Parasitol Res
https://doi.org/10.1007/s00436-017-5672-y
ORIGINAL PAPER
Helminth infections in a pair of sympatric congeneric
lizard species
Thiago Maia-Carneiro 1 & Tatiana Motta-Tavares 1 & Robson Waldemar Ávila 2 &
Carlos F. D. Rocha 1
Received: 28 December 2016 / Accepted: 1 November 2017
# Springer-Verlag GmbH Germany, part of Springer Nature 2017
Abstract We analyzed parameters of parasitism by helminths
in a pair of sympatric congeneric lizard species (Tropidurus
hispidus and Tropidurus semitaeniatus). Differences in their
supracommunities (richness, composition, and abundance)
and the influence of helminthic loads on minimum flight ini-
tiation distances and body temperatures were evaluated. We
reported new findings of Piratuba digiticauda infecting
T. hispidus and Oochoristica bresslaui infecting
T. semitaeniatus. Parapharyngodon alvarengai was the most
abundant helminth in both host species. Tropidurus hispidus
individuals hosted a higher abundance and richness of hel-
minths than T. semitaeniatus, with females of the former hav-
ing larger helminthic loads than males. Dissimilarities be-
tween host species may be attributed to differences in their
utilization of niche dimensions (time, food, and structural
and thermal space), the occurrence of morphological differ-
ences that result in differential exposure to the sources and
agents of infection, and/or differential immunological func-
tions. Our data suggests that infection by P. alvarengai led
to some limitations in locomotor performance of T. hispidus
resulting in decreased minimum flight initiation distance as
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00436-017-5672-y) contains supplementary
material, which is available to authorized users.
* Thiago Maia-Carneiro
tmaiacarneiro@gmail.com
1
Departamento de Ecologia, Universidade do Estado do Rio de
Janeiro, Rua São Francisco Xavier 524, Rio de Janeiro 20550-013,
Brazil
2
Departamento de Química Biológica, Universidade Regional do
Cariri, Rua Coronel Antônio Luiz 1161, Crato, Ceará 63100-000,
Brazil
infection rates increased. Individuals opted for a prolonged
period of immobility to avoid capture. There was a negative
relationship between helminthic loads and body temperatures
in T. semitaeniatus, possibly due to decreased activity and
thermoregulation rates, and increased use of shelters by lizards
with high infection levels to avoid predation.
Keywords Body temperature . Minimum flight initiation
distance . Parasitism . Tropiduridae . Tropidurus hispidus .
Tropidurus semitaeniatus
Introduction
Phylogenetically closely related hosts, including lizards, typically
share parasite species despite variations in the richness, compo-
sition, and abundance of parasites among host species and pop-
ulations (Freeland 1983; Aho 1990; Ávila and Silva 2010; Anjos
et al. 2013). Similarities in parasitic fauna may be greater in
congeneric sympatric species than in different populations of
the same species (Aho 1990). Disparities in the abundance and
richness of parasites within and between species may be owing to
distinct morphology, ecology, behavior, and immunological
functions (Freeland 1983; Aho 1990). Sexes do not appear to
influence the structure of helminth communities in lizards (Aho
1990; Van Sluys et al. 1994, 1997; Rocha 1995; Poulin 1996;
Ribas et al. 1998; Vrcibradic et al. 2000; Anjos et al. 2013;
Pereira et al. 2012). Regardless, variations in male and female
helminth loads occur if there are considerable inter-sexual differ-
ences in morphology, ecology, behavior, or immunological re-
sponses (Aho 1990; Poulin 1996; Galdino et al. 2014). Infection
by parasites also has adverse effects on escape abilities and ac-
tivity levels of hosts (Main and Bull 2000; Fenner and Bull 2008;
Adelman and Martin 2009; Robar et al. 2010; McElroy and
Buron 2014; Zamora-Camacho et al. 2014).

