Nematode infection patterns in four sympatric lizards from a

restinga habitat (Jurubatiba) in Rio de Janeiro state,

southeastern Brazil

Davor Vrcibradic1,2, Mônica Cunha-Barros1 , Joaquim J. Vicente3 , Conrado A.C.

Galdino1 , Fábio H. Hatano1 , Monique Van Sluys1 , Carlos Frederico D. Rocha1
1 Setor de Ecologia, DBAV, I. Biologia, Universidade do Estado do Rio de Janeiro, R. São Francisco Xavier 524,
20550-013, Rio de Janeiro, RJ, Brazil
e-mail: cfdrocha@uerj.br
2 Pós-Graduação em Ecologia, Departamento de Zoologia, IB, Universidade Estadual de Campinas, C.P. 6109,

13081-970, Campinas, SP, Brazil

3 Departamento de Helmintologia, Instituto Oswaldo Cruz, 21045-900, Rio de Janeiro, RJ, Brazil

Abstract. Specimens of the four most abundant diurnal lizards (Tropidurus torquatus, Cnemidophorus littoralis,
Mabuya macrorhyncha and M. agilis) inhabiting the restinga of Jurubatiba, Rio de Janeiro state, Brazil were
examined for nematodes. Eight species of nematodes were found. Tropidurus torquatus had the richest (8 species)
and most diverse nematode fauna, whereas that of C. littoralis was the poorest (2 species) and less diverse.
Tropidurus torquatus also had the highest overall prevalence (92%) and mean infection intensity (37.2; standard
deviation 82.0; range 2-549). Similarities in nematode faunal composition between host species was generally
low, except between the two Mabuya species.

Introduction

One of the best studied single localities in Brazil concerning reptile helminth parasites
is the “restinga” (coastal sand-dune habitat) of Barra de Maricá, in Rio de Janeiro State,
which has been the subject of several recent studies (Rodrigues et al., 1990; Rodrigues,
1992; Ribas et al., 1995, 1998a, b; Rocha, 1995). Another restinga area, in the municipality
of Linhares, Espírito Santo state, has also been the subject of a study dealing with
nematodes associated to the three commonest diurnal lizard species in that area (Van Sluys
et al., 1997).
In the present study, we survey the nematode community associated with the four
commonest diurnal lizards of a restinga area in the Brazilian state of Rio de Janeiro for

c Koninklijke Brill NV, Leiden, 2000

® Amphibia-Reptilia 21: 307-316
308 D. Vrcibradic et al.

which no studies involving reptiles have yet been conducted. Our goals are: i) to determine
which nematode species are associated with each host species; ii) assess prevalences and
infection intensities (sensu Bush et al., 1997) for each host species, making interspeciŽ c
comparisons; iii) compare the diversities of the nematode faunas among host species;
iv) calculate the degree of similarity (overlap) of nematode faunas among host species.

Material and methods

Study area

The study was carried out at the restinga of Jurubatiba — more speciŽ cally in an
area adjacent to the Cabiúnas lagoon (22 ° 17¢S; 41° 41¢W), Carapebus municipality — in
northern Rio de Janeiro state, Brazil. Restingas are sand-dune open habitats found along
most of the Brazilian coastline (Eiten, 1992) and characterized by predominantly scrubby
and herbaceous xerophilic vegetation.Rainfall in the area averages 1164 mm annually, and
is highly seasonal, with mean monthly totals ranging from 41 mm in winter to 189 mm in
summer (Henriques et al., 1986). Mean monthly temperature varies from 29.7° C in January
to 20.0° C in July, with annual average of 22.6° C (Henriques et al., 1986).

