The Biologist (Lima), 2017, 15(2), jul-dec: 459-468
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTH PARASITES OF RHINELLA MARINA (LINNAEUS, 1758) (ANURA: BUFONIDAE)
FROM TARAPOTO, PERU
HELMINTOS PARÁSITOS DE RHINELLA MARINA (LINNAEUS, 1758) (ANURA: BUFONIDAE) DE
TARAPOTO, PERÚ
1UNESP - Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia, Botucatu,
São Paulo, Brazil.
2UFPI - Universidade Federal do Piauí, Piauí, Brazil.
3URP - Universidad Ricardo Palma, Facultad de Ciencias Biológicas, Lima, Perú.
4UNFV – Universidad Nacional Federico Villarreal, Facultad de Ciencias Naturales y Matemática, Lima, Perú.
5Wabash College, Lima, Perú.
6UAP - Universidad Alas Peruanas, Tarapoto, Perú.
Correspondence author: gisatoledo@hotmail.com
ISSN Versión Impresa 1816-0719
ISSN Versión en linea 1994-9073 ISSN Versión CD ROM 1994-9081
459
ABSTRACT
Rhinella marina is a large bufonid with nocturnal and terrestrial habit, which inhabits humid areas with
adequate cover, with a preference for open or disturbed habitat such as tracks, roads, low grassland, and
areas that are near human settlement. Aiming to expand the knowledge on the amphibian parasites in
Neotropical region, the helminth fauna associated with R. marina from two different environments at the
municipality of Tarapoto, Peru was reported. A total of 30 R. marina specimens was surveyed for helminth
parasites: 10 specimens from the Urku – Amazonian Studies and Cordillera Escalera Reserve (preserved
area) and 20 from the Santa Rosa (anthropogenic area), both in the municipality of Tarapoto, Peru. The
helminth component community included eight species (seven nematodes and one cestode). A total of
1,799 helminths was recovered, with a mean intensity of infection (MII) in animals from the preserved
area (MII = 57.9 ± 23.8) not differing from those of the anthropogenic area (MII = 61.0 ± 11.5). The
nematode Oswaldocruzia urubambaensis Guerrero, 2013 was the dominant species (d = 0.26) for the
preserved area and Cylindrotaenia americana Jewell, 1916 was the dominant species (d = 0.46) for the
anthropogenic area. The richness of parasites between two areas was similar and the diversity of helminth
was also not different. The helminth component communities showed no differences in relation the
richness and composition. However, the helminth community structure shows a slight difference in the
infracommunities, suggesting that environmental characteristics can influence the structuration of
helminth community parasites of this anuran species, since some species of parasites presented
differences in prevalence, abundance, and relative importance values between the two infracommunities.
Keywords: amphibians – anura – infracommunity – Nematoda – Peruvian Amazon
The Biologist (Lima)
1 2 3,4
Gislayne Melo Toledo ; Mariluce Gonçalves Fonseca ; Jose Iannacone ;
5 6 1
Jorge Manuel Cárdenas Callirgos ; Carlos Urbano Mendoza Vidaurre & Reinaldo José da Silva
The Biologist
(Lima)
460
RESUMEN
Rhinella marina es un bufónido grande con hábito nocturno y terrestre, que habita áreas húmedas con
cobertura adecuada, con preferencia por hábitat abierto o perturbado como vías, caminos, pastizales bajos
y áreas cercanas al asentamiento humano. Con el objetivo de ampliar el conocimiento sobre los anfibios
parásitos en la región Neotropical, se registró la fauna de helmintos asociada a R. marina de dos ambientes
diferentes en la municipalidad de Tarapoto, Perú fue reportado. Un total de 30 ejemplares de R. marina
fueron estudiados para detectar helmintos parásitos: 10 especímenes de Urku - Estudios Amazónicos y de
la Reserva Cordillera Escalera (área preservada) y 20 de Santa Rosa (área antropogénica), ambos en la
municipalidad de Tarapoto, Perú. El componente de la comunidad de helmintos incluyó ocho especies
(siete nematodos y un céstode). Se recuperó un total de 1.799 helmintos, con una intensidad media de
infección (IMI) en animales del área preservada (IMI = 57,9 ± 23,8) que no difiere de los del área
antropogénica (IMI = 61,0 ± 11,5). El nematodo Oswaldocruzia urubambaensis Guerrero, 2013 fue la
especie dominante (d = 0,26) para el área preservada y Cylindrotaenia americana Jewell, 1916 fue la
especie dominante (d = 0,46) para el área antropogénica. La riqueza de parásitos entre las dos áreas fue
similar y la diversidad de helmintos tampoco fue diferente. El componente de la comunidad de helmintos
no mostró diferencias en relación con la riqueza y composición. Sin embargo, la estructura de la
comunidad de helmintos muestra una leve diferencia en las infracomunidades, lo que sugiere que las
características ambientales pueden influir en la estructuración de helmintos parásitos comunitarios de esta
especie de anuro, ya que algunas especies de parásitos presentan diferentes prevalencias, abundancias, y
valor de importancia relativa entre las dos infracomunidades.
