Zoological Studies 51(8): 1454-1463 (2012)

Community Structure of Helminth Parasites of Leptodactylus bufonius

(Anura: Leptodactylidae) from Northeastern Argentina
Monika Inés Hamann*, Arturo Ignacio Kehr, and Cynthya Elizabeth González
Consejo Nacional de Investigaciones Científicas y Técnicas, Centro de Ecología Aplicada del Litoral, Ruta 5 Km 2.5, W 3400 AMD,
Corrientes, Argentina

(Accepted September 19, 2012)

Monika Inés Hamann, Arturo Ignacio Kehr, and Cynthya Elizabeth González (2012) Community structure of
helminth parasites of Leptodactylus bufonius (Anura: Leptodactylidae) from northeastern Argentina. Zoological
Studies 51(8): 1454-1463. The main goals of this study were to determine the richness and diversity of helminth
parasites of Leptodactylus bufonius at the component and infracommunity levels and evaluate whether the
composition of the parasite community is determined by biotic and abiotic factors. In total, 76 specimens were
collected near the city of Corrientes, Corrientes Province, Argentina. The helminth component community in L.
bufonius in this area was comprised of 16 species. The predominant groups of helminth parasites (larval and
adult) were trematodes (50%) followed by nematodes (38%); other groups of parasites were represented by only
1 species (Cestoda: Cylindrotaenia sp. and Acanthocephala: Centrorhynchus sp.). Helminth species showed
unequal abundances with a typical aggregated pattern of distribution. The prevalence of infection was 93% in
specimens of L. bufonius examined. The main helminth species in the community was Aplectana hylambatis
(importance value: I = 96.41), followed by Catadiscus inopinatus (I = 2.32). At the infracommunity level, the
mean individual species richness was no more than 3 helminth species per infected host; the diversity and
equitability of helminths were 0.18 ± 0.14 and 0.44 ± 0.32, respectively. The host body size was the main factor
in determining the infrapopulation structure of various helminth species. Species richness was significantly and
positively correlated with the host body size. Data revealed significant positive correlations between helminth
species (Cat. inopinatus/Centrorhynchus sp. and A. hylambatis/Centrorhynchus sp.). A significant negative
correlation was observed between A. hylambatis and Cos. podicipinus. Only 2 associations were found among
the 7 species considered. The parasite community of L. bufonius showed wide variations in its helminth fauna
and included helminths of aquatic and terrestrial habitats. The correspondence between host habits and
parasite biology is reflected in the parasites harbored by these amphibian hosts.
http://zoolstud.sinica.edu.tw/Journals/51.8/1454.pdf

Key words: Ecology, Parasites, Amphibian, Neotropical realm.

S tudies on helminth communities of McKenzie 2007, King et al. 2008, Marcogliese et

American amphibians have increased in recent al. 2009). At the same time, intrinsic factors such
years. These ecological studies suggested that as the host body size play important roles in the
the community structure depends on interactions of helminth parasite composition (Goater et al. 1987,
extrinsic factors such as the characteristic habitat Aho 1990, Tucker and Joy 1996, McAlpine 1997,
of the host (Aho 1990, Muzzall 1991, McAlpine Joy and Pennington 1998, Gillilland and Muzzall
1997, Kehr et al. 2000, Bolek and Coggins 2003, 1999, Bolek and Coggins 2001, Hamann et al.
Luque et al. 2005, Hamann et al. 2006a b, Yoder 2006a b 2010, Santos and Amato 2010).
and Coggins 2007, Campião et al. 2009) and In Argentina, despite the existence of a highly
anthropogenic perturbations (Hamann et al. 2006b, diverse amphibian fauna (Frost 2011), studies

*To whom correspondence and reprint requests should be addressed. Tel: 54-379-4454418. Fax: 54-379-4454421.
E-mail:monika_hamann@yahoo.com