Tropidurus hispidus and Tropidurus semitaeniatus are liz-
ard species that occur sympatrically in some localities in
Brazil (e.g., Vitt 1995; Ribeiro and Freire 2010; this study).
Individuals of these species have characteristics in terms of
their utilization of niche dimensions that facilitate their local
c o - e x i s t e n c e. U n l i ke th e g e n er a l i s t T. hi sp i du s ,
T. semitaeniatus has specializations associated with the use
of sloping, vertical habitats, and crevices in rocky outcrops
(Maia-Carneiro and Rocha 2015; Maia-Carneiro and Rocha
unpublished data). Despite similar daily activity cycles, differ-
ences in movement rates, such as variations in the timing of
the start and end of activities and periods of reduction or
maintenance of activity during midday, occurred (Vitt 1995;
Ribeiro and Freire 2010; Maia-Carneiro and Rocha unpub-
lished data). Lizards of both species are omnivorous, consum-
ing arthropods and plant material, but sizes of food may vary
in relation to body size (Van Sluys et al. 2004; Ribeiro and
Freire 2011; Maia-Carneiro et al. 2017). Moreover, spatial use
by both lizard species differs in terms of sunlight incidence,
microhabitat temperatures, perch height, and microhabitat
structure (Maia-Carneiro and Rocha unpublished data).
Based on these dissimilarities between T. hispidus and
T. semitaeniatus, we investigated the differences and similar-
ities between the structure of helminth communities in hosts
based on species richness, composition, and relative abun-
dance. Furthermore, we evaluated the influence of helminth
loads on host flight responses and body temperatures.
Materials and methods
Study area
This study was conducted in Igatu, municipality of Andaraí, in
the surroundings of the conservation unit for nature protection
Parque Nacional da Chapada Diamantina, state of Bahia,
Brazil (12° 53′ S, 41° 19′ W). This region possesses highly
diverse habitats, including the Atlantic Forest, rupestrian
fields, Caatinga, and Cerrado. The area is located in a region
(Diamantina Plateau) characterized by the predominance of
plateaus of rocky outcrops dating back to the
Mesoproterozoic era (Delgado et al. 1994 cited in Pedreira
1997). Chapada Diamantina exhibits the Cwb climate (humid
subtropical with dry winters and temperate summers) and ex-
perience little annual rainfall and is one of the driest Cwb
locations in Brazil (Alvares et al. 2013). Prominent rocky
outcrops and shallow soils are characteristic of this region
(Rocha et al. 2005).
Data collection and analytical procedures
Data collection occurred in March 2013 during visual encoun-
ter surveys (VES) for lizards. VES were performed using 30-
Parasitol Res
min transects at hourly intervals between 09:00 and 17:00
(disregarding the summer time). Whenever a T. hispidus or
T. semitaeniatus individual was sighted, we estimated the min-
imum flight initiation distance as the distance from the poten-
tial predator (investigator: Thiago Maia-Carneiro) to the lizard
when it started to escape. When a lizard was sighted, the
investigator moved straight towards it at a slow walking pace
(approximately two steps per second). The initial positions of
the lizards (18 T. hispidus and 24 T. semitaeniatus) and inves-
tigator were marked using scratches on the rocks or by tying a
ribbon to a rock after the lizards moved (see Maia-Carneiro
and Rocha 2015). Subsequently, lizards were captured using
the noose technique or by hand. Snout-vent length (SVL)
using a caliper (precision 0.01 mm), body mass using spring
scales (precision 0.25 g for individuals up to 30 g, and preci-
sion 1.0 g for individuals larger than 30 g), and body temper-
ature (Tb) using a Miller and Weber quick-reading cloacal
thermometer (precision of 0.2 °C) were measured. Minimum
flight initiation distances were assessed using a measure tape
precision 0.1 cm). Twenty-seven T. hispidus and thirty-nine
T. semitaeniatus captured were killed and preserved in 10%
formalin (collection permit IBAMA/ICMBio no. 17474-1).
In the laboratory, collected lizards were dissected and their
sex was identified. Subsequently, the peritoneal cavity was
carefully inspected for the presence of helminths, and the
lungs, stomach, and small and large intestines were removed
and examined for the presence of helminths. The helminths
were mounted temporarily on glass slides and cleared with
Hoyer’s medium for identification using stereomicroscopes
and compound microscopes. Nematoda and Cestoda species
were identified according to Vicente et al. (1993) and Bursey
and Goldberg (1996), respectively. The helminths were pre-
served in 70% ethanol and voucher specimens were deposited
in the Coleção Parasitológica da Universidade Regional do
Cariri (URCA), Brazil.
For each helminth species, we calculated the abundance,
prevalence, and mean infection intensity. Prevalence was con-
sidered the percentage of individuals of each lizard species
hosting helminths and infection intensity was considered the
mean number of helminths hosted per infected lizard of each
species. To test for differences in total abundance of parasites
between T. hispidus and T. semitaeniatus and between sexes
within each species, we performed analyses of variance
(ANOVA) and analyses of covariance (ANCOVA) controlling
for influences of SVL and body mass. The data for SVL of
T. semitaeniatus and T. semitaeniatus females deviated from
normality according to Kolmogorov-Smirnov tests (see
Appendix 1 in the Supplementary material). Nevertheless,
we applied parametric tests on these data because they seemed
normally distributed according to parameters of skewness,