Field data collection and analyses

We collected specimens of the four commonest diurnal lizard species in the restinga of
Jurubatiba: Tropidurus torquatus (Wied, 1820) (Tropiduridae), Cnemidophorus littoralis
Rocha, Araujo, Vrcibradic and Costa, 2000 (Teiidae), Mabuya agilis (Raddi, 1823) and
Mabuya macrorhyncha Hoge, 1946 (Scincidae). The lizards were collected with air ri es,
rubber bands, a noose, and glue-traps. Collections were carried out during March 1999,
though we also utilized data from Mabuya spp. collected on earlier visits to the area (in
April 1997 and in January, September, October and December 1998) to increase sample
sizes for those species. The study was, thus, entirely restricted to the wet season (see
Henriques et al., 1986), in order to minimize possible seasonal effects. Ri e shots were
always aimed at the head, so as not to damage internal organs, and lizards that were not
killed instantly were transferred to a plastic bag and euthanized with ether. For each lizard
collected, we took its snout-vent length (SVL) in the Ž eld using digital calipers (to the
nearest 0.1 mm), before injecting it with 10% formalin for preservation.
In the laboratory, upon dissecting each lizard, we identiŽ ed its sex and removed its entire
digestive tract, which we later carefully checked for the presence of helminths under a
stereomicroscope. We also checked for the presence of helminths within the lizards¢ body
cavities and lungs, after their entrails have been removed. Worms were preserved in 70%
alcohol. The nematodes were cleared in phenol and examined as temporary mounts.
Ecological terms used throughout the text follow Bush et al. (1997). Intersexual
differences in overall prevalence were tested using the Z-test for proportions (Zar, 1984).
Nematodes of sympatric lizards 309

Intersexual differences in infection intensity were tested using One-Way Analysis of

Variance (ANOVA), unless the distribution deviated from normality (which we veriŽ ed
using the Normal Distribution Goodness-of-Fit test), in which case we used the Mann-
Whitney test (Siegel, 1956). The relationship between overall infection intensity and
host-size (SVL) was tested for each species using linear regression. The diversity of
the nematode fauna associated with each host species was estimated using the mean
Brillouin¢s Diversity Index (HB, values calculated using natural logarithms; Magurran,
1988), considering only parasitized individuals. Between-species similarities in nematode
community composition were assessed using Sorensen¢s index for qualitative (C S ) and
quantitative(CN ) data (Magurran, 1988), using the abundance(sensu Bush et al., 1997) of
each nematode species for each host species in the latter case.
Voucher specimens of all helminth species recovered were deposited at the Coleção
Helmintológica do Instituto Oswaldo Cruz (CHIOC), the U.S. National Parasite Collection
(USNPC) and the helminthological collection of the Queensland Museum (QM) (see
Appendix).

Results

Eight nematode species were identiŽ ed from the lizards: Physaloptera lutzi Cristó-
faro, Guimarães and Rodrigues, 1976, Physaloptera retusa Rudolphi, 1819, and Physa-
lopteroides venancioi (Lent, Freitas and Proença, 1946) (Physalopteroidea; Physalopteri-
dae), Skrjabinelazia intermedia (Freitas, 1941) (Seuratoidea; Seuratidae), Strongyluris os-
cari Travassos, 1923 (Heterakoidea; Heterakidae), Subulura sp. (Subuluroidea; Subuluri-
dae), Hexametra boddaertii (Baird, 1860)(Ascaridoidea; Ascarididae), and an unidentiŽ ed
species of Acuariidae (Acuarioidea) (table 1). The latter two species were found only as
larvae. Due to their damaged state and/or young stage, some Physaloptera could not be
identiŽ ed to species and some nematodes could not be identiŽ ed to genus, and are thus
cited in the tables as “sp.” or “indeterminate.” Two adult male T. torquatus harbored, re-
spectively, 539 and 299 specimens of S. intermedia (among other nematodes), most of
them in the small intestine, but all other lizards harbored less than 100 specimens of any
given nematode species.
The only species of nematode found in all four host species was H. boddaertii (table 1).
Four nematodes (P. lutzi, S. intermedia, S. oscari and Subulura sp.) occurred in only one
host species ( T. torquatus). The most frequent site of infection used by nematodes in T.
torquatus and C. littoralis was the stomach, while for M. agilis it was the stomach and
stomach wall and for M. macrorhyncha it was the body cavity (table 1). The lizard species
having the richest associated nematode fauna was T. torquatus, which was infected by
all eight species (table 1). The mean number of nematode species per host (including both
infected and uninfected individuals)was 2.40 for T. torquatus, 0.82 for C. littoralis, 0.75 for
Table 1. Epidemiological data for six lizard species (sample sizes in parentheses) and their respective nematode parasites at the restinga of Jurubatiba, SE Brazil. For
310