1454
 Hamann et al. – Ecology of Parasites of Amphibians 1455

related to the patterns and processes underlying is intermediate between that of an ambush
the structure of helminth parasite communities predator and an actively foraging predator (Duré
are just beginning (Hamann 2011). In this sense, and Kehr 2004).
it is necessary to examine more amphibian hosts The main goals of this study were to: 1)
to ascertain if amphibian helminth communities determine the richness and diversity of parasites
generally correspond to the pattern described at the component and infracommunity levels;
by Aho (1990). That author recognized that 2) identify and examine species affinities in the
the parasite communities of amphibians are helminth communities; and 3) analyze relationships
considered highly variable, depauperate, and between helminths and frog characteristics.
non-interactive, and found that some of the most
important factors affecting the structure of helminth
communities include, as suggested by Kennedy et MATERIALS AND METHODS
al. (1986), the various host habitats (e.g., terrestrial
and aquatic), and different aspects of the host Study area
biology (e.g., diet, age, sex ratio, and vagility) and
of the life cycle of the parasite. Additionally, local The study area was located ~15 km east of
availability of parasitic species and colonization the city of Corrientes (27°30'S, 58°45'W). Although
abilities of parasites can affect parasite diversity limited to 30 ha, the predominant vegetation
(Esch et al. 1988), which in turn could affect the in the study area is forest with an herbaceous
degree of interspecific interaction and distribution strata composed of grasslands, numerous cacti,
of parasite species among infracommunities (see and terrestrial bromeliads. The habitat is also
Holmes and Price 1986). Thus, the present study characterized by temporary, semipermanent,
attempted to characterize helminth parasites of and permanent ponds. The aquatic vegetation
the Vizcacheras’ white-lipped frog Leptodactylus in a permanent pond (30 m long, 15 m wide, and
bufonius Boulenger, 1894 at the component and 0.8 m deep) sampled in this study consisted of
infracommunity levels. floating and submerged hydrophytes, surrounded
González and Hamann (2006) reported by several species of grasses. The mean annual
a preliminary study of the helminth parasite temperature for the area is 23°C, and the mean
composition of L. bufonius; nevertheless, that annual precipitation is 1500 mm, without a well-
study did not analyze the ecological implications defined dry season, although periods of rain
of different biotic and abiotic factors. Based on shortage occur every 4-6 yr (Carnevali 1994).
certain assumptions, the approach employed
in the current study predicted that (1) helminth Collection and examination of amphibians
parasite species are determined by the particular
habitat and habits of the host; (2) the depauperate Seventy-six specimens of Leptodactylus
community is related to the host being ectothermic; bufonius collected between Sept. 2002 and
and (3) large amphibians commonly have more Nov. 2010 were examined for the presence of
individuals and species of helminths than do helminths. Frogs were hand-captured, mainly
smaller amphibians. These premises were tested at night, using the sampling technique defined
by analyzing specific compositions of larval and as the “visual encounter survey” (Crump and
adult helminths present in L. bufonius. This Scott 1994). Specimens were transported live
anuran species occurs in southern Bolivia to to the laboratory, killed in a chloroform (CHCL 3)
northern Argentina, Paraguay, and central Brazil solution, and their snout-vent length (SVL) and
(Frost 2011); the adult frog lives and breeds in body weight (BW) were recorded. At necropsy,
burrows (i.e., a fossorial habitat) and leaves them hosts were sexed and the esophagus, stomach,
only to forage. The breeding season occurs in gut, lungs, liver, urinary bladder, kidneys, body
spring, summer, and autumn; eggs are placed in cavity, musculature, integument, and brain were
a mass of foam in the nest. Hatching and caring examined for parasites. Helminths were observed
for embryos occur in the nest, and when the nest in vivo, counted, killed in hot distilled water, and
is flooded by rainfall, the larvae escape to the preserved in 70% ethyl alcohol. Digeneans,
surrounding aquatic habitat (see Philibosian et cestodes, and acanthocephalans were stained
al. 1974). Leptodactylus bufonius is considered with hydrochloric carmine, cleared in creosote, and
a generalist feeder, with a diet dominated by mounted in Canada balsam. Nematodes were
isopterans and coleopterans; its foraging strategy cleared in glycerin or lactophenol, and examined
1456 Zoological Studies 51(8): 1454-1463 (2012)

as temporary mounts. Systematic determination of AjBj

Ij = (Mj) 100
the helminths was carried out following Yamaguti
Σ
16
i=1 AiBi
(1961 1963 1971 1975), Anderson et al. (1974),
Gibson et al. (2002), and Jones et al. (2005).
Specimens of parasite species were deposited where A j is number of individual parasites in
in the Helminthological Collection of Centro de species j, B j is number of hosts infected with
Ecología Aplicada del Litoral (CECOAL), Consejo parasite j, and Mj is a maturity factor equal to 1.0 if
Nacional de Investigaciones Científicas y Técnicas at least 1 mature specimen of species j was found
(CONICET), Corrientes Province, Argentina and equal to 0 otherwise.
(with accession numbers CECOAL, 04011507, Helminth communities were classified
Glypthelmins repandum (Rudolphi, 1819); at the infracommunity level (i.e., all helminth
10021702, Catadiscus inopinatus Freitas, 1841; infrapopulations within a single Vizcacheras’ white-
10022306, Haematoloechus longiplexus Stafford, lipped frog) and component community level (i.e.,
1902; 06022411, Bursotrema tetracotyloides all of the different helminth infrapopulations within
Szidat, 1960; 04011507, Travtrema aff. stenocotyle all Vizcacheras’ white-lipped frogs in our area)
Cohn, 1902; 06022413, Opisthogonimus sp.; (Esch et al. 2002). Spearman’s rank test (rs) was
09102809, Strigea sp.; 06030607, Cylindrotaenia used to assess the relationship between the host
sp.; 09102808, Cosmocerca podicipinus Baker and body size and infracommunity descriptors and
Vaucher, 1984; 10022310, Cos. parva Travassos, calculate possible correlations between the host
1925; 10113010, Aplectana hylambatis (Baylis, body size and parasite abundances. Species
1927); 02123272, Aplectana sp.; 08022601, co-variation was analyzed with the Spearman
Rhabdias elegans Gutierrez, 1945; 02113228, test correlation. Species associations were
Ortleppascaris sp.; and 10021703, Centrorhynchus analyzed using a Chi-squared test (χ2), with the
sp.). Yates correction for continuity. The variance/
mean ratio was used to determine the spatial
Statistical analysis distribution of parasites. The software used was
Xlstat 7.5 (Addinsoft 2004). For correlations and
The infection prevalence, intensity, and associations, only species that had at least 10%
abundance were calculated for helminths following occurrences in each of the amphibian populations
Bush et al. (1997). Measurements of community (7 species) were considered.
richness and diversity employed included the total
number of helminth species (= richness), Shannon
index (H´) (Shannon and Weaver 1949), and RESULTS
evenness (J’) as H´/H´ maximum (Pielou 1966,
Zar 2010). The mean helminth species richness Community structure analysis
is the sum of helminth species per individual frog,
including uninfected individuals, divided by the total The infection prevalence was 93% for the
sample size. The diversity index was used with 76 frogs examined. The helminth component
decimal logarithms (log10). The Berger-Parker community of this frog population consisted of 16
index of dominance (d) was used to determine species of helminths (Table 1). The predominant
the most abundant species (Magurran 2004). All groups of helminth parasites (larval and adult)
values are expressed as the mean ± standard were trematodes (50%) followed by nematodes
deviation (SD). The helminth community structure (38%); other groups of parasites were represented
was examined according to the methodology by only 1 species (Cestoda: Cylindrotaenia sp. and
outlined by Thul et al. (1985), where helminth Acanthocephala: Centrorhynchus sp.). In contrast,
species are classified into 4 groups (dominant, comparison of the richness of adult helminths
codominant, subordinate, and unsuccessful) by showed an inverted pattern: 56% nematodes and
taking into account the prevalence, intensity, and 33% trematodes. Helminth diversity was 0.51 and
maturation factor, which is related to the degree evenness was 0.42. The nematode A. hylambatis
of host specificity. The importance value (I) was was the dominant species (d = 0.71). Most
calculated for each helminth species as follows: helminth parasites (0.75%) showed aggregated
patterns of distribution. Parasites were found in the
small intestine, large intestine, lungs, mesenteries,
and body cavity with a prevalence of > 10% (Table
 Hamann et al. – Ecology of Parasites of Amphibians 1457