Palabras clave: Amazonía peruana – anfibios – anura – infracomunidad – Nematoda
INTRODUCTION
The family Bufonidae Gray, 1825 currently
includes 592 species distributed in 52 genera and
has a wide geographic distribution, occurring on all
continents except Antarctica, Madagascar, and
oceanic regions (Lima et al., 2006; Frost, 2017).
The genus Rhinella Fitzinger, 1826 is represented
by 93 species, of which 29 occur in Peru (Frost,
2017), including terrestrial anurans, with
oviposition in gelatinous cords, inside or the margin
of water bodies (Lima et al., 2006).
Rhinella marina (Linnaeus, 1758), commonly
known as cane toad, is a large buffoon, occurring
naturally from southern Texas, USA, through
tropical Mexico and Central America to the north of
South America (Solís et al., 2009). This nocturnal
and terrestrial toad that inhabits humid areas with
adequate cover, with a preference for open or
disturbed habitat such as trails, roads, low pastures
and areas that are close to human settlements (Solís
et al., 2009). Their feeding is composed mainly of
arthropods (especially ants and termites) and small
vertebrates; and has great flexibility regarding the
breeding site (Solís et al., 2009).
In Peru, the first study of helminths in the genus
Rhinella was done by Tantaleán & García (1989).
However, in recent years, studies on anuran
parasites infecting species of this genus have
increased in the region of South America (Table 1).
Tantaleán & García (1989) and Bursey et al. (2001)
have reported in previous studies the composition
of the parasitic fauna of R. marina in Peru.
However, we analyzed in this study the
implications of two contrasting areas on the
helminth fauna of these anurans. The first is an area
of Amazon Forest, that is highly preserved
representing a more stable environment, and the
second is an urban area known as Santa Rosa, with
greater human influence representing a more
unstable environment.
The aims of this study were: (1) to determine the
structure of the parasite helminth community; 2) to
determine the richness and diversity of parasite
communities; and (3) to analyze the relationship
between the composition of the helminth
communities and the characteristics of the
environment.
Toledo et al.
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
461
Table 1. Richness of helminth species at the level of community component of Rhinella species of South America.
Amphibians Sample
number
Total
Richness
Locality Reference
Rhinella marina
30
8
Peru
Present study
Rhinella spinulosa
(Wiegmann, 1834)
-
4
Peru
Tantaleán & García (1989)
Rhinella arequipensis
(Vellard, 1959)
- 3 Peru Tantaleán &
García (1989)
Rhinella limensis
(Werner, 1901)
- 5 Peru Tantaleán &
García (1989)
Rhinella marina
- 3 Peru Tantaleán &
García (1989)
Rhinella marina
5 5 Peru Bursey et al.
(2001)
Rhinella poeppigii
(Tschudi 1845)
32 5 Peru Chero et al.
(2015a)
Rhinella limensis
30 4 Peru Chero et al.
(2015b)
Rhinella spinulosa
90 7 Peru Chero et al.
(2016)
Rhinella icterica
(Spix, 1824)
32 15 Brazil Luque et al.
(2005)
Rhinella icterica
58 12 Brazil Lux Hoppe et al.