each host species, the mean SVL and range (in mm), the prevalence (in absolute values and proportions) and intensity of infection (mean ± one standard deviation,
with range in parentheses) by nematodes (overall and by species) and the sites of infection used by each nematode species are given. Abbreviations for infection
sites are: OC = oral cavity; OE = oesophagus; SW = stomach wall; ST = stomach; SI = small intestine; LI = large intestine; LV = liver; LU = lung; BC = body
cavity. Infection sites are presented in decreasing order of prevalence per site (when prevalences are equal, sites are presented in decreasing orde r of mean intensity).
Asterisks indicate new host records (for species, genera or families).

Host species ( n) Mean SVL (range) Parasite species Prevalence (%) Mean intensity (range) Sites of infection
T. torquatus (62) 67.5 ± 14.92 (36.5-88.7) Physaloptera lutzi 51 (82.3) 11.9 ± 10.5 (1-58) ST, SI, OC, LI, OE, BC, SW
Physaloptera retusa 22 (35.5) 3.8 ± 4.2 (1-19) ST, BC, SI, OE, SW
Physaloptera sp. (indet.) 26 (41.9) 6.4 ± 8.9 (1-39) ST, BC, SI, OE, LI, OC, LU
Physalopteroides venancioi* 2 (3.2) 8.5 (5-12) ST, LI
Skrjabinelazia intermedia* 16 (25.8) 62.3 ± 146.7 (1-539) SI, ST, LI, LV, OE
Strongyluris oscari 38 (61.3) 3.2 ± 3.9 (1-15) SI, LI, BC, LU, ST
Subulura sp.* 1 (1.6) 5.0 SI, LI
Hexametra boddaertii (larvae)* 13 (21.0) 2.9 ± 3.2 (1-13) BC
Acuariidae indet. (larvae)* 4 (6.4) 3.8 ± 3.0 (1-8) SW
Nematoda indet. 16 (25.8) 2.6 ± 2.8 (1-11) ST, BC, SI, LI
total 57 (91.9) 37.2 ± 82.0 (2-549)

C. littoralis (22) 59.7 ± 9.65 (37.9-73.5) Physaloptera retusa 15 (68.2) 9.9 ± 9.2 (1-32) ST, SI, OE, OC
Physaloptera sp. (larvae) 2 (9.1) 1.5 (1-2) SW
Hexametra boddaertii (larvae)* 1 (4.5) 1.0 BC
Nematoda indet. 3 (13.6) 1.0 ST, SI
total 17 (77.3) 9.2 ± 9.6 (1-33)

M. macrorhyncha (40) 64.1 ± 9.00 (43.0-76.3) Physalopteroides venancioi* 8 (20.0) 1.1 ± 1.1 (1-2) ST, SI
Hexametra boddaertii (larvae) 16 (40.0) 7.4 ± 7.1 (1-25) BC, ST, LV
Acuariidae indet. (larvae)* 6 (15.0) 2.8 ± 1.7 (1-5) SW, LI, ST
Nematoda indet. 2 (5.0) 1.0 ST, SI
total 23 (57.5) 7.6 ± 7.0 (1-27)
M. agilis (8) 64.7 ± 6.72 (52.0-73.0) Physalopteroides venancioi* 3 (37.5) 1.7 ± 1.2 (1-3) ST
Hexametra boddaertii (larvae) 4 (50.0) 2.5 ± 3.0 (1-7) BC
Acuariidae indet. (larvae)* 5 (62.5) 6.6 ± 4.8 (1-13) SW
Nematoda indet. 1 (12.5) 1.0 SI
total 7 (87.5) 7.0 ± 3.9 (1-13)
D. Vrcibradic et al.
Nematodes of sympatric lizards 311

Table 2. Number and percentage (%; in parentheses) of infected individuals of each lizard species harboring one,
two, three, four or Ž ve nematode species simultaneously at the restinga of Jurubatiba, SE Brazil. UnidentiŽ ed
nematodes and unidentiŽ ed Physaloptera larvae and/or adults were ignored when other identiŽ able nematodes
and identiŽ able Physaloptera species, respectively, were also present.