1). Of all adult specimens of helminths examined, direct life cycles (Cylindrotaenia sp., Cosmocerca.
the primary site of infection was the digestive podicipinus, Cos. parva, A. hylambatis, Aplectana
tract, except for Haematoloechus longiplexus and sp. and R. elegans) (Table 2).
Rhabdias elegans that were found in the lungs. At the infracommunity level, the mean
Three species were assumed to have indirect life helminth richness was 2.49 ± 1.43 (maximum,
cycles (Glypthelmins repandum, Cat. inopinatus, 7) species per infected frog. Multiple infections
and H. longiplexus), and 6 were assumed to have were common, with 0, 1, 2, 3, 4, 5, and 7 species

Table 1. Helminths recorded in L. bufonius. The dispersion (S2/x), dominance (d), prevalence (%), mean
abundance (MA) ± 1 standard deviation (S.D.), mean intensity (MI) ± 1 S.D., and site of infection are shown

Helminth Stage S2/x d Percent (%) MA ± 1 S.D. MI ± 1 S.D. Siteb

Catadiscus inopinatus Adult 12.91 0.04 32.89 1.61 ± 4.56 4.88 ± 6.87 Li
Glypthelmins repandum Adult 6.04 0.01 15.79 0.46 ± 1.67 2.92 ± 3.23 Si
Haematoloechus longiplexusa Adult 1.00 0.00 1.32 0.01 ± 0.11 1.00 ± 0.00 Lu
Bursotrema tetracotyloidesa Larva 22.90 0.01 1.32 0.30 ± 2.62 23.00 ± 0.00 K
Travtrema aff. stenocotylea Larva 25.58 0.02 7.89 0.74 ± 4.35 9.33 ± 12.63 BM
Opisthogonimus sp.a Larva 90.74 0.10 13.16 4.08 ± 19.24 31.00 ± 44.49 BM
Strigea sp.a Larva 12.53 0.01 9.35 0.38 ± 2.18 9.67 ± 5.56 B
Strigeidae gen. sp.a Larva 1.00 0.00 1.32 0.01 ± 0.11 1.00 ± 0.00 B
Aplectana hylambatis Adult 42.45 0.71 73.68 29.80 ± 35.57 40.45 ± 35.87 Si Li
Aplectana sp. Adult 6.43 0.01 3.95 0.21 ± 1.16 5.33 ± 2.63 Li
Cosmocerca podicipinus Adult 6.89 0.02 19.74 0.72 ± 2.23 3.67 ± 3.79 Si Li
Cosmocerca parva Adult 0.85 0.00 6.58 0.07 ± 0.25 1.00 ± 0.00 Li
Rhabdias elegans Adult 3.11 0.01 15.79 0.38 ± 1.09 2.42 ± 1.61 Lu
Ortleppascaris sp. Larva 6.94 0.00 3.95 0.16 ± 1.05 4.00 ± 3.56 L
Cylindrotaenia sp.a Adult 1.00 0.00 1.32 0.01 ± 0.11 1.00 ± 0.00 Si
Centrorhynchus sp. Larva 15.33 0.08 46.05 3.18 ± 6.98 6.91 ± 8.95 SM
a
New host. bSite of infection: K, kidneys; B, body cavity; P, pharyngeal zone; Si, small intestine; Li, large intestine; S, serous of
stomach; M, mesenteries; Lu, lungs; L, liver.

Table 2. Summary of helminth life cycles in L. bufonius from Corrientes Province, Argentina

Host
Helminth Referenceb
Second intermediate Definitive

Travtrema aff. stenocotyle Amphibian Snake Ostrowski de Núñez (1979a)