(2008)
Rhinella schneideri
(Werner, 1894)
42 6 Brazil Lux Hoppe et al.
(2008)
Rhinella icterica
15 5 Brazil Pinhão et al.
(2009)
Rhinella fernandezae
(Gallardo, 1957)
90 13 Brazil Santos &
Amato (2010)
Rhinella icterica
60
12
Brazil
Santos et al.
(2013)
Rhinella major
(Müller and Hellmich, 1936)
19
4
Argentina
González &
Hamann (2006)
Rhinella fernandezae
25
4
Argentina
González &
Hamann (2007)
Rhinella bergi
(Céspedez, 2000)
20
4
Argentina
González &
Hamann (2007)
Rhinella schneideri
11
8
Argentina
González &
Hamann (2008)
Rhinella fernandezae 65 22 Argentina Hamann et al. (2013)
Rhinella major 85 15 Argentina Hamann & González (2015)
MATERIALS AND METHODS
Study area
Anurans were collected in the municipality of
Tarapoto, Peru (Figure 1). The city is located near
the line of Ecuador, with a mean altitude of 250 m
(Google Earth) and is characterized by a tropical
rainy climate, with temperatures ranging from 18
°C to 33 °C.
In the municipality of Tarapoto, the animals were
collected in two different landscapes. The first was
represented by the preserved area of the Amazon
Forest located at URKU – Amazonian Studies (6 °
27'52.42 "S, 76 ° 21'7.73" W) and Cordillera
Escalera Reserve (6 ° 27'41.30 "S, 76 ° 18'42.56 "
O). In these localities, the specimens were
collected in trials of closed forest area, where there
is no human presence (Figure 1A). The second
landscape was represented by an anthropogenic
area, a district known as Santa Rosa (6 ° 25'39.84
"S, 76 ° 18'32.28" W), that is near of a highway,
where there are several human residences, with
many domestic animals (dogs, cats, horses, cattle,
pig, among others) and great amount of garbage,
characterizing a high degree of environmental
degradation (Figure 1B).
Collection and examination of amphibians
Thirty specimens of R. marina were collected in
March 2014 in the municipality of Tarapoto, Peru.
Amphibians were sampled by active search at
night. Toads were transported live to the laboratory
and then euthanized with sodium thiopental
solution, in accordance with Resolution No. 301
and Ordinance No 148/2012 of the Conselho
Federal de Biologia – CFBio. The snout–vent
length (SVL) and body mass were recorded. Then
they were necropsied, sexed and organs of the
gastrointestinal tract, lungs, heart, kidneys, liver,
urinary bladder, gall bladder, and body cavity were
surveyed for the presence of helminths. The
collection was authorized by Director's Resolution
Parasites of Rhinella marina from Peru
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
462
Figure 1. Geographical location of anuran sampling landscapes in the municipality of Tarapoto, Peru. A) Visualization of host
sampling landscapes; B) Area of trail in the reserve URKU – Amazonian Studies (preserved environment); C) Forest of the
Reserve Cordillera Escalera (preserved environment); D-E) Pond in Santa Rosa (anthropized environment). A, C and E, source
Google Earth.
Toledo et al.
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
463
locations. The Berger-Parker index of dominance
(d) was used to determine the most dominant
species (Magurran, 2004).
The helminth community structure was examined
according to the methodology outlined by Thul et
al. (1985), where helminth species are classified
into 4 groups (dominant, codominant, subordinate,
and unsuccessful colonizer) by taking into account
the prevalence, intensity, and maturation factor,
which is related to the degree of host specificity.
The importance value (I) was calculated for each
helminth species as follows:
where Aj is number of individual parasites in
species j, Bj is number of hosts infected with
parasite j, and Mj is a maturity factor equal to 1.0 if
at least 1 mature specimen of species j was found
and equal to 0 otherwise.
The analyses were performed in the BioEstat 5.0
program (Ayres et al., 2007).
The 30 amphibians analyzed were infected with at
least one helminth species (overall prevalence =
100%). Results of the parasitological descriptors of
the two localities are presented in Table 2. Eight
helminth species, totaling 1,799 individuals, were
found in R. marina in the two localities (Table 3).