kurtosis, and Shapiro-Wilk normality tests (T. semitaeniatus:
W = 0.968, P = 0.334; T. semitaeniatus females: W = 0.929,
P = 0.206). Differences in richness associated with T. hispidus
Parasitol Res
and T. semitaeniatus individuals and between the sexes within
each species were assessed using Mann-Whitney U tests.
We estimated the levels of aggregation for each taxonomic
group of helminths in either lizard species through the index
of discrepancy (D) as follows:
! groups of helminths present were P. alvarengai (N = 150)
N i
2∑ ∑ xj
i¼1 j¼1
D ¼ 1−
xN ðN þ 1Þ
where x is the number of helminths associated with the host j,
and N is the number of hosts (Poulin 1993).
This index estimates the difference between the hypothet-
ical distribution where all hosts shelter the same number of
parasites and the observed parasite distribution (Poulin 1993).
The values of this index vary from zero (D = 0), if all the hosts
shelter the same number of helminths, to one (D = 1), if all the
helminths were found in only one host.
Simple linear regression analyses were performed to eval-
uate relationships between helminth abundance and SVL,
body mass, and minimum flight initiation distance of infested
lizards. To test for interactions between abundance and body
temperature, we performed a simple regression analysis for
T. semitaeniatus and a Spearman correlation for T. hispidus.
We also used Spearman correlations to test for associations
between richness and body size (SVL and body mass) in each
host species. We performed Kolmogorov-Smirnov one-sam-
ple tests to evaluate the normality of data distribution (see
Appendix 1 in the Supplementary material). We also analyzed
the data distribution considering parameters of skewness and
kurtosis. The descriptive statistics are presented throughout
the text as mean ± standard deviation.
Results
D u r i n g V E S i n I g a t u , 2 7 T. h i s p i d u s a n d 3 9
T. semitaeniatus individuals were captured. The overall
prevalence of helminths was 96.3% in T. hispidus (26
individuals) and 38.5% in T. semitaeniatus (15 individ-
uals) (Table 1). As many as 344 and 45 individual hel-
m i n t h s w e r e a s s o c i a t e d w i t h T. h i s p i d u s a n d
T. semitaeniatus, respectively (Table 1), with infection
intensities of 13.2 ± 7.2 and 3 ± 2.1, respectively
(Table 1). The helminths recorded in the hosts belonged
to 10 different taxonomic groups, eight and four of which
associated with T. hispidus and T. semitaeniatus, respec-
tively (Tables 1 and 2). The highest prevalence in
T. hispidus was by the nematodes Parapharyngodon
alvarengai (92.6% of the lizards), followed by
Physaloptera retusa (74.1%). The highest prevalence in
T. semitaeniatus was by P. alvarengai (25.6%) and
Strongyluris oscari (17.9%) (Table 1). The most intense
helminth infections were by P. alvarengai (6.0 ± 3.5) and
Physaloptera lutzi (5.8 ± 5.3) in T. hispidus, and
P. alvarengai (2.4 ± 1.7) and S. oscari (2.1 ± 1.5) in
T. semitaeniatus (Table 1). The most abundant taxonomic
and P. retusa (N = 93) in T. hispidus and P. alvarengai
(N = 24) and S. oscari (N = 15) in T. semitaeniatus
[Tables 1 (values of D) and 2]. The most infected body
regions were the large intestines (N = 191 helminths) and
stomachs (N = 114 helminths) in T. hispidus and the large
(N = 32 helminths) and small (N = 10 helminths) intes-
tines in T. semitaeniatus (Table 2).
Tropidurus hispidus hosted a greater abundance of hel-
minths than T. semitaeniatus (r2 = 0.426, F [1, 39] = 28.964,
P < 0.0001) (Fig. 1a, Tables 1 and 2). This was still the case
when the effects of SVL (r2 = 0.498, F [2, 38] = 5.412,
P = 0.025) and body mass (r2 = 0.502, F [2, 38] = 5.765,
P = 0.021) (Tables 1, 2, and 4) were factored out. The mean
richness of helminths associated with individuals was signif-
icantly higher (U = 349.000, P < 0.0001) in T. hispidus
[2.6 ± 0.9 (1–5)] than in T. semitaeniatus [1.3 ± 0.5 (1–2)]
(Fig. 1b).
There was no difference in the abundance of helminths
between sexes in either T. hispidus (F [1, 24] = 0.001,
P = 0.980) or T. semitaeniatus (F [1, 13] = 0.565, P = 0.466)
(Table 3). In T. hispidus, females hosted more helminths than
males when the influence of SVL (r2 = 0.209, F [2, 23] = 6.091,
P = 0.021) was removed. There was no difference in the hel-
minthic load of male and female T. hispidus after controlling
the influences from body mass (F [2, 23] = 3.585, P = 0.071).
There were no differences in abundance of helminths between
male and female T. semitaeniatus after factoring out the effects
of body size (SVL: F [2, 12] = 1.871, P = 0.196; body mass: F
[2, 12] = 2.903, P = 0.114) (Tables 3 and 4). The helminthic
richness in T. hispidus females and males were 2.6 ± 0.9 (1–4)
and 2.6 ± 1.0 (2–5), respectively, and did not differ statistically
(U = 89.000, P = 0.719). Similarly, in T. semitaeniatus, these
values were 1.3 ± 0.5 (1–2) and 1.2 ± 0.4 (1–2) for females
and males, respectively, and did not differ (U = 30.000,
P = 0.645).
Helminth abundance was not related to SVL in either
T. h i s p i d u s ( F [ 1 , 2 4 ] = 3 . 3 5 9 , P = 0 . 0 7 9 ) a n d
T. semitaeniatus (F [1, 13] = 2.649, P = 0.128) (Tables 1 and
4). The same trend occurred with body mass (T. hispidus: F [1,
24] = 3.524, P = 0.073; T. semitaeniatus: F [1, 13] = 3.649,
P = 0.078) (Tables 1 and 4). Similarly, helminth richness
was not related to SVL or body mass in either T. hispidus
(SVL: r = 0.127, P = 0.537; body mass: r = 0.144,
P = 0.483) and T. semitaeniatus (SVL: r = − 0.017,
P = 0.951; body mass: r = − 0.035, P = 0.901) (Table 4).
The minimum flight initiation distance of T. hispidus in-
fected with P. alvarengai was negatively related to helminth
 Parasitol Res