Opisthogonimus sp. Amphibian Snake Grabda-Kazubska (1963)
Bursotrema tetracotyloides Amphibian Mammal Yamaguti (1975)
Strigea sp. Amphibian Bird Yamaguti (1975)
Strigeidae gen. sp. Amphibian Bird, mammal Yamaguti (1975)
Glypthelmins repandum Amphibian Amphibian Smyth and Smyth (1980)
Haematoloechus longiplexus Aquatic insect larva Amphibian Smyth and Smyth (1980)
Catadiscus inopinatus Aquatic vegetation Amphibian Ostrowski de Núñez (1979b)
Cosmocerca podicipinus - Amphibian Fotedar and Tikoo (1968)
Cosmocerca parva - Amphibian Fotedar and Tikoo (1968)
Rhabdias elegans - Amphibian Anderson (2000)
Aplectana hylambatis - Amphibian Anderson (2000)
Aplectana sp. - Amphibian Anderson (2000)
Ortleppascaris sp. Amphibiana Snake Anderson (2000)
Centrorhynchus sp. Amphibiana Bird Schmidt (1985)
Cylindrotaenia sp. - Amphibian Prudhoe and Bray (1982)
a
Paratenic host. bReferences: life cycles of congener species or species of the same family.
 1458 Zoological Studies 51(8): 1454-1463 (2012)

occurring in 5, 15, 21, 15, 15, 4, and 1 frogs, Infection in relation to host body size
respectively. The observed distribution of helminth
infracommunity species richness showed a good The total lengths of frogs ranged 21.00-
fit to the Poisson distribution (χ2 = 5.29, d.f. = 6, 59.00 (43.65 ± 8.73) mm, and their weights
p = 0.507) (Fig. 1). The mean helminth diversity ranged 0.93-38.10 (10.16 ± 5.38) g. The helminth
was 0.18 ± 0.14, and evenness was 0.44 ± 0.32. infracommunity species richness was significantly
correlated with the host body size (length: rs = 0.31,
Species infracommunity affinities n = 71, p < 0.05; and weight: rs = 0.32, n = 71,
p < 0.05); significant correlations were also found
Two correlations between species were between the abundances of 5 helminth species
positive and significant: Cat. inopinatus/ and the host body size (Table 4).
Centrorhynchus sp. and A. hylambatis/ Lengths of female frogs ranged 25.50-58.00
Centrorhynchus sp., and one was negative and (42.41 ± 8.71) mm, and weights ranged 1.35-
significant: Cos. podicipinus/A. hylambatis (Table 19.90 (9.25 ± 4.81) g. These variables were
3). Only 2 associations were found among not significantly correlated with infracommunity
the 7 species considered: Cat. inopinatus/ descriptors; however, the host body size showed
Centrorhynchus sp. (χ2 = 3.8; d.f. = 1; p < 0.05) a significant correlation with the abundances of
and A. hylambatis/Centrorhynchus sp. (χ2 = 12.3; 3 helminth parasites (Table 4). Lengths of male
d.f. = 1; p < 0.05). frogs ranged 21.00-59.00 (44.26 ± 8.68) mm,
and weights ranged 0.93-38.10 (10.61 ± 5.59) g.
These variables were significantly correlated with
25 the helminth infracommunity species richness, and
Observed
Expected also with abundances of 4 nematode species (Table
20 4).

Infection in relation to host specificity

Number of frogs

15

Helminth species were classified according to

10 community importance values (Table 5); 2 species
were strongly characteristic of the community
5 (dominant), and 5 species significantly contributed
to the community, although to a lesser degree.
Two species occurred infrequently and did not
0
0 1 2 3 4 5 6 7 significantly contribute to the community, and 7
Number of helminth species species that were able to enter the host but not to
reach maturity contributed little to the community
Fig. 1. Observed and expected frequency distributions of and are characteristic of another host.
helminth infracommunity species richness in L. bufonius,
according to a Poisson distribution pattern.

Table 3. Co-variation based on Spearman coefficient correlations (rs) among 7 common helminth species in
L. bufonius from Corrientes Province, Argentina

Species Table ID (1) (2) (3) (4) (5) (6) (7)

Rhabdias elegans (1) 1

Aplectana hylambatis (2) 0.042 1
Cosmocerca podicipinus (3) -0.037 -0.274* 1
Catadiscus inopinatus (4) -0.031 0.214 -0.120 1
Opisthogonimus sp. (5) -0.095 0.222 -0.088 0.213 1
Glypthelmins repandum (6) 0.166 -0.231 -0.053 0.002 -0.181 1
Centrorhynchus sp. (7) 0.166 0.572* -0.211 0.268* 0.098 -0.113 1

*Significant at p < 0.05.

 Hamann et al. – Ecology of Parasites of Amphibians 1459

DISCUSSION (Table 6). Species causing helminth infections

in L. bufonius showed unequal abundances and
In Argentina, previous reports found that a typical aggregated pattern of distribution for
the helminth communities of leptodactylids many of the parasites (0.75%). The clumped
predominantly consisted of trematodes (or overdispersed) distributions of most parasite
(Hamann et al. 2006a b). In the present study, species observed in L. bufonius were inferred
Leptodactylus bufonius also presented large by the heterogeneity between these amphibians
numbers of trematode species; nevertheless, when in terms of their susceptibility to infection, i.e.,
only adult helminths were compared, nematode possibly due to differences related to age, sex, and
species showed high richness, and this result was the immunological state (Anderson and Gordon
similar to previous studies in different species 1982); and by its exposure to highly aggregated
of the genus Leptodactylus from South America infective stages (Esch et al. 1988).