Nematoda was the predominant parasite group in
this sample (seven species), while Cestoda was
represented by only one species. About the species
found, five have a direct life cycle (Aplectana
hylambatis (Baylis, 1927), Aplectana vellardi
Travassos, 1926, Oswaldocruzia urubambaensis
Guerrero, 2013, Rhabdias pseudosphaerocephala
Kuzmin, 2007, and Cylindrotaenia americana
Jewel, 1916) and three have an indirect life cycle
(Falcaustra concordaqui Ibañez & Córdova, 1976,
Ochoterenella vellardi (Travassos, 1929)
Esslinger, 1986, and larvae Physaloptera
Rudolphi, 1819).
The helminth component communities of the
animals from preserved and anthropic areas shared
the same helminth species (Table 3), differentiating
N°024-2014-SERFOR-DGGSPFFS.
Collection, preparation, and identification of
helminths
The helminths were collected and processed
following the methodologies used by Amato et al.
(1991) and preserved in 70% ethyl alcohol until the
preparation of the temporary slides for species
identification. Cestodes were stained with
hydrochloric carmine and cleared with creosote.
Nematodes were cleared in lactophenol and
examined as temporary mounts. Morphometric
data and photomicrographs of helminths were
obtained using a computerized LAS V3 image
analysis system (Leica Application Suite, Leica
Microsystems, Wetzlar, Germany) coupled to a
DM 5000B microscope with differential
interference contrast (Leica Microsystems,
Wetzlar, Germany).
The voucher species will be deposited at the
Coleção Helmintológica do Instituto de
Biociências de Botucatu (CHIBB), Department of
Parasitology, at the Universidade Estadual Paulista
(UNESP), São Paulo State, Brazil and at the
Colección Helmintológica y de Invertebrados
Relacionados del Museo de Historia Natural (MUS
- UNMSM) at the Universidad Nacional Mayor de
San Marcos, Lima, Peru.
Statistical analysis
Quantitative descriptors of parasitism as
prevalence, mean abundance, mean intensity,
parasite richness, and amplitude were calculated as
infection patterns for all infrapopulations of
parasites found, according to Bush et al. (1997).
The richness is described as the total number of
helminth species. The mean helminth species
richness is the sum of parasite species per
individual host, divided by the total sample size.
Measurements of community richness and
diversity included the species richness, Shannon
index (H´), and evenness (J') as H´/H´maximum
(Zar, 2010). The Brillouin index (BH) and evenness
(E) w e r e u sed to compa r e h elminth
infracommunities (Pielou, 1966). The diversity
indices were used with decimal logarithms (log10).
The Student t-test was used to compare differences
in intensity and mean diversity of infection
between the two environments. The Mann-
Whitney U test was used to test differences in
helminth species abundances between the two
Ij = (Mj) AjBj 100
ΣAiBi
RESULTS
Parasites of Rhinella marina from Peru
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
464
was 2.9 ± 0.4 (maximum = 5) species per infected
host. Multiple infections were common with 1, 2, 3,
4, and 5 species occurring in 1, 4, 2, 1, and 2 hosts,
respectively (Figure 2).
in the abundances of each species. In the preserved
habitat the diversity of helminths was 0.77 and the
equitability was 0.86. The nematode O.
urubambensis was the dominant species (d = 0.26).
At the infracomunity level, mean helminth richness
Table 2. Parameters of infection of the helminth community associated with Rhinella marina from the municipality
of Tarapoto, Peru. Preserved Areas - Urku and Reserve Cordillera Escalera; Anthropogenic Areas - Santa Rosa.
Parameters
Area
Preserved
Anthropogenic
Number of hosts 10
20
Prevalence 100%
100%
Mean intensity of infection
57.9 ± 23.8
61.0 ± 11.5
Range 3 – 240
4 -
245
Number of helminths
579 1220
Richness of species
8 8
Mean richness of species
2.9 ± 0.4
3.2 ± 0.3
Maximum number of species/host 5 5
Diversity (H´) / Evenness (J) 0.77/0.86 0.64/0.71
5) species per infected host. Multiple infections
were common with 1, 2, 3, 4, and 5 species
occurring in 1, 6, 4, 7, and 2 hosts, respectively
(Figure 2).