Host species n Number of co-ocurring nematode species

1 2 3 4 5

T. torquatus 57 8 (14.0) 19 (33.3) 18 (31.6) 11 (19.3) 1 (1.8)

C. littoralis 17 16 (94.1) 1 (5.9) – – –
M. macrorhyncha 23 16 (69.6) 7 (30.4) – – –
M. agilis 7 3 (42.8) 2 (28.6) 2 (28.6) – –

Table 3. Diversity of the nematode fauna for each host species and similarities of nematode faunas among
each species-pair at the restinga of Jurubatiba, SE Brazil. Values on the diagonal represent the mean Brillouin¢s
diversity index (HB) ± s for each host species. Values above and below the diagonal represent Sorensen¢s index
of similarity for quantitative (CN ) and qualitative data (CS ), respectively.

Species T. torquatus C. littoralis M. macrorhyncha M. agilis

T. torquatus 0.203 ± 0.140 0.037 0.059 0.062

C. littoralis 0.40 0.004 ± 0.017 0.010 0.008
M. macrorhyncha 0.55 0.40 0.039 ± 0.074 0.398
M. agilis 0.55 0.40 1.00 0.105 ± 0.116

M. macrorhyncha, and 1.86 for M. agilis. Most individuals of each lizard species harbored
only one nematode species, with T. torquatus being the exception (table 2).
In T. torquatus, host SVL was positively and signiŽ cantly correlated with overall
infection intensity (r 2 = 0.09; P < 0.05; n = 57) and with number of nematode species
per host (r 2 = 0.32; P = 0.001; n = 57); such correlations were not signiŽ cant for the
remaining species (P > 0.05 for all). Mean infection intensity did not differ among sexes
in either C. littoralis (ANOVA; F1,15 = 1.84, P > 0.1) or M. macrorhyncha (ANOVA;
F1,21 = 0.19, P > 0.1), but in T. torquatus it was signiŽ cantly higher for males (52.5;
s = 102.0; range 2-549) than for females (13.6; s = 9.7; range 2-30) (Mann-Whitney
test for large samples; z = 2.84, P < 0.005). Intersexual difference in overall nematode
prevalence was not signiŽ cant for T. torquatus (males: 35/37; females: 20/23; Z = 1.04,
P > 0.1) nor C. littoralis (males: 6/9; females: 11/13; Z = ­ 0.99, P > 0.1), and was
only marginally signiŽ cant for M. macrorhyncha (males: 14/20; females: 9/20; Z = 1.6,
P = 0.055). Intersexual differences were not tested for M. agilis due to the small sample
size.
The species harboring the most diverse nematode fauna was T. torquatus, while that
harboring the least diverse was C. littoralis (table 3). Qualitative similarities in nematode
faunas among host species were relatively high, but quantitativesimilarities were generally
low, except between the two Mabuya species (table 3).
312 D. Vrcibradic et al.

Discussion

The presences of P. venancioi and Acuariidae in T. torquatus, M. macrorhyncha and

