33
Clinostomum marginatum
in
Poecilia reticulata
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Neotropical Helminthology
Neotropical Helminthology, 2025, vol. 19 (1), 33-49
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
ENDOPARASITES ASSOCIATED WITH ANURAN AMPHIBIANS
IN A CONSERVATION AREA IN THE SETE CIDADES NATIONAL PARK,
PIAUÍ STATE, BRAZIL
ENDOPARÁSITOS ASOCIADOS A ANFIBIOS ANUROS EN UN ÁREA
DE CONSERVACIÓN DEL PARQUE NACIONAL DE SETE CIDADES,
ESTADO DE PIAUÍ, BRASIL
Jacilene de Sousa Uchôa
1,4
, Cicero Ricardo de Oliveira
2,4,*
, Etielle Barroso de Andrade
3
& Diva Ma-
ria Borges-Nojosa
1,4
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20251911905
Universidad Nacional
Federico Villarreal
Volume 19, Number 1 (jan - jun) 2025
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Inventories are the basis of studies, essential for determining which and how many species are part of an ecosystem and
important for understanding the diversity and functioning of organisms. Studies on parasitic fauna are based on the
importance of these organisms as disease-causing agents that can inf uence the biosecurity of ecosystems and natural
environments. T us, research that investigates the relationship between helminths and anurans provides information
that helps in the conservation of these species and their habitats. T is study aims to describe the parasitic community
associated with anuran amphibians in the Sete Cidades National Park (PNSC), an important conservation area in the
north of the state of Piauí, Brazil. We analyzed 318 anuran amphibians, distributed among 21 species and four families.
Of these, 142 individuals were parasitized by at least one species of endoparasite, giving an overall prevalence of 44.65%.
A total of 8056 parasite specimens were counted and identif ed in 26 parasite taxa, with an average infection intensity
of 56.73 and abundance of 25.33. Among the most abundant species found were
Raillietnema spectans
Gomes, 1964
1
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Biologia, Campus do Pici, Universidade
Federal do Ceará, Fortaleza, Brasil, Av. Mister Hull, s/n, Fortaleza, CE, 60440-900, Brasil
2
Universidade Federal do Cariri, Instituto de Formação de Educadores, Laboratório de Biologia e Ecologia de Vertebrados,
63.260-000, Brejo Santo, CE, Brasil.
3
Grupo de Pesquisa em Biodiversidade e Biotecnologia do Centro-Norte Piauiense, Instituto Federal de Educação, Ciência e
Tecnologia do Piauí, Campus Pedro II, Rua Antonino Martins de Andrade, 750, Pedro II, PI, 64255-000, Brasil.
4
Núcleo Regional de Of ologia, Universidade Federal do Ceará, Fortaleza, CE, Brasil.
* Corresponding author: riccicer@gmail.com
Jacilene de Sousa Uchôa:
https://orcid.org/0000-0003-3426-1391
Cicero Ricardo de Oliveira:
https://orcid.org/0000-0002-3194-7067
Etielle Barroso de Andrade:
https://orcid.org/0000-0002-5030-1675
Diva Maria Borges-Nojosa:
https://orcid.org/0000-0002-8696-0170
34
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
(3034),
Schrankiana schranki
(Travassos, 1925) (2383), and
Aplectana hylambatis
(Baylis, 1927) (1540). In this study, we
expanded the parasite fauna of anurans in the PNSC, which previously consisted of 13 parasite taxa in just four anuran
species. Here, we recorded 21 additional parasite taxa, with new records of infection in 17 anuran host species. We also
added 19 new parasite taxa to the existing records for the state of Piauí, signifcantly expanding our knowledge of the
region.
Keywords:
Anurans – Helminthes – Inventory – Nematodes – Semi-arid
RESUMEN
Los inventarios son la base de los estudios, esenciales para determinar cuáles y cuántas especies forman parte de un
ecosistema e importantes para comprender la diversidad y el funcionamiento de los organismos. Los estudios sobre la
fauna parasitaria se basan en la importancia de estos organismos como agentes causantes de enfermedades que pueden
infuir en la bioseguridad de los ecosistemas y entornos naturales. Así, las investigaciones que indagan en la relación
entre helmintos y anuros proporcionan información que ayuda a la conservación de estas especies y sus hábitats. El
objetivo de este estudio es describir la comunidad parasitaria asociada a anfbios anuros en el Parque Nacional de Sete
Cidades (PNSC), una importante área de conservación en el norte del estado de Piauí. Analizamos 318 anfbios anuros,
distribuidos entre 21 especies y cuatro familias. De ellos, 142 individuos estaban parasitados por al menos una especie
de endoparásito, lo que supone una prevalencia global del 44,65%. Se contabilizaron un total de 8056 ejemplares
parasitados y identifcados en 26 taxones de parásitos, con una intensidad media de infección de 56,73 y una abundancia
de 25,33. Entre las especies más abundantes se encontraron
Raillietnema spectans
Gomes, 1964 (3034),
Schrankiana
schranki
(Travassos, 1925) (2383), y
Aplectana hylambatis
(Baylis, 1927) (1540). En este estudio, hemos ampliado la
fauna de parásitos de anuros en el PNSC, que anteriormente constaba de 13 taxones de parásitos en sólo cuatro especies
de anuros. Aquí, registramos 21 taxones de parásitos adicionales, con nuevos registros de infección en 17 especies de
anuros hospedadores. También añadimos 19 nuevos taxones de parásitos a los registros existentes para el estado de Piauí,
ampliando signifcativamente nuestro conocimiento de la región.
