaldocruzia aff. brasiliensis, SP=Spauligodon sp., PA=Parapharyngodon sp., PH=Physaloptera sp., AC=Acuariidae,
and QN=nematode cyst.
Minaya-Angoma et al.
249
Neotropical Helminthology, 2018, 12(2), jul-dic
Figure 3. A. Raillietiella hebitihamata, B-C. Oochoristica vanzolinii, B. Scolex, C. Madure proglottid, D. Paradistomum sp.1.
and E. Geckobia hemidactyli.
Metazoans of the Afro-American house gecko
250
Neotropical Helminthology, 2018, 12(2), jul-dic
Figura 4. A. Parapharyngodon sp., B-C. Spauligodon sp, D. Physaloptera sp, E. Oswaldocruzia aff. brasiliensis.
Minaya-Angoma et al.
251
Neotropical Helminthology, 2018, 12(2), jul-dic
Figure 5. Non-metric multidimensional scaling (NMDS) plots results of all lengths (1, 6.0 cm -8.0 cm. 2, 8.1 cm 10.0 cm. 3, 10.1
cm -12.0 cm 4, 12.1-14.0cm 5, >14cm) in terms of their parasitic abundance. Bray Curtis similarity. 2D Stress = 0.58. 1 =•. 2 = . 3
= . 4 =∆. 5= .
Figure 6. Non-metric multidimensional scaling (NMDS) plots results of sex (1, males. 2, females) in terms of their parasitic
abundance. Bray Curtis similarity. 2D Stress = 0. 58. 1= ■. 2= .
Metazoans of the Afro-American house gecko
252
Neotropical Helminthology, 2018, 12(2), jul-dic
DISCUSSION
Figure 7. Non-metric multidimensional scaling (NMDS) plots results of localities (1, Leoncio Prado (Huánuco). 2, San Martín
(San Martín). 3, Lamas (San Martín). 4, Bellavista (San Martín)) in terms of their parasitic abundance. Bray Curtis similarity. 2D
Stress = 0. 58. 1= ■. 2= . 3 =♦. 4 =∆.
In this study, 11 species of parasites were recorded
parasitizing the H. mabouia gecko collected in San
Martin and Huánuco, Peru. To date, studies have
been carried out in Brazil where 18 taxa of
parasites have been reported: 15 helminths, 2
pentastomids and 1 mite (Anjos et al., 2008, Ávila
& Silva, 2010, Paredes-León et al., 2013). In
comparison to that reported by Anjos et al. (2008),
where on l y 5 s p ecies of h e lmint h s (1
acanthocephalans and 4 nematodes) were recorded
in 291 individuals of H. mabouia collected in
southeastern Brazil, in this study the species
richness of helminths is higher (n = 9) for a smaller
population size (n = 91) to the one studied by Anjos
et al. (2008). In this same work, the degree of
association of the parasitic prevalence with the TL
of the host was evaluated and no association
between both was detected. In contrast, in the
present study, it was observed that the TL of the
host significantly influences the parasitism of the
species of R. hebitihamata and Parapharyngodon
sp.
Another study addressing the parasitic fauna of H.
mabouia is the one carried out by Sousa et al.
(2014) in which it records 6 parasitic species
(between helminths and pentastomids) for 76
individuals collected in Northeast Brazil. This is
still lower than what was recorded in our study. It is
important to point out that in the studies conducted
by Anjos et al. (2008) and Sousa et al. (2014)
trematode species were not recovered.
Pterygosomatidae mites have a worldwide
distribution and are comprised of 10 genera and
177 species, some of which have high specificity
towards the host. Within Pterygosomatidae, the
genus Geckobia Mégnin, 1878 is the one that has
the widest geographic distribution and the greatest
richness with 72 parasitic species of Geckonidae
lizards (Quiroz-Gutiérrez et al., 2015). In this study
we found G. hemidactyli parasitizing H. mabouia
with moderate prevalence (P = 45%) and there was
no influence on the parasitic load with the TL and
Minaya-Angoma et al.
253
Neotropical Helminthology, 2018, 12(2), jul-dic
Parasite
Location stage n N P (%)
MA
MI
ACARI
Adults,
nymphs,
larvae
Geckobia hemidactyli
Lawrence, 1936
Skin 41 379 45.05
4.16
9.24
PENTASTOMIDA
Raillietiella hebitihamata
Self & Kuntz, 1960
Lung Adult 30 185 32.97
2.03
6.17
TREMATODA
Paradistomum sp.1
Kossack, 1910
Bile duct Adult 10 153 10.99
1.68
15.30
Paradistomum sp.2 Kossack, 1910
Bile duct Adult 3 23 3.30
0.25
7.67
CESTODA
Oochoristica vanzolinii
Rego & Rodrigues, 1965
Intestine Adult 20 45 21.98
0.49
2.25
NEMATODA
Spauligodon sp.