M. agilis, of H. boddaertii in T. torquatus and C. littoralis, and of the genus Subulura
Molin, 1860 in T. torquatus all represent new host records. Furthermore, although Vicente
(1981) reported S. intermedia from T. torquatus of Salvador, Bahia, NE Brazil, the
geographic distribution of the torquatus complex given by Rodrigues (1988) suggests that
the species concerned must have been either T. hispidus or T. hygomi, or both. Thus, our
report also represents the Ž rst actual record of S. intermedia infecting T. torquatus sensu
strictu.
At Jurubatiba, T. torquatus appears to be the speciŽ c host for P. lutzi and S. oscari, while
C. littoralis is apparently the speciŽ c host for P. retusa. On the other hand, the lizards here
studied are not the Ž nal hosts for all nematode species associated to them: although the
larvae of H. boddaertii and of Acuariidae have previously been recorded in lizards (Roca
et al., 1986; Roca, 1995; Vrcibradic et al., 1999), adults of those worms are known only as
parasites of snakes (Sprent, 1978; Baker, 1987) and birds (Anderson, 1992), respectively;
thus, lizards may represent accidental or paratenic hosts for such nematodes. The presence
of Subulura sp. in T. torquatus is also probably accidental, since this nematode genus is
typical of mammals and birds (Anderson, 1992); even though a new Subulura species
has recently been reported to occur with high prevalences and intensities in Tropidurus
nanuzae from Minas Gerais, Brazil (Van Sluys et al., in press), this is not the case for our
T. torquatus sample, in which only one lizard harbored such worms.
We observed some interesting trends among intra- and interspeciŽ c patterns of the
nematode faunas of the lizard guild studied. For each host species, the nematode fauna
appeared to be dominated by one particular species (with the exception of M. agilis,
though this might be due to the small sample size). It is curious that in the two Mabuya
species the commonest nematodes were species which do not use the lizards as Ž nal hosts
(see above). Nevertheless, there was a clear trend for such species ( Hexametra and the
acuariid) to occur preferentially in the skinks, perhaps because they may have a greater
susceptibility to infection by such worms than the other sympatric lizards and/or may be
the preferential prey of their Ž nal hosts (presumably snakes and birds, respectively). The
only species which used Mabuya spp. as Ž nal hosts ( P. venancioi) had a high speciŽ city
for these hosts in the area (evidenced by their absence or very rare occurrence in the
remaining lizard species), but had relatively low prevalences compared to the speciŽ c
predominant nematodes of T. torquatus and C. littoralis. Since P. venancioi is known
to infect toads (Baker, 1987), it is also possible that the speciŽ c host for this species
in the area is an amphibian, despite the fact that it also occurs in lizards. Tropidurus
torquatus had the richest and most diverse nematode fauna among the species studied,
which seems uncontestable even allowing for the fact that the sample for this species
was larger than for the other three (which would increase the probability of occurrence
of rare species, i.e. Subulura sp. and P. venancioi). It was also the only host species in
Nematodes of sympatric lizards 313

which two nematode species attained core status (i.e. prevalences > 50%; see Aho, 1990).
The Jurubatiba population of T. torquatus harbors a richer nematode fauna than any other
Tropidurus population so far studied (Prieto, 1980; Vicente, 1981; Van Sluys et al., 1994,
1997; Roca, 1997; Cruz et al., 1998; Ribas et al., 1998a) and its mean species richness per
individual(2.4) is very close to the highest value (2.5; including non-nematode helminths)
observed by Aho (1990) among 100 studied populations of lizards in nine families. The
maximum number of helminth species per host for lizards (in nine families) and reptiles
(155 species surveyed) found by that author in the same survey were respectively Ž ve
and ten, while the population of T. torquatus studied here harbored a total of 11 helminth
species, eight of which were nematodes (the remaining three were a cestode, a digenean
and an acathocephalan). The helminth fauna of the referred lizard population thus seems
unusually rich for squamatans, but it should not be ignored that Aho (1990) compiled data
mostly from North American herpetofauna, whose helminth comunity patterns may differ
from those of tropical forms.
Although Aho (1990) suggested that, among reptiles and amphibians, wide-foraging
forms tend to harbor richer and more complex helminth communities than sit-and-wait
foragers, the lizard guild we studied showed the opposite trend: the wide-foraging teiid
had the most depauperate nematode fauna, while the sit-and-wait tropidurid had the richest
and most diverse one, with those of the scincids (active foragers with limited vagility
and movimentation; e.g. Anderson, 1993; Vitt, 1995) being intermediate. It is possible
that the feeding habits of those species may be partly reponsible for such patterns; Aho
(1990), for instance, cited selectivity and breadth of diet as factors in uencing the richness
and size of helminth communities in reptiles and amphibians. The diets of the four
species studied in Jurubatiba (unpubl. data) are generally similar to those of corresponding
conspeciŽ c populations in Barra de Maricá, where T. torquatus has the most diversiŽ ed
diet, including both arthropods and plant material (Araújo, 1991; Fialho et al., 2000), the
skinks have diets including various arthropods but very little plant food (Vrcibradic and
Rocha, 1996), and C. littoralis has the most specialized diet, centered on termites (Araújo,
1991; Rocha et al., 2000). Thus, it is possible that nematode diversity may somewhat
parallel food niche breadth in the lizard guild we studied. Our data point to a contradiction
in Aho¢s hypothesis concerning the relationship between foraging tactics and complexity
of helminth communities, since wide foragers tend to have both great vagility (which may
expose them to a wide range of parasites) and specialized diets (which would have the
opposite effect). Moreover, wide-foraging lizards frequently consume many insect larvae
(e.g. Bergallo and Rocha, 1994; Vitt, 1995; Vitt et al., 1997), which are likely to be less
parasitized than adult insects, whereas sit-and-wait foragers tend to feed largely on ants,
which usually carry lots of nematodes (L.J. Vitt, pers. comm.). Thus, it seems that Aho¢s
logic may be seriously  awed, at least with regard to lizards.
Aho (1990) also mentioned the importance of host geographical range and local
abundance for determining local helminth faunal richness. Since T. torquatus is the most
abundant lizard species in the area (pers. obs.) and has a wide geographic distribution
314 D. Vrcibradic et al.