Palabras clave:
Anuros – Helmintos – Inventario – Nematodos – Semiárido
INTRODUCTION
Amphibians are the vertebrates most at risk of extinction,
with 40.7% of species threatened worldwide (Luedtke
et al
., 2023). Emerging infectious diseases and habitat
loss are currently the main causes of amphibian decline
(Luedtke
et al
., 2023; Ruggeri
et al
., 2023). Amphibians
are intermediate, paratenic, and/or defnitive hosts for
various species of parasitic helminths (Koprivnikar
et
al
., 2012; Campião
et al
., 2014; Amorim
et al
., 2019;
Herczeg
et al
., 2021; Mascarenhas
et al
., 2021). In this
way, parasites can also cause species decline, afecting
host immunity and population dynamics (Bittencourt &
Rocha, 2003; Hudson, 2005).
Te parasite fauna comprises a large part of the planet’s
biodiversity (Kuris, 2008), where parasitism is a complex
ecological interaction that can involve ecological processes
of multiple hosts (Bower
et al
., 2019) and can have a
long history of coevolution between hosts and their
parasites (Ebert & Fields, 2020). Among other things,
they represent an important modulator of biodiversity
at diferent trophic levels and are models for studying
parasite-host relationships (Cardoso
et al
., 2016).
Inventories, which are the basis of studies, are essential
for determining which and how many species are part
of an ecosystem and are important for understanding
the diversity and functioning of organisms (Segalla
et al
., 2021). Studies on parasitic fauna are based on
the importance of these organisms as disease-causing
agents that can infuence the biosecurity of ecosystems
and natural environments (Brooks & Hoberg, 2000).
Tus, research investigating the relationship between
helminths and anurans provides information that helps
in the conservation of these species and their habitats
(Coimbra
et al
., 2023). In addition to parasites having
this ecological importance, anurans are also important as
35
Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
environmental bioindicators (Chaukulkar
et al
., 2018;
Cramp & Franklin, 2018).
Helminths are the most common invertebrates parasitizing
amphibians (Santos & Amato, 2013). Among these, the
most abundant are nematodes (Campião
et al
., 2014;
Oliveira
et al
., 2022) due to the biological aspects of the
host and environmental conditions (Sena
et al
., 2018;
Oliveira
et al
., 2022), where changes in natural ecosystems
can cause variations in the transmission patterns of these
parasites, facilitating their occurrence and dispersal (Poulin,
2007). Tese parasitic aspects are also closely related to
the phylogeny and life history of the hosts (Poulin, 2007;
Brito
et al
., 2014). Tus, many of the characteristics of
the host habitat can infuence colonization by parasites
(Goater
et al
., 2005). Tis is due to how hosts respond to
biotic factors such as temperature, humidity, precipitation,
and others (Poulin & Krasnov, 2010).
Amphibian parasites can be directly afected by the
environment, physiology, behavior, and ecology of
their host (Bower
et al
., 2019). In amphibians, parasites
can induce behavioral changes in their hosts that favor
their establishment or transmission to their fnal host
(Hernandez-Caballero
et al
., 2022). Stress-induced
physiological changes can increase the host’s vulnerability
to parasitic infections (Herczeg
et al
., 2021), such as
physiological responses caused by pesticides (Rohr
et
al
., 2008; Hua
et al
., 2017). In addition, the presence
and abundance of highly lethal parasites in amphibian
populations may indicate susceptibility to disease and
environmental disturbances (Koprivnikar, 2012).
However, according to Oliveira
et al
. (2023), parasites are
distributed according to the dispersal of their hosts and are
not directly infuenced, as they are endoparasites, by the
biotic factors that commonly limit the dispersal of other
species. In this case, parasites are present in most anuran
species. Knowledge of the diversity and distribution of
parasites is therefore important for understanding the
role of parasite-host ecological relationships in ecosystem
dynamics (Poulin & Krasnov, 2010; Campião
et al
.,
2015b).
Since there is a lack of information on the parasitic fauna
of anuran amphibians in Piauí (Vieira
et al
., 2021), and
given their impact on the ecology of populations and
communities, the study of parasitism is important to
understand the relationships between host and parasite,
their impact on the trophic chain, and the infuence of
environmental factors on these relationships (Berkhout
et
al
., 2019; Oliveira
et al
., 2023). Furthermore, helminths
can also be used as bioindicators of environmental health
(Koprivnikar
et al
., 2012). Tis study aims to describe the
parasitic community associated with anuran amphibians
in the Sete Cidades National Park (PNSC), an important
conservation area in the state of Piauí, Brazil.
MATERIALS AND METHODS
Anuran amphibians were collected in the Sete Cidades
National Park (PNSC), an environmental protection
area located in the northern region of the state of Piauí
(04°02-08‘S, 41°40-45’W), Brazil, which has an average
altitude ranging from 100 and 290 meters (Ivanov &
Lemos, 2020). Te territory has typical characteristics
of a transition zone, with areas of Caatinga and Cerrado
(Della-Favera, 2002; Oliveira
et al
., 2010; Lopes
et al
.,
2011). Te anurans were collected at fve sampling points
throughout the park during the region’s rainy season,
using auditory and visual searches (Heyer
et al
., 1994),
during 19 collection days between March and May 2024,
from 18:00 to 00:00.
In the laboratory, the anurans were euthanized with a
lethal injection of thiopental sodium (Tiopentax®),
fixed in 10% formaldehyde, and preserved in 70%
alcohol. They were necropsied with ventral incisions in
the anteroposterior axis, and the following organs were
analyzed using a stereoscopic microscope: gastrointestinal
tract, lungs, liver, kidneys, and internal cavity. The
parasites were collected and