In the anthropogenic habitat, the diversity of
helminths was 0.64 and the equitability was 0.71.
The cestode C. americana was the dominant
species (d = 0.46). At the infracommunity level,
mean helminth richness was 3.2 ± 0.3 (maximum =
Figure 2. Number of Rhinella marina infected with 1, 2, 3, 4 and 5 helminth species in Tarapoto, Peru.
Toledo et al.
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
The helminth species were classified according to
importance value (Table 4). In the anthropogenic
area, C. americana was the species with the highest
value of importance, followed by O.
urubambaensis; in the preserved area the
nematodes O. urubambaensis, A. hylambatis, and
A. velardi were the most important species of the
community (highest values of importance).
The helminth diversity between the two localities
was similar (t = -1.25, GL = 28, p = 0.21). As well
as, there was no significant variance between the
two habitats in relation to the mean intensity of
infection (t = -0.13, GL = 28, p = 0.89). When
parasitic abundance between the localities was
compared, only C. americana was found in higher
abundance in relation to the preserved area (U = 37;
p < 0.05).
465
Parasites of Rhinella marina from Peru
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
Table 3. Helminths recorded in Rhinella marina from Tarapoto, Peru. Berger-Parked index (d), prevalence (P, in %), mean abundance and mean intensity infection
(MII), followed by the standard error (SE) and the site of infection (SI).
Helminths
d
%
MA
± SE
MII
± SE
Area
SI*
Preserved
Anthropogenic
d
P
MA
± SE
MII ± SE
d
P
MA ± SE MII ± SE
Cestoda
Cylindrotaenia americana
0.37
56.7
22.4 ± 6.2
39.6 ± 8.9
SI, LI
0.2
10
11.4 ± 11.4a
114
0.46
80
28.0 ± 7.2a34.9 ± 8.1
Nematoda
Aplectana hylambatis
0.12
33.3
7.4 ± 4.3
22.1 ± 11.9
SI, LI
0.22
30
12.7 ± 11.5
42.3 ± 36.8
0.08
35
4.7 ± 3.1 13.4 ± 8.3
Aplectana vellardi
0.07
26.7
4.3 ± 2.4
16.3 ± 7.7
S, SI, LI
0.16
30
9.5 ± 6.8
31.7 ± 18.4
0.03
25
1.8 ± 0.9 7.0 ± 2.5
Falcaustra concordaqui
0.07
23.3
4.3 ± 2.2
18.3 ± 7.4
SI, LI
0.06
40
3.4 ± 2.6
8.5 ± 6.0
0.08
15
4.7 ± 3.0 31.3 ± 12.9
Ochoterenella vellardi
0.03
23.3
1.9 ± 1.1
8.3 ± 3.8
BC
0.07
50
3.8 ± 2.8
7.6 ± 5.4
0.02
10
1.0 ± 0.7 10.0 ± 3.0
Oswaldocruzia urubambaensis
0.26
70
15.8 ± 3.5
22.5 ±
4.2
SI, LI
0.26
60
14.9 ± 5.5
24.8 ± 6.5
0.27
75
16.2 ± 4.6 21.6 ± 5.4
Physaloptera sp. 0 10 0.2 ± 0.1 1.7 ± 0.7 S 0.01 10 0.3 ± 0.3 3 0 10 0.1 ± 0.1 1
Rhabdias pseudosphaerocephala 0.06 63.3 3.7 ± 1.2 5.8 ± 1.8 L 0.03 60 1.9 ± 0.7 3.2 ± 0.8 0.08 65 4.6 ± 1.8 7.1 ± 2.5
a
*Site of infection: BC = body cavity corporal; S = stomach; SI = small intestine; LI = large intestine; L = lung. p < 0.05.
466
The helminth species recorded in this toad have low
host specificity since their presence has been reported
in species of amphibians belonging to several
families. Cylindrotaenia americana, A. hylambatis,
and Physaloptera sp. found parasitizing R. marina in
the present study had also been recorded in other
studies of helminth fauna with the same host
(Tantaleán & García, 1989; Bursey et al., 2001).