Skrjabin, Schikhobalova & Lagodovskaja, 1960
Intestine Adult 34 240 37.36
2.64
7.06
Parapharyngodon sp.
Chatterji, 1933
Intestine Adult 16 68 17.58
0.75
4.25
Physaloptera sp.
Rudolphi, 1819
Intestine Larvae 10 21 10.99
0.23
2.10
Acuariidae sp. Railliet, Henry & Sisoff, 1912
Intestine Larvae 2 2 2.20
0.02
1.00
Oswaldocruzia aff
brasiliensis
Lent et Freitas, 1935
Intestine Adult 2 3 2.20
0.03
1.50
Non identied nematode species Liver Cyst 1 1 1.10 0.01 1.00
Table 1. Ecological descriptors, location, and stage of Hemidactylus mabouia parasites of San Martin and Huánuco, Peru. P (%) = Prevalence, AM =
average abundance, IM = average intensity of infection, n = number of infected hosts, N = total number of parasites.
Metazoans of the Afro-American house gecko
254
Neotropical Helminthology, 2018, 12(2), jul-dic
Type of infection Total
% total
Machos
Hembras
Monospecic with one species
25
27.47
20
5
Polyspecic or múltiple
with two species
35
38.46
26
9
with three species
15
16.48
13
2
with four species
6
6.59
6
0
with ve species
1
1.09
1
0
Not parasited zero species 9 9.89 6 3
Table 2. Individual or multiple parasitic infections in males and females of Hemidactylus mabouia of San Martin
and Huanuco, Peru.
Table 3. Values of the index of specific importance, frequency of dominance and frequency of relative dominance,
and of the aggregation indexes (id = dispersion index, PDI = Poulin Discrepancy index and the K of the negative
2
binomial equation with its respective value of X ) applied to the most prevalent parasites. ISI = index of specific
importance, FD = frequency of Dominance and FRD = frequency of Relative Dominance of the parasitic component
of Hemidactylus mabouia of San Martin and Huánuco, Peru.
Parasite ISI FD FRD id PDI K X2
ACARI
Geckobia hemidactyli
461.5
17 0.33 12.70 0.72
ND**
ND**
PENTASTOMIDA
Raillietiella hebitihamata
236.3
5 0.16 16.10 0.85 0.14
5.97
TREMATODA
Paradistomum sp.1
179.1
4 0.13 28.39 0.93 0.02
4.19
Paradistomum sp.2
28.3
0 0.02 ND* ND*
ND*
ND*
CESTODA
Oochoristica vanzolinii
71.4
1 0.04 4.28 0.85 0.19
4.69
NEMATODA
Spauligodon sp
301.1
11 0.21 11.19 0.80 0.17
11.25
Parapharyngodon sp
92.3
4 0.06 8.02 0.90 0.08
2.98
Physaloptera sp
34.1
0 0.02 3.19 0.92 0.09
0.84
Acuariidae gen. sp
4.4
0
0.002
ND*
ND*
ND*
ND*
Oswaldocruzia aff brasiliensis 5.5 0 0.003 ND* ND* ND* ND*
Nematodo gen. sp. 2.2 0 0.001 ND* ND* ND* ND*
the sex of the geckos. Martínez-Rivera et al. (2003)
also recorded G. hemidactyli in H. mabouia
collected near buildings in Culebra and Mona
Island in Puerto Rico. They found high prevalences
(P = 100%) in adults and a range of mites from 3 to
<300 parasites per individual. Revisions of
samples of H. mabouia collected in Peru (Tarapoto,
Moyobamba, and Iquitos) showed no infestation
with mites. The authors argue that this is due to the
age of the samples, their different uses for other
studies, and the constant change of the preservation
status where they were.
Pentastomid crustaceans are common parasites of
the respiratory tract of reptiles. The infection with
Raillietiella Sambon, 1910 species in geckos in
America (Rego, 1983) is known. The prevalence of
R. hebitihamata parasitizing H. mabouia found in
this study (P = 32.9%) was lower than that reported
in the same host Gecko of Puerto Rico (89%)
(Simonsen & Sarda, 1985) and H. angulatus
Hallowell, 1854 of the Hispaniola Caribbean
Island (62%) (Powell et al., 1993). However, our
results were higher than those reported in H.
turcicus (Linnaeus, 1758) from the United States
ND * = Not determined by having prevalences of less than 10%
ND ** = Not determined due to signicantly different variances.