Table 4. Spearman correlation (rs) between helminth parasites and the body size of L. bufonius from
Corrientes Province, Argentina

Helminth parasite All frogs Frog♂ Frog♀

Weight Length Weight Length Weight Length

Infracommunity descriptors
Diversity 0.206 0.193 0.216 0.215 0.137 0.074
Evenness -0.030 -0.054 -0.001 -0.023 -0.089 -0.135
Richness 0.310* 0.324* 0.313* 0.342* 0.277 0.228
Parasitic abundance
Rhabdias elegans 0.355* 0.217 0.434* 0.257 0.206 0.130
Aplectana hylambatis 0.512* 0.549* 0.428* 0.537* 0.584* 0.497*
Cosmocerca podicipinus -0.485* -0.400* -0.460* -0.430* -0.420* -0.327
Catadiscus inopinatus 0.209 0.239* 0.120 0.219 0.328 0.252
Opisthogonimus sp. 0.099 0.123 0.048 0.068 0.205 0.256
Glypthelmins repandum 0.145 0.033 -0.064 -0.075 0.481* 0.276
Centrorhynchus sp. 0.283* 0.418* 0.258 0.406* 0.296 0.373

*Significant at p < 0.05.

Table 5. Importance values (I) and classification of helminth parasite species in L. bufonius from Corrientes
Province, Argentina

Helminth species I Classification

Aplectana hylambatis 96.410 Dominant

Catadiscus inopinatus 2.318 "
Cosmocerca podicipinus 0.627 Codominant
Glypthelmins repandum 0.319 "
Rhabdias elegans 0.265 "
Aplectana sp. 0.036 "
Cosmocerca parva 0.019 "
Haematoloechus longiplexus 0.001 Subordinate
Cylindrotaenia sp. 0.001 "
Bursotrema tetracotyloides 0.000 Unsuccessful pioneer
Travtrema aff. stenocotyle 0.000 "
Opisthogonimus sp. 0.000 "
Strigea sp. 0.000 "
Strigeidae gen. sp. 0.000 "
Ortleppascaris sp. 0.000 "
Centrorhynchus sp. 0.000 "
1460 Zoological Studies 51(8): 1454-1463 (2012)

The helminth community in the present trematode parasite life cycles compared to other
study was predominantly composed of generalist anurans in the same area, e.g., Leptodactylus
species; however, A. hylambatis which was one chaquensis (Leptodactylidae) and Scinax nasicus
of the most important species (I = 96.41), uses (Hylidae) which show high infection rates by
L. bufonius as a specific definitive host; infection Metacercariae that complete their development in
by this species is comparatively rare in other mammals (e.g., Bursostrema tetracotyloides) and
sympatric amphibians (Hamann et al. 2006a reptiles (e.g., Opisthogonimus sp.) (Hamann et al.
b). The high prevalence of A. hylambatis found 2006b 2010). Adult trematodes were represented
in L. bufonius agrees with a previous report by by species with complex life cycles, where infection
Bursey et al. (2001) for other American terrestrial occurs by skin penetration of the Cercariae in
leptodactylids. These data suggest that adult L. tadpoles and adult frogs (e.g., G. repandum) or by
bufonius that inhabits forests and lands with sandy Metacercariae ingested with aquatic vegetation
soil makes such infections possible through the (e.g., Cat. inopinatus) and aquatic insects (e.g., H.
ingestion of or skin penetration by infective larval longiplexus) by a definitive host (Smyth and Smyth
stages (Anderson 2000). 1980). The uncommon occurrence of the latter
Adults of L. bufonius breed in burrows and species shows that the intermediate host (e.g.,
enter the water for short periods as tadpoles, dragonfly larvae and adults) is not a main prey
acting as intermediate and definitive hosts for item in the diet of this host.
various trematodes species (Table 2). Infection As predicted by Aho (1990), the adult
by larval trematodes showed low values as a infracommunities of L. bufonius showed low
consequence of the short period that L. bufonius species richness. An individual frog generally
is in the water, i.e., implying a lower probability of harbored only 3 helminth species, with scarce
penetration by the Cercariae. It can be assumed evidence of species affinities. On the 1 hand,
that this amphibian plays an insignificant role in we noted associations for those larval and adult

Table 6. Helminth species richness at the component community level for Leptodactylus species from South
America

Adult helminth Larval helminth

Host n Total richness Locality Reference
N T C n t c a

L. bufonius 76 16 5 3 1 1 5 ˗ 1 Corrientes, Argentina Present paper

L. latinasus 36 17 6 3 ˗ ˗ 6 1 1 Corrientes, Argentina Hamann et al. (2006a)
L. chaquensis 40 18 3 6 ˗ 1 7 ˗ 1 Corrientes, Argentina Hamann et al. (2006b)
L. chaquensis 132 19 4 5 1 1 6 1 1 Corrientes, Argentina Hamann et al. (2006b)
L. ocellatus 78 10 7 3 ˗ ˗ ˗ ˗ ˗ Rio de Janeiro, Brazil Vicente and dos Santos (1976)
L. podicipinus 43 8 5 3 ˗ ˗ ˗ ˗ ˗ Mato Grosso, Brazil Campião et al. (2009)
L. mystaceus 1 1 1 ˗ ˗ ˗ ˗ ˗ ˗ Pará, Brazil Goldbeg et al. (2007)
L. rhodomystax 5 4 2 1 ˗ 1 ˗ ˗ ˗ Pará, Brazil Goldbeg et al. (2007)
L. fuscus 12 3 3 ˗ ˗ ˗ ˗ ˗ ˗ Pará, Brazil Goldbeg et al. (2007)
L. martinezi 3 1 ˗ 1 ˗ ˗ ˗ ˗ ˗ Pará, Brazil Goldbeg et al. (2007)
L. ocellatus 31 7 3 1 ˗ 2 ˗ ˗ 1 Tocantins, Brazil Goldbeg et al. (2009)
L. fuscus 15 3 3 ˗ ˗ ˗ ˗ ˗ ˗ Tocantins, Brazil Goldbeg et al. (2009)
L. petersii 31 2 1 ˗ ˗ 1 ˗ ˗ ˗ Tocantins, Brazil Goldbeg et al. (2009)
L. pustulatus 19 4 3 ˗ ˗ 1 ˗ ˗ ˗ Tocantins, Brazil Goldbeg et al. (2009)
L. mystaceus 2 1 1 ˗ ˗ ˗ ˗ ˗ ˗ Tocantins, Brazil Goldbeg et al. (2009)
L. leptodactyloides 9 3 1 ˗ ˗ 1 ˗ ˗ 1 Tocantins, Brazil Goldbeg et al. (2009)
L. lineatus 2 1 1 ˗ ˗ ˗ ˗ ˗ ˗ Pastaza, Ecuador McAllister et al. (2010)
L. bolivianus 14 6 4 ˗ ˗ 2 ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)
L. leptodactyloides 14 4 3 ˗ ˗ 1 ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)
L. mistaceus 12 5 4 ˗ ˗ 1 ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)
L. pentadactylus 6 6 4 ˗ ˗ 2 ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)
L. petersii 24 1 1 ˗ ˗ ˗ ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)
L. rhodonotus 22 3 2 ˗ ˗ 1 ˗ ˗ ˗ Amazonia, Peru Bursey et al. (2001)