Table 1 Prevalence, infection intensity (values recorded as mean ± standard deviation), and index of discrepancy (D) of Tropidurus hispidus (N = 27)
and Tropidurus semitaeniatus (N = 39) in terms of helminth species that infected each lizard in Igatu. Prevalence (absolute numbers), ranges, and
abundance of helminths infecting the lizards are recorded in parentheses

Helminths Tropidurus hispidus Tropidurus semitaeniatus

Prevalence Intensity of infection D Prevalence Intensity of infection D

Oochoristica bresslaui – – 2.6 (1) 5 (5–5, N = 5) 0.95

Oochoristica sp. 3.7 (1) 2 (2–2, N = 2) 0.93 – –
Parapharyngodon alvarengai 92.6 (25) 6 ± 3.5 (1–15, N = 150) 0.39 25.6 (10) 2.4 ± 1.7 (1–6, N = 24) 0.78
Physaloptera lutzi 18.5 (5) 5.8 ± 5.3 (2–15, N = 29) 0.86 – –
Physaloptera retusa 74.1 (20) 4.7 ± 3.3 (1–14, N = 93) 0.53 – –
Physaloptera sp. – – 2.6 (1) 1 (1–1, N = 1) 0.95
Physalopteroides venancioi 7.4 (2) 2 ± 0 (2–2, N = 4) 0.83 – –
Piratuba digiticauda 14.8 (4) 2 ± 0.82 (1–3, N = 8) 0.85 – –
Rhabdias sp. 3.7 (1) 1 (1–1, N = 1) 0.93 – –
Strongyluris oscari 37 (10) 5.7 ± 4.7 (1–17, N = 57) 0.72 17.9 (7) 2.1 ± 1.5 (1–5, N = 15) 0.84
Overall 96.3 (26) 13.2 ± 7.2 (2–31, N = 344) 38.5 (15) 3 ± 2.1 (1–8, N = 45)

abundance (r2 = − 0.272, F [1, 14] = 5.239, P = 0.038) (Fig. 2, Discussion

Tables 1 and 4), suggesting that predators were allowed to get
closer in T. hispidus with higher infection intensities before the
lizards ran. In T. semitaeniatus, there was no relationship be-
tween flight initiation distance and the abundance of
P. alvarengai (F [1, 5] = 3.031, P = 0.142) (Tables 1 and 4).
Helminth abundances and body temperature were not related
in T. hispidus hosts (r2 = − 0.088, P = 0.668); however, they
were negatively related in T. semitaeniatus (r2 = 0.294, F [1,
13] = 5.407, P = 0.037) (Fig. 3, Tables 1 and 4).
In Igatu, we recorded helminth species previously unknown to
infect the lizard species evaluated: Piratuba digiticauda in
T. hispidus and Oochoristica bresslaui in T. semitaeniatus.
Similarly, in previous studies, P. digiticauda was recorded in
Tropidurus guarani, Tropidurus spinulosus, and Tropidurus
torquatus, whereas O. bresslaui was in T. hispidus,
T. spinulosus, and T. torquatus (Ávila and Silva 2010 and in
Anjos et al. 2013). Variations in helminth fauna occur among

Table 2 Distribution of helminths identified within different body regions in Tropidurus hispidus (N = 27) and Tropidurus semitaeniatus (N = 39) in
Igatu. Percentages are within parentheses

Helminths Tropidurus hispidus Tropidurus semitaeniatus

Celoma Lungs Stomach Small Large Celoma Lungs Stomach Small Large
intestine intestine intestine intestine

Oochoristica bresslaui – – – – – – – – 5.0 (50) –

Oochoristica sp. – – – 2 (9.5) – – – – – –
Parapharyngodon alvarengai – – 1 (0.9) 6 (28.6) 143 (74.9) – – – 2 (20.0) 22 (68.8)
Physaloptera lutzi – – 26 (22.8) 2 (9.5) 1 (0.5) – – – – –
Physaloptera retusa – – 85 (74.5) 3 (14.3) 5 (2.6) – – – – –
Physaloptera sp. – – – – – – – 1 (33.3) – –
Physalopteroides venancioi – – 2 (1.8) 2 (9.5) – – – – – –
Piratuba digiticauda 6 (100) – – – 2 (1.0) – – – – –
Rhabdias sp. – 1 (8.3) – – – – – – – –
Strongyluris oscari – 11 (91.7) – 6 (28.6) 40 (21.0) – – 2 (66.7) 3 (30.0) 10 (31.2)
Total 6 (100) 12 (100) 114 (100) 21 (100) 191 (100) – – 3 (100) 10 (100) 32 (100)
Parasitol Res