(Rodrigues, 1988), a combination of these traits with a generalized mixed diet of animal
and plant matter may be responsible for it harboring a relatively rich and diverse nematode
community in the area.
The similarities of nematode faunas among host species were relatively high in quali-
tative terms, apparently due to the reduced number of nematode species. In quantitative
terms, however, similarities were usually low, except for the two congeneric skinks. This
agrees with Aho¢s (1990) observation that similarities in helminth faunas among closely
related sympatric hosts are usually high, commonly equalling or exceeding values obtained
for interpopulational comparisons of a single host species.
In short, the results of our survey generally agree with the patterns cited by Aho (1990)
as characteristic of helminth faunas of reptiles and amphibians, such as a relatively low
number of species (compared to other vertebrate hosts) and dominance of generalist
species. The latter term would apply even to the species found only in T. torquatus, since
those species (with the exception of Subulura sp.) are widespread parasites of several
Tropidurus species (e.g. Vicente, 1981; Van Sluys et al., 1994; 1997; Roca, 1997; Ribas
et al., 1998a). Also, it seems that T. torquatus may be a key host species for the lizard
nematode community of Jurubatiba, and that the presence of that species is fundamental
for maintaining the richness and complexity of such community as a whole.

Acknowledgements. This study is a portion of the results of the “Programa de Ecologia, Conservação e Manejo
de Ecossistemas do Sudeste Brasileiro” and of the Southeastern Brazilian Vertebrate Ecology Project (Laboratory
of Vertebrate Ecology), both of the Setor de Ecologia, Instituto de Biologia, Universidade do Estado do Rio de
Janeiro. Permission to collect the lizards was conceded by the Instituto Brasileiro do Meio Ambiente e Recursos
Naturais Renováveis — IBAMA (Permit # 096/99-DIFAS). Charles R. Bursey and John F.A. Sprent kindly helped
to identify some of the helminths. Laurie J. Vitt and an anonymous referee reviewed the manuscript and gave
valuable suggestions. The study was partially supported by a grant from the Fundação de Amparo à Pesquisa
do Estado do Rio de Janeiro — FAPERJ (Process E-26/170.385/97 — APQ1) and by research grants from
the Conselho Nacional de Desenvolvimento CientíŽ co e Tecnológico (CNPq) to C.F.D.R. and M.V.S. (process
# 300819/94-3, and 301117/95-0, respectively).

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Received: November 10, 1999. Accepted: February 22, 2000.

Appendix
Voucher specimens of helminths recovered from Tropidurus torquatus, Cnemidophorus littoralis, Mabuya
macrorhyncha, and Mabuya agilis from the restinga of Jurubatiba, Rio de Janeiro, Brazil, deposited at the
Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), the U.S. National Parasite Collection (USNPC)
and the helminthological collection of the Queensland Museum (QM). Samples marked with an asterisk represent
mounted slides; the remaining material is preserved in 70% alcohol.
Physaloptera lutzi — CHIOC 33857; 34209a-d*
Physaloptera retusa — CHIOC 33858; USNPC 89089
Physalopteroides venancioi — CHIOC 34210*; USNPC 89080; 89084
Skrjabinelazia intermedia — CHIOC 33861; 34208a-d*
Strongyluris oscari — CHIOC 34859-60
Subulura sp. — CHIOC 33862
Hexametra boddaertii — USNPC 89083; 89088; QM 9665-67
Acuariidae indet. — USNPC 89081; 89090