Adult/ larval helminths: nematodes (N/n), trematodes (T/t), cestodes (C/c), and acanthocephalans (a).
 Hamann et al. – Ecology of Parasites of Amphibians 1461

species which were located in different organs of are determining factors of lower infections by
the frog (e.g., Centrorhynchus sp. + A. hylambatis); helminths with complex life cycles. At the same
on the other hand, we found a negative correlation time, the correspondence between low vagility
between 2 species at the same infection site, and terrestrial habitat preferences of L. bufonius
with the same guild (e.g., Cos. podicipinus vs. A. significantly contributed to the high occurrence
hylambatis). Similarly to other local amphibians of nematode infections, while its fauna showed
(Hamann et al. 2006a b 2010), there was no low Metacercariae infections that result from
discernible pattern or structure to L. bufonius’s acquisition of species by penetration of infective
infracommunities, although their proximity to larvae into the host through natural orifices or the
the isolationist extreme of the continuum was skin (Hamann and González 2009).
demonstrated. This may also indicate that there
are numerous vacant niches in the digestive tract Acknowledgments: This project was partially
of this frog species. supported by Consejo Nacional de Investigaciones
Regarding the host size, other researchers Científicas y Técnicas (CONICET) from Argentina,
stated that frogs with larger bodies harbor more through a grant (PIP 2945) to M.I. Hamann.
helminth species than do small bodied frogs
(Muzzall 1991, McAlpine 1997, Hamann et al.
2006a b 2010, Yoder and Coggins 2007). In the REFERENCES
present study, the size of amphibian individuals
was a determining factor for the parasite species Addinsoft. 2004. Xlstat for Excel. London: Addinsoft.
richness, which suggests that larger frogs ingest Aho JM. 1990. Helminth communities of amphibians and
reptiles: comparative approaches to understanding
a more diverse diet and greater amounts of food, patterns and processes. In GW Esch, AO Bush, JM Aho,
and also provide more surface area for parasite eds. Parasite communities: patterns and processes.
colonization, i.e., a greater probability of skin London: Chapman and Hall, pp. 157-195.
penetration by larval stages; a larger size is also Anderson RC. 2000. Nematode parasites of vertebrates: their
related to a longer life and more time to become development and transmission. Wallingford, Oxford, UK:
CABI International.
infected, which favor higher values of parasitism Anderson R, D Gordon. 1982. Processes influencing the
and species richness. distribution of parasite numbers within host population with
Additionally, the infrapopulations of some special emphasis on parasite-induced host-mortalities.
species increase in abundance in larger hosts; Parasitology 85: 373-398.
e.g., the adult A. hylambatis can occur through Anderson RC, AG Chabaud, S Willmont. 1974. CHI. Keys to
the nematodes parasites of vertebrates. Faruham Royal,
predation of a greater number of larval stages (L3) Bucks, UK: Commonwealth Agricultural Bureaux.
accompanied by an increase in the intestinal area Bolek MG, JR Coggins. 2001. Seasonal occurrence and
in hosts with a larger body size; nevertheless, community structure of helminth parasites in green frogs,
the Cos. podicipinus abundance decreased in Rana clamitans melanota, from southeastern Wisconsin,
larger hosts. This suggests that skin penetration U.S.A. Comp. Parasitol. 68: 164-172.
Bolek MG, JR Coggins. 2003. Helminth community structure
of larvae in adult frogs is presumably limited by of sympatric eastern American toad, Bufo americanus
its tegument (i.e., a thicker integument compared americanus, northern leopard frog, Rana pipiens, and
to juvenile frogs); and by the immune response blue-spotted salamander, Ambystoma laterale, from
of the host. Similarly, Hamann et al. (2006a) southeastern Wisconsin. J. Parasitol. 89: 673-680.
also found a negative correlation between this Bursey CR, SR Goldberg, JR Parmelee. 2001. Gastrointestinal
helminths of 51 species of anurans from Reserva Cuzco
nematode species and the size of the frog L. Amazónico, Peru. Comp. Parasitol. 68: 21-35.
latinasus (Leptodactylidae) from the same area Bush AO, KD Lafferty, JM Lotz, AW Shostak. 1997.
of Corrientes Province. On the other hand, Parasitology meets ecology on its own terms: Margolis et
larger males were also more heavily parasitized al. revisited. J. Parasitol. 83: 575-583.
(e.g., species richness), suggesting that reduced Campião KM, RJ da Silva, VL Ferreira. 2009. Helminth
parasites of Leptodactylus podicipinus (Anura:
immune function and the differential behavior of Leptodactylidae) from south-eastern Pantanal, State of
males may also explain the increased levels of Mato Grosso do Sul, Brazil. J. Helminthol. 83: 345-349.
parasites (Folstad and Karter 1992, Poulin 1996). Carnevali R. 1994. Fitogeografía de la provincia de Corrientes.
In conclusion, L. bufonius showed a Asunción, Paraguay: Litocolor.
wide variation in its helminth fauna, including Crump ML, NJ Scott Jr. 1994. Visual encounters surveys. In
WR Heyer, MA Donnelly, RW Mc-Diarmid, LC Hayek, MS
helminths characteristic of aquatic and terrestrial Foster, eds. Measuring and monitoring biological diversity
habitats. This community suggests that the - standard methods for amphibians. Washington DC:
feeding habits and particularly the diet of this frog Smithsonian Institution Press, pp. 84-91.
1462 Zoological Studies 51(8): 1454-1463 (2012)