Table 3 Number of Tropidurus hispidus and T. semitaeniatus females and males (percentages within parentheses), helminth infection intensity, snout-
vent length (mm), and body mass (g) of female and male T. hispidus and T. semitaeniatus in Igatu. Range and sample size are within parentheses

Data Number of lizards Intensity of infection Snout-vent length Body mass

with helminths

Tropidurus hispidus
Females (N = 16) 15 (93.8) 13.2 ± 6.2 (2–24, N = 198) 80.4 ± 10.1 (57.7–94.7, N = 16) 16.8 ± 5.9 (57.7–94.7, N = 16)
Males (N = 11) 11 (100) 13.3 ± 8.6 (4–31, N = 146) 104.9 ± 18.9 (71.6–133.2, N = 11) 48.2 ± 24.1 (11–90.5, N = 11)
Tropidurus semitaeniatus
Females (N = 17) 6 (35.3) 2.5 ± 1.6 (1–5, N = 15) 55 ± 4.6 (44.9–61.6, N = 17) 3.3 ± 0.7 (2.25–4.75, N = 17)
Males (N = 19) 9 (47.4) 3.33 ± 2.3 (1–8, N = 30) 60.8 ± 6.6 (44.1–69.6, N = 19) 5.2 ± 1.8 (2–7.75, N = 19)

lizard populations, but congeneric hosts, including Tropidurus
spp., commonly share parasite species (Ávila and Silva 2010,
Anjos et al. 2013). The potentially similar environmental con-
ditions within conspecific hosts favor the sharing of helminths
(Aho 1990).
P. alvarengai and P. retusa had a greater prevalence and
abundances in T. hispidus in Igatu, whereas P. alvarengai and
S. oscari had greater abundance and occurred more often
within T. semitaeniatus. Highly prevalent parasite species neu-
tralize aggregations within few hosts by reducing variations in
the number of parasites in different hosts (Aho 1990, Poulin
1993, Perez-del-Olmo et al. 2011). In this study, the most
representative helminth species within T. hispidus
(P. alvarengai: D = 0.39; P. retusa: D = 0.53) and
T. semitaeniatus (P. alvarengai: D = 0.78; S. oscari:
D = 0.84) presented the lowest values of aggregation.
Helminths belonging to the genus Parapharyngodon appear
to have close associations with Tropidurus lizards, being pres-
ent in all species analyzed to date, except T. oreadicus (Ávila
and Silva 2010; Anjos et al. 2013). Current data suggest that
P. sceleratus is the most widespread helminth species of the
genus Parapharyngodon infecting Tropidurus (Ávila and
Silva 2010; Anjos et al. 2013), but in Igatu, T. hispidus and
T. semitaeniatus were infected by P. alvarengai alone.
T. hispidus hosted more helminths than T. semitaeniatus,
regardless of body size, suggesting the influence of other
factors. Furthermore, similar to other localities (T. hispidus:
Ávila et al. 2012; Anjos et al. 2013; Galdino et al. 2014;
T. semitaeniatus: Ávila et al. 2012; Brito et al. 2014; Bezerra
et al. 2015), the richness associated with individuals was
higher in T. hispidus than in T. semitaeniatus in Igatu.
Susceptibility to infection is influenced by variations in food
consumption (quantitatively and qualitatively), time of activ-
ity, and spatial distribution (Freeland 1983; Aho 1990).
T. hispidus has access to food items that are not available to
T. semitaeniatus due to morphological limitations, and con-
sumes larger-sized food items in greater amounts (Van Sluys
1993; Van Sluys et al. 2004; Ribeiro and Freire 2011; Maia-
Carneiro et al. 2017). The activity cycles of T. hispidus and
T. semitaeniatus are typically similar with some differences in
movement rates during the day (Vitt 1995; Maia-Carneiro and
Rocha unpublished data). Tropidurus hispidus lizards use
structurally more diverse and more shaded, colder, and higher
microhabitats compared to the rock specialist T. semitaeniatus
(Vitt 1995; Vitt et al. 1996; Ribeiro and Freire 2010; Maia-
Carneiro and Rocha unpublished data). Although T. hispidus
and T. semitaeniatus perch on rocks, individuals of the latter
species are more selective (Maia-Carneiro and Rocha unpub-
lished data). Exposure on rocks is unfavorable for the devel-
opment of some nematodes (Austin et al. 2009; Bezerra et al.
2015). The larger body size of T. hispidus (Kolodiuk et al.
2010, Ribeiro and Freire 2011; Maia-Carneiro and Rocha

Table 4 Mean ± standard deviation of snout-vent length (mm), body mass (g), body temperature (°C), and minimum flight initiation distance (cm) of
Tropidurus hispidus and Tropidurus semitaeniatus in Igatu. Range and number of observations are within parentheses

Data Tropidurus hispidus Tropidurus semitaeniatus

Snout-vent length 90.4 ± 18.7 (57.7–133.2, N = 27) 57.2 ± 7.1 (41.3–69.6, N = 39)
Body mass 29.6 ± 22.2 (6–90.5, N = 27) 4.1 ± 1.7 (1.25–7.75, N = 39)
Minimum flight initiation distancea 165.6 ± 71.4 (72.8–282.0, N = 16) 89.4 ± 54.8 (22.7–196.7, N = 7)
Body temperaturea 35.5 ± 2.38 (30.2–39.2, N = 26) 36.3 ± 1.96 (32–39.8, N = 15)
a
Individuals infected by P. alvarengai