However, Cosmocerca brasiliense and Cosmocerca
parva recorded by Bursey et al. (2001) were not
found in this study.
In general, for R. marina there was no difference
between the localities in relation to the parasitological
descriptors. The populations of analyzed hosts
presented parasitic fauna with the same parasite
species. However, some species of parasites
presented differences in prevalence, abundance, and
relative importance values between the two
infracommunities. Of the dominant species recorded
for the preserved area, only O. vellardi was not
dominant in the anthropogenic area, but the
importance values of the other nematodes were
smaller, whereas for the cestode C. americana the
values was significantly larger. This is important
since O. vellardi has an indirect life cycle involving
hematophagous arthropods as a possible vector agent
(Wong & Bundy, 1985) and the instability of the
environment (eg, pollution) may have influenced the
permanence of this intermediate host, inducing the
lowest abundance and occurrence of this parasite.
In conclusion, the community of helminth parasites in
R. marina, in this region of Peru, has the following
characteristics: parasitic community composed
predominantly of adult nematodes with monoxenic
cycles; the helminth infracommunities did not show
The results of the present study indicate that R.
marina is a host with relative high helminth species
richness (Espinola- Novelo et al., 2017), which was
similar to previous studies with other Rhinella species
in South America (Table 1). The parasitic fauna of R.
marina included preferably nematode species. The
high richness of this parasite may be related to the
terrestrial habit of the host, since adult toads enter the
water for a short period, only for breeding (Lima et
al., 2006). Anurans with terrestrial habits generally
present low prevalence and mean intensity of
infection by digenetic trematode, which involves the
ingestion of aquatic arthropods and snails (Bolek &
Coggins 2000, 2003; Espinola- Novelo et al., 2017).
According to Aho (1990), the time that the hosts
remain in the terrestrial or aquatic environment
during the larval phase and the period of reproduction
is determinant for the parasitic richness. Tadpoles are
more exposed to helminths with aquatic life cycles;
on land, anurans are more exposed to nematodes with
monoxenic life cycles (eg, Oswaldocruzia spp.,
Rhabdias spp., and cosmocercids), because most
nematodes infect anurans by skin penetration or egg
ingestion (Barton, 1999; Bolek & Coggins, 2000,
2001, 2003; Muzzal et al., 2001; Yoder & Coggins,
2007).
Rhinella marina acted as the definitive host for more
than 80% of the helminth species found to parasite
this anuran. This anuran participated as an
intermediate host of Physaloptera sp., a nematode
that remains in the gastric mucosa for variable periods
of time without reaching the adult stage (Anderson,
2000).
Toledo et al.
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
DISCUSSION
Table 4. Values of importance (I) and classication of the species of helminths in Rhinella marina from Tarapoto,
Peru.
Helminth species
Area
Preserved
Anthropogenic
I
Classication
I
Classication
Cylindrotaenia americana
5.39
Dominant
55.33
Dominant
Aplectana hylambatis
18.02
Dominant
4.11
Dominant
Aplectana vellardi
13.34
Dominant
1.08
Dominant
Falcaustra concordaqui
6.43
Dominant
1.74
Dominant
Ochoterenella vellardi
8.99
Dominant
0.25
Codominant
Oswaldocruzia
urubambaensis
42.29
Dominant
30.06
Dominant
Physaloptera sp.
0.0
Unsuccessful colonizer
0.0
Unsuccessful colonizer
Rhabdias
pseudosphaerocephala 5.39 Dominant 7.4 Dominant
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Parasites of Rhinella marina from Peru
The Biologist (Lima). Vol. 15, Nº2, jul - dec 2017
differences in relation to helminth richness and
composition; and the relative importance of helminth
species differed in the two habitats.
The authors are grateful to colleagues from the
Laboratório de Parasitologia de Animais Silvestres
(LAPAS) - UNESP, for help with the fieldwork. G. M.
Toledo thanks the Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq)
for an doctoral scholarship (140301/2013-5). Silva is
grateful to Pro-Reitoria de Pós-graduação da UNESP
(PROPG-UNESP), CNPq (307808/2014-9) and
CNPq-PROTAX (440496/2015-2) / FAPESP
2016/50377-1.
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