Duré MI, AI Kehr. 2004. Influence of microhabitat on the contrasting environments from northeastern Argentina. J.
trophic ecology of two leptodactylids from northeastern Parasitol. 92: 1171-1179.
Argentina. Herpetologica 60: 295-603. Hamann MI, AI Kehr, CE González. 2010. Helminth community
Esch GW, A Barger, KJ Fellis. 2002. The transmission of structure of Scinax nasicus (Anura: Hylidae) from a South
digenetic trematodes: style, elegance, complexity. Integr. American subtropical area. Dis. Aquat. Organ. 93: 71-82.
Compar. Biol. 42: 304-312. Holmes JC, PW Price. 1986. Communities of parasites. In
Esch GW, CR Kennedy, AO Bush, JM Aho. 1988. Patterns in DJ Anderson, J Kikkawa, eds. Community ecology:
helminth communities in freshwater fish in Great Britain: pattern and process. Oxford, UK: Blackwell Scientific
alternative strategies for colonization. Parasitology 96: Publications, pp. 187-213.
519-532. Jones A, RA Bray, DI Gibson. 2005. Keys to the Trematoda.
Folstad I, AJ Karter. 1992. Parasites, bright males, and the London: CABI Publishing and Natural History Museum.
immunocompetence handicap. Am. Mid. Nat. 139: 603- Joy JE, JL Pennington. 1998. Ecology of Megalodiscus
622. temperatus (Digenea: Paramphistomatidae) in red-spotted
Fotedar DN, R Tikoo. 1968. Studies on the life cycle of newts, Notophthalmus v. viridescens, from West Virginia.
Cosmocerca kashmirensis Fotedar, 1959, a common J. Helminthol. Soc. Wash. 65: 205-211.
oxyurid nematode parasite of Bufo viridis in Kashmir. Kehr AI, BFJ Manly, MI Hamann. 2000. Coexistence of
Indian Sci. Congr. Assoc. Proc. 55: 460. helminth species in Lysapsus limellus (Anura: Pseudidae)
Frost DR. 2011. Amphibian species of the world: an online from an Argentinean subtropical area: influence of biotic
reference. Vers. 5.5. New York: American Museum of and abiotic factors. Oecologia 125: 549-558.
Natural History electronic database. Available at http:// Kennedy CR, AO Bush, JM Aho. 1986. Patterns in helminth
research.amnh.org/vz/herpetology/amphibia Accessed 31 communities: Why are birds and fish different? Parasi-
Aug. 2012. tology 93: 205-215.
Gibson DI, A Jones, RA Bray. 2002. Keys to the Trematoda. King KC, AD Gendron, JD Mclaughlin, I Giroux, P Brousseau, D
London: CABI Publishing and Natural History Museum. Cyr et al. 2008. Short-term seasonal changes in parasite
Gillilland MG, PM Muzzall. 1999. Helminths infecting froglets community structure in northern leopard froglets (Rana
of the northern leopard frog (Rana pipiens) from Foggy pipiens) inhabiting agricultural wetlands. J. Parasitol. 94:
Bottom Marsh Michigan. J. Helminthol. Soc. Wash. 66: 13-22.
72-77. Luque JZ, AA Martins, LER Tavares. 2005. Community
Goater TM, GW Esch, AO Bush. 1987. Helminth parasite structure of metazoan parasites of the yellow Cururu toad
of sympatric salamanders: ecological concepts at infra- Bufo ictericus (Anura, Bufonidae) from Rio de Janeiro,
community, component and compound community levels. Brasil. Acta Parasitol. 50: 215-220.
Am. Midl. Nat. 118: 289-300. Magurran AE. 2004. Measuring biological diversity. Oxford,
Goldberg SR, CR Bursey, JP Caldwell, DB Shepard. 2009. UK: Blackwell Publishing.
Gastrointestinal helminths of six sympatric species of Marcogliese DJ, KC King, HM Salo, M Fournier, P Brousseau,
Leptodactylus from Tocantins State, Brazil. Comp. P Spear et al. 2009. Combined effects of agricultural
Parasitol. 76: 258-266. activity and parasites on biomarkers in the bullfrog, Rana
Goldberg SR, CR Bursey, JP Caldwell, LJ Vitt, GC Costa. catesbeiana. Aquat. Toxicol. 9: 126-134.
2007. Gastrointestinal helminth from six species of frog McAllister CT, CR Bursey, PS Freed. 2010. Helminth parasites
and three species of lizard simpatrics in Pará State, of selected amphibians and reptiles from the Republic of
Brazil. Comp. Parasitol. 74: 327-342. Ecuador. Comp. Parasitol. 77: 52-66.
González CE, MI Hamann. 2006. Helmintos parásitos McAlpine DF. 1997. Helminth communities in bullfrogs (Rana
de Leptodactylus bufonius Boulenger, 1894 (Anura: catesbeiana), green frogs (Rana clamitans), and leopard
Leptodactylidae) de Corrientes, Argentina. Rev. Esp. frogs (Rana pipiens) from New Brunswick, Canada. Can.
Herpetol. 20: 39-46. J. Zool. 75: 1883-1890.
Grabda-Kazubska B. 1963. The life cycle of Metalepthophallus McKenzie VJ. 2007. Human land use and patterns of
gracillimus (Lühe, 1909) and some observations on parasitism in tropical amphibian hosts. Biol. Conserv.
the biology and morphology of developmental stages 137: 102-116.
of Letophalus nigrovenosus (Bellingham, 1844). Acta Muzzall PM. 1991. Helminth infracommunties of the frogs
Parasitol. Pol. 11: 349-370. Rana catesbeiana and Rana clamitans from Turkey
Hamann MI. 2011. Current state of knowledge of helminth Marsh, Michigan. J. Parasitol. 77: 366-371.
parasites of amphibians in Argentina: a taxonomic Ostrowski de Núñez M. 1979a. Ungewohnliche
and ecological approach. In Anais do XXII Congresso Xiphidiocercarie aus Ampullaria canaliculata nebst
Brasileiro de Parasitologia, São Paulo. Rev. Patol. Trop. Bemerkungen ubre Travtrema stenocotyle. Angew.
40 (Supplement 2): 1-3. Parasitol. 20: 46-52.
Hamann MI, CE González. 2009. Larval digenetic trematodes Ostrowski de Núñez M. 1979b. Fauna de agua dulce de la
of tadpoles of six amphibian species from northeastern república Argentina. IX. Sobre representantes de la
Argentina. J. Parasitol. 95: 623-628. fauna Paramphistomatidae (Trematoda). Physis 38: 55-
Hamann MI, CE González, AI Kehr. 2006a. Helminth 62.
community of Leptodactylus latinasus (Anura: Philibosian R, R Ruibal, VH Shoemaker, LL McClanahan.
Leptodactylidae) from Corrientes, Argentina. Acta 1974. Nesting behavior and early larval life of the frog
Parasitol. 51: 294-299. Leptodactylus bufonius. Herpetologica 30: 381-386.
Hamann MI, AI Kehr, CE González. 2006b. Species Pielou EC. 1966. The measurement of diversity in different
affinity and infracommunity ordination of helminths of types of biological collections. J. Theor. Biol. 13: 131-144.
Leptodactylus chaquensis (Anura: Leptodactylidae) in two Poulin R. 1996. Sexual inequalities in helminth infections: a
 Hamann et al. – Ecology of Parasites of Amphibians 1463