Fig. 1 Differences (a) in total number of helminths and (b) number of
helminth taxonomic groups between Tropidurus hispidus and Tropidurus
semitaeniatus in Igatu
Fig. 2 Relationship between minimum flight initiation distance (FID,
cm, N = 16) and number of Parapharyngodon alvarengai (NPA, log) in
Tropidurus hispidus in Igatu
Parasitol Res
2015; Maia-Carneiro et al. 2017) represents the existence of
additional internal space that allows for the accumulation of a
greater abundance and richness of helminths. Such morpho-
logical, ecological, and behavioral differences between
T. hispidus and T. semitaeniatus potentially influence the
probability of their encounter with sources and agents of in-
fection. Moreover, these differences may explain why of the
10 taxonomical groups of helminths identified in this study,
only P. alvarengai and S. oscari were present in both host
species despite the greater tendency of closely related species
to share similar helminth species in their supracommunities
(Freeland 1983; Aho 1990; Vrcibradic et al. 2000).
Dissimilarities with respect to helminth communities between
the host species may be also due to varying immunological
functions. Inter-specific differences in the longevity of indi-
viduals might influence the acquisition of taxonomically di-
verse helminth faunas, as well as a higher number of parasites;
lizards with a longer life span are more likely to encounter and
to accumulate helminths.
In contrast to studies by Brito et al. (2014) and Galdino
et al. (2014), where males had greater helminthic loads, in
Igatu, T. hispidus females hosted more helminths than males
when body size (SVL) was accounted for. The data for this
study were collected during the potentially stressful (which
may undermine immune responses—French et al. 2010;
Lucas and French 2012) reproductive season of T. hispidus
(Pietro et al. 1976; Ribeiro et al. 2012). Some level of immu-
nosuppression may have occurred in reproductive females of
T. hispidus due to trade-offs between reproductive and immu-
nological functions (French et al. 2007, 2009; French and
Moore 2008; Galdino et al. 2014) and exposure to stressors
(French et al. 2010; Lucas and French 2012). Inter-sexual
morphological, ecological, and behavioral differences also po-
tentially result in differential acquisition of helminths. We
need to recognize the limitations of the estimations regarding
Fig. 3 Relationship between body temperature (°C, N = 15) and total
number of helminths in Tropidurus semitaeniatus (N = 15) in Igatu
Parasitol Res
sexual differences in this study due to small datasets. The
cautiousness regarding the interpretation of sexual differences
is reinforced by the low value of the regression coefficient
(r2 = 0.209), making precise statements challenging.
Our data suggests that the infection by P. alvarengai led to
limitations in performance in T. hispidus, resulting in a reduc-
tion in minimum flight initiation distances of lizards as hel-
minth abundance increased. The lizards opted for prolonged
immobility to avoid capture (see Maia-Carneiro and Rocha
2015). Some parasites are capable to cause morphological,
ecological, and/or behavioral modifications in hosts, reducing
their performance (McElroy and Buron 2014 and references
therein). Individuals harboring greater parasitic loads are sus-
ceptible to increased predation risks (Møller and Erritzøe
2000; Genovart et al. 2010; Robar et al. 2010) and reduced
escape capacities because of locomotor performance con-
straints (Oppliger et al. 1996; Main and Bull 2000).
The body temperature of T. semitaeniatus individuals was
inversely related to the abundance of helminths. Higher hel-
minthic loads in these host lizards supposedly imposed activ-
ity restrictions, resulting in thermoregulatory deficits and the
increased utilization of shelters. T. semitaeniatus individuals
with higher helminthic loads (Fenner and Bull 2008; Adelman
and Martin 2009; Zamora-Camacho et al. 2014) are potential-
ly more vulnerable to predation due to impaired locomotor
abilities caused by lower body temperatures (Maia-Carneiro
and Rocha 2015; Autumn et al. 1994). These lizards are prone
to reduced reproductive success if they remain in shelters for
longer periods due to predator avoidance (Fenner and Bull
2008; Zamora-Camacho et al. 2014), which implies a reduc-
tion in overall activity rates (e.g., feeding rates, vigilance, and
reproduction).
Acknowledgements We thank Caio Faro for the valuable suggestions
regarding the English language.