Minaya-Angoma et al.
& De la Riva, 1999 (2.5%) (Dias et al., 2005), and
Tropidurus hispidus (Spix, 1825) (11.1%)
(Almeida et al., 2008).
Anjos et al. (2008) determined the mean infection
intensity (MI) for R. hebitihamata (MI = 1.8) in H.
mabouia. Barton (2007) also shows values of the
MI of R. hebitihamata in H. frenatus from different
(19.8%) (Riley et al., 1988) and H. frenatus
Duméril & Bibron, 1836 from Indonesia (25-33%)
(Matsuo & Oku, 2002). In Brazil, studies have
shown an unequal prevalence in native lizard
species Brasiliscincus agilis (Raddi, 1823) (3.6-
9.0%) (Vrcibradic et al., 2002); Cnemidophorus
abaetensis Reis Dias, Rocha & Vrcibradic, 2002
(6.0%) (Dias et al., 2005) and C. ocellifer Dirksen
255
Neotropical Helminthology, 2018, 12(2), jul-dic
Table 4. Hemidactylus Correlation coefficients (r) used to evaluate the relationship between the total length (TL) of
mabouia versus the prevalence (P), mean abundance (MA) and mean intensity (MI) of the parasites. Test of t of
student (t) and Chi squared (X ) used to evaluate the relationship between the sex of and prevalence and
2H. mabouia
parasitic abundance.
Parasite
P vs TL
Spearman
r/p
MA vs TL
Pearson r/p MI vs TL
Pearson r/p
P vs sex
X2/p
MA vs sex
t/p
MI vs sex
t/p
Geckobia hemidactyli
0.60/0.29
0.20/0.75 -0.23/0.72
0.05/0.82
0.42/0.68**
3.56/0.73**
Raillietiella hebitihamata
0.90/0.04
0.92/0.88 -0.13/0.84
0.87/0.65
1.16/0.26*
1.63/0.18*
Paradistomum sp.1
0.10/0.87
-0.25/0.69 -0.02/0.97
0.01/0.94
0.97/0.33**
0.84/0.55*
Oochoristica vanzolinii
0.70/0.19
0.85/0.07 0.81/0.10 2.08/0.15
1.14/0.26**
0.45/0.66**
Spauligodon sp.
-0.15/0.81
0.98/0.00 0.99/0.00 0.35/0.55
0.53/0.60**
0.21/0.83**
Parapharyngodon sp.
0.90/0.04
0.76/0.14 0.86/0.05 8.35/0.00
2.95/0.00*
ND***
Physaloptera sp. 0.10/0.87 0.15/0.81 010/0.87 0.52/0.47
0.91/0.37*
1.09/0.31**
p = level of signicance, ND = not determined by the absence of data in the group of females.
* Unequal variances (Levene test) . ** Equa l Variances (Levene Test).
Values in bold indicate that they are statistically signicant.
Metazoans of the Afro-American house gecko
Table 5. Summary of main results of the non-parametrical permutational ANOVA (PERMANOVA) relating
abundances of parasite species of Hemidactylus mabouia and length, sex and locality.
Source
F
P(perm)
Length
0.82
0.63
Groups (bounferroni
test)
6-8 cm x 8.1-10cm
0.47
6-8 cm x 10.1-12cm
0.31
6-8 cm x 12.1-14cm
0.37
6-8 cm x >14 cm
0.22
8.1-10cm x 10.1-12cm 0.38
8.1-10cm x 12.1-14cm 0.63
8.1-10cm x >14cm
0.59
10.1-12cm x 12.1-14cm 0.33
10.1-12cm x >14cm
0.93
12.1-14cm x >14 cm
0.84
Sex
1.67 0.15
Groups (bounferroni
test)
Males x females
0.14
Locality
0.93 0.44
Groups (bounferroni
test)
Leoncio Prado x San Martín 0.29
Leoncio Prado x Lamas 0.74
Leoncio Prado x Bellavista
0.13
localities and their values range from 3 to 8.3. In
our study, a MI of 6.17 is observed. Raillietiella
hebitihamata is not a specific parasite of its host;
this is shown in a report shown by Barton (2007)
which summarizes a list of 6 species of Geckonidae
lizards, one species of Agamidae, and one species
of Scincidae as hosts of this parasite.
Species of the genus Paradistomum have been
reported parasitizing the bile ducts and the intestine
of reptiles in Europe, South East Asia, Madagascar,
Australia, and Brazil. In America, only three
species of Paradistomum are known: P. boae
(McCallum, 1921) Travassos, 1924, P.
parvissimum Travassos, 1918, and P. rabusculum
Kossack, 1910, all three are found in South
America and only P. parvissimum is recorded
parasitizing H. mabouia (Ávila & Silva, 2010). Our
s pe c i m e n s o f P a r a d i s t o m u m sp 1 a n d
Paradistomum sp2. differ from P. parvissimum by
the position of the vitelline glands, being those of
the latter posterior to the testicles and in our
previous one, as well as the proportion of the
suckers, being the oral wider than the ventral one in
P. parvissimum and vice versa in the specimens
collected in our study.
Seven species of Oochoristica have been recorded
in South America: O. ameivae (Beddard, 1914), O.
bresslaui Fuhrmann, 1927, O. freitasi Rêgo &
Ibáñez, 1965, O. iguanae Bursey & Goldberg,
1996, O. insulamargaritae López -Neyra & Diaz-
Ungría, 1957, O. travassosi Rêgo & Ibáñez, 1965,
and O. vanzolinii Rêgo & Oliveira-Rodrigues,
1965, all parasitizing the intestine of reptiles, but
only O. ameivae, O. freitasi, O. iguanae, and O.
travassosi have been registered for Peru (Ávila &
Silva, 2010). Goldberg & Bursey (2010) conducted
helminth studies on 4 species of Phyllodactylus
Gray, 1828 in Peru and found O. travassosi
parasitizing only P. johnwrighti Dixon & Huey,
1970 with P = 11% and MI = 1. Bursey et al. (2005)
found O. ameivae parasitizing the lizard Ameiva
ameiva Linnaeus, 1758 with P = 12% and MI = 1.2
in Peru. Here we report O. vanzolinii parasitizing
H. mabouia with a higher prevalence and infection
intensity (P = 21.98%, MI = 2.25), and at the same
time it is reported to Peru as a new geographical
place for this species of cestode.
T h e s p e c i e s o f S p a u l i g o d o n s p . a n d
Parapharyngodon sp. were not identified at the
256
Neotropical Helminthology, 2018, 12(2), jul-dic Minaya-Angoma et al.
species level, because only females were found in
the case of Parapharyngodon and few males for
Spauligodon. The lack of male specimens made the
identification work difficult because these
nematode species are differentiated by the
copulatory structures of the males. These nematode
species are common parasites of Peruvian geckos
and their prevalences have been recorded by
several authors, including Spauligodon
oxkutzcabiensis Chitwood, 1938 in Phyllodactylus
inaequalis Cope, 1876 (P = 14%, MI = 2), P.
johnwrighti (P = 8%, MI = 3.7), P. microphyllus
Cope, 1876 (P = 45%, MI = 18.6), and
Thecadactylus rapicauda (Houttuyn, 1782) (P =
20%, MI = 13.5) (Bursey et al., 2005; Goldberg &
Bursey, 2010). We registered Spauligodon sp. in H.
mabouia with P = 37.3, MI = 7.06. For the case of
Parapharyngodon, this nematode has also been
recorded in the Goldberg & Bursey (2010) studies,
as Parapharyngodon scleratus (Travassos, 1923)
Freitas, 1957 parasitizing P. johnwrighti (P=55%,
MI = 1.8). Other Parapharyngodon species are
also reported for Peru as is the case of P. scleratus
in Varzea bistriata (Spix, 1825) (P = 9%, MI = 1),
A. ameiva (P = 4%, MI = 1), and Kentropyx
pelviceps (Cope, 1868) (P = 7%, MI = 1) (Bursey et
al., 2005). In this study, Parapharyngodon
specimens were recorded parasitizing only H.
mabouia males with P = 17.58% and MI = 4.25,
values higher than those recorded above.
High homogeneity among metazoan parasite
communities of H. mabouia was observed. The
parasites communities generally did not exhibit
clear differences in abundance in relation to length,
sex, and locality of H. mabouia.
It is concluded that the parasitic fauna associated
with H. mabouia from the Huanuco and San Martin
region, Peru was composed of 11 parasitic species
of which R. hebitihamata and Parapharyngodon
sp. were positively correlated with the TL of the
host, while the MA of O. vanzolinii and
Spauligodon sp. were significantly associated with
the TL of the H. mabouia gecko. Only the species
Parapharyngodon sp. showed to have a greater
preference of infection in prevalence and
abundance in host males. Oochoristica vanzolinii
and R. hebitihamata are new recorded parasites for
Peru.
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