cost of being a male? Am. Nat. 147: 287-295. parasitic helminths of wood ducks, Aix sponsa, in the
Prudhoe S, RA Bray. 1982. Platyhelminth parasites of the Atlantic Flyway. Proc. Helminthol. Soc. Wash. 52: 297-
amphibian. London: British Museum (Natural History), 310.
Oxford Univ. Vicente JJ, E dos Santos. 1976. Fauna helmintológica de
Santos VGT, SB Amato. 2010. Helminth fauna of Rhinella Leptodactylus ocellatus (L., 1758) de Volta Redonda,
fernandezae (Anura: Bufonidae) from the Rio Grande do Estado do Rio de Janeiro. Atas Soc. Biol. Rio de Janeiro
Sul coastland, Brazil: analysis of the parasite community. 18: 27-42.
J. Parasitol. 96: 823-826. Yamaguti S. 1961. Systema helminthum. The nematodes of
Schmidt GD. 1985. Development and life cycles. In vertebrates. New York: Interscience.
DWT Crompton, BB Nickol, eds. Biology of the Yamaguti S. 1963. Systema helminthum. The Acantocephala
Acanthocephala. Cambridge, UK: Cambridge Univ., pp. of vertebrates. New York: Interscience.
273-305. Yamaguti S. 1971. Synopsis of the digenetic trematodes of
Shannon CE, W Weaver. 1949. The mathematical theory of vertebrates. Tokyo: Keigaku Publishing.
communication. Urbana, IL: Univ. of Illinois, Press. Yamaguti S. 1975. A synoptical review of life histories of
Smyth JD, MM Smyth. 1980. Frogs as host-parasite systems. digenetic trematodes of vertebrates. Tokyo: Keigaku
I. An introduction to parasitology through the parasites of Publishing.
Rana temporaria, R. esculenta and R. pipiens. London: Yoder HR, JR Coggins. 2007. Helminth communities in five
Macmillan. species of sympatric amphibians from three adjacent
Tucker RB, JE Joy. 1996. Relationships between Glypthelmins ephemeral ponds in southeastern Wisconsin. J. Parasitol.
pennsylvaniensis (Trematoda: Digenea) infections and 93: 755-760.
host size. J. Helminthol. Soc. Wash. 63: 42-46. Zar JH. 2010. Biostatistical analysis. Englewood Cliffs, NJ:
Thul JE, DJ Forrester, CL Abercrombie. 1985. Ecology of Prentice-Hall.