Funding information We thank the Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq), which provided
grants to CFDR (process numbers 304791/2010–5, 470265/2010–8,
472287/2012-5, and 302974/2015-6) and RWA (process number
303622/2015-6). We acknowledge Fundação Carlos Chagas Filho de
Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), which sup-
ports CFDR through the Program “Cientistas do Nosso Estado” (process
numbers E–26/102.765/2012 and E-26/202.920.2015). T. Motta-Tavares
received a master fellowship from Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) and T. Maia-Carneiro received a PhD
fellowship from CAPES and FAPERJ.
References
Adelman JS, Martin LB (2009) Vertebrate sickness behaviors: adaptive
and integrated neuroendocrine immune responses. Integr Comp Biol
49(3):202–214
Aho JM (1990) Helminth communities of amphibians and reptiles: com-
parative approaches to understanding patterns and processes. In
Esch GW, Bush AO, Aho JM. Parasite communities: patterns and
processes. Chapman & Hall
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013)
Köppen’s climate classification map for Brazil. Meteorol Zeitsc 22:
711–728
Anjos LA, Ávila RW, Ribeiro SC, Almeida WO, da Silva RJ (2013)
Gastrointestinal nematodes of the lizard Tropidurus hispidus
(Squamata: Tropiduridae) from a semiarid region of northeastern
Brazil. J Helmintol 87(4):443–449
Austin E, Semmens K, Parsons C, Treonis A (2009) Granite rock out-
crops: an extreme environment for soil nematodes. J Nematol 41:
84–91
Autumn K, Weinstein RB, Full RJ (1994) Low cost of locomotion in-
creases performance at low temperature in a nocturnal lizard.
Physiol Zool 67:238–262
Ávila RW, Silva RJ (2010) Checklist of helminths from lizards and
amphisbaenians (Reptilia, Squamata) of South America. J Venom
Anim Tox Trop Dis 16:543–572
Ávila RW, Anjos LA, Ribeiro SC, Morais DH, Silva RJ, Almeida WO
(2012) Nematodes of lizards (Reptilia: Squamata) from Caatinga
biome, northeastern Brazil. Comp Parasitol 79(1):56–63
Bezerra CH, Ávila RW, Passos DC, Zanchi-Silva D, Galdino CAB (2015)
Levels of helminth infections in the flat lizard Tropidurus
semitaeniatus from north-eastern Brazil. J Helminthol. https://doi.
org/10.1017/S0022149X15000826
Brito SV, Ferreira FS, Ribeiro SC, Anjos LA, Almeida WO, Mesquita
DO, Vasconcellos A (2014) Spatial-temporal variation of parasites
in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and
Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in
northeastern Brazil. Parasitol Res 113:1163–1169
Bursey CR, Goldberg SR (1996) Oochoristica maccoyi n. sp. (Cestoda:
Linstowiidae) from Anolis gingivinus (Sauria: Polychrotidae) col-
lected in Anguilla, Lesser Antilles. Carib J Sci 32:390–394
Delgado IM, Pedreira AJ, Thorman CH (1994) Geology and mineral
resources of Brazil: A review. Inte Geol Rev 36: 503–544
Fenner AL, Bull CM (2008) The impact of nematode parasites on the
behaviour of an Australian lizard, the gidgee skink Egernia stokesii.
Ecol Res 23(5):897–903
Freeland WJ (1983) Parasites and the coexistence of animal host species.
Am Nat 121(2):223–236
French SS, Moore MC (2008) Immune function varies with reproductive
stage and context in female and male tree lizards, Urosaurus
ornatus. Gen Comp Endocrinol 155(1):148–156
French SS, DeNardo DF, Moore MC (2007) Trade-offs between the re-
productive and immune systems: facultative responses to resources
or obligate responses to reproduction? Am Nat 170(1):79–89
French SS, Moore MC, Demas GE (2009) Ecological immunology: the
organism in context. Integr Comp Biol 49(3):246–253
French SS, DeNardo DF, Greives TJ, Strand CR, Demas GE (2010)
Human disturbance alters endocrine and immune responses in the
Galapagos marine iguana (Amblyrhynchus cristatus). Horm Behav
58:792–799
Galdino CAB, Ávila RW, Bezerra CH, Passos DC, Melo GC, Zanchi-
Silva D (2014) Helminths infection patterns in a lizard (Tropidurus
hispidus) population from a semiarid Neotropical area: associations
between female reproductive allocation and parasite loads. J
Parasitol 100(6):864–867
Genovart M, Negre N, Tavecchia G, Bistuer A, Parpal L, Oro D (2010)
The young the weak and the sick: evidence of natural selection by
predation. PLoS One 5:e9774
Kolodiuk MF, Ribeiro LB, Freire EMX (2010) Diet and foraging behav-
ior of two species of Tropidurus (Squamata, Tropiduridae) in the
Caatinga of northeastern Brazil. S Am J Herpetol 5(1):35–44
Lucas LD, French SS (2012) Stress-induced trade-offs in a free-living
lizard across a variable landscape: consequences for individuals
and populations. PLoS One 7(11):e49895

Maia-Carneiro T, Rocha CFD (2015) Flight initiation distances of
Tropidurus hispidus and Tropidurus semitaeniatus (Squamata,
Tropiduridae) in sympatry. Herpetol Conserv Biol 10(2):661–665
Maia-Carneiro T, Motta-Tavares T, Rocha CFD (2017) Partition of tro-
phic niche dimensions of a pair of syntopic lizard species
(Squamata, Tropidurus). Herpetol J 27:143–150
Main AR, Bull CM (2000) The impact of tick parasites on the behaviour
of the lizard Tiliqua rugosa. Oecologia 122:574–581
McElroy EJ, Buron I (2014) Host performance as a target of manipulation
by parasites: a meta-analysis. J Parasitol 100(4):399–410
Møller AP, Erritzøe J (2000) Predation against birds with low immuno-
competence. Oecologia 122:500–504
Oppliger A, Célérier ML, Clobert J (1996) Physiological and behaviour
changes in common lizards parasitized by haemogregarines.
Parasitology 113:433–438
Pedreira AJ (1997) Sistemas deposicionais da Chapada Diamantina
Centro-oriental, Bahia. Rev Bras Geociênc 27:229–240
Pereira FB, Sousa BM, Lima SS (2012) Helminth community structure of
Tropidurus torquatus (Squamata: Tropiduridae) in a rocky outcrop
area of Minas Gerais state, southeastern Brazil. J Parasitol 98(1):6–
10
Perez-del-Olmo A, Morand S, Raga JA, Kostadinova A (2011)
Abundance-variance and abundance-occupancy relationships in a
marine host-parasite system: the importance of taxonomy and ecol-
ogy of transmission. Int J Parasitol 41:1361–1370
Pietro AS, León JR, Lara O (1976) Reproduction in the tropical lizard,
Tropidurus hispidus (Sauria: Iguanidae). Herpetologica 32(3):318–
323
Poulin R (1993) The disparity between observed and uniform distribu-
tions: a new look at parasite aggregation. Int J Parasitol 23:937–944
Poulin R (1996) Sexual inequalities in helminth infections: a cost of being
a male? Am Nat 147(2):287–295
Ribas SC, Rocha CFD, Teixeira-Filho PF, Vicente JJ (1998) Nematode
infection in two sympatric lizards (Tropidurus torquatus and Ameiva
ameiva) with different foraging tactics. Amphib-Reptil 19:323–330
Ribeiro LB, Freire EMX (2010) Thermal ecology and thermoregulatory
behaviour of Tropidurus hispidus and T. semitaeniatus in a caatinga
area of northeastern Brazil. Herpetol J 20:201–208
Ribeiro LB, Freire EMX (2011) Trophic ecology and foraging behavior
of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata,
Tropiduridae) in a Caatinga area of northeastern Brazil. Iheringia
Ser Zool 101(3):225–232
Parasitol Res
Ribeiro LB, Silva NB, Freire EMX (2012) Reproductive and fat body
cycles of Tropidurus hispidus and Tropidurus semitaeniatus
(Squamata, Tropiduridae) in a caatinga area of northeastern Brazil.
Rev Chil Hist Nat 85:307–320
Robar N, Burness G, Murray DL (2010) Tropics, trophics and taxonomy:
the determinants of parasite-associated host mortality. Oikos 119:
1273–1280
Rocha CFD (1995) Nematode parasites of the Brazilian sand lizard,
Liolaemus lutzae. Amphib-Reptil 16:412–415
Rocha WJSF, Chaves JM, Rocha CC, Funch L, Juncá FA (2005)
Avaliação ecológica rápida da Chapada Diamantina. In: Juncá FA,
Funch L, WJSF R (eds) Biodiversidade e Conservação da Chapada
Diamantina. Ministério do Meio Ambiente, Brasília, pp 29–45 411 p
Van Sluys M (1993) Food habits of the lizard Tropidurus itambere
(Tropiduridae) in southeastern Brazil. J Herpetol 27(3):347–351
Van Sluys M, Rocha CFD, Ribas SC (1994) Nematodes infecting the
lizard Tropidurus itambere in southeastern Brazil. Amphib-Reptil
15:405–408
Van Sluys M, Rocha CFD, Bergallo HG, Vrcibradic D, Ribas SC (1997)
Nematode infection in three sympatric lizards in an isolated frag-
ment of restinga habitat in southeastern Brazil. Amphib-Reptil 18:
442–446
Van Sluys M, Rocha CFD, Vrcibradic D, Galdino CAB, Fontes AF
(2004) Diet, activity and microhabitat use of two syntopic
Tropidurus species (Lacertilia: Tropiduridae) in Minas Gerais,
Brazil. J Herpetol 38(4):606–611
Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM (1993) Nematóides do
Brasil. Parte III: Nematóides de répteis. Rev Bras Zool 10(1):19–
168
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast
Brazil. Occ Pap Oklah Mus Nat Hist 1:1–29
Vitt LJ, Zani PA, Caldwell JP (1996) Behavioral ecology of Tropidurus
hispidus on isolated rock outcrops in Amazonia. J Trop Ecol 12:81–
101
Vrcibradic D, Cunha-Barros M, Vicente JJ, Galdino CAC, Hatano FH,
Van Sluys M, Rocha CFD (2000) Nematode infection patterns in
four sympatric lizards from a restinga habitat (Jurubatiba) in Rio de
Janeiro state, southeastern Brazil. Amphib-Reptil 21:307–316
Zamora-Camacho FJ, Reguera S, Rubiño-Hispán MV, Moreno-Rueda G
(2014) Eliciting an immune response reduces sprint speed in a liz-
ard. Behav Ecol 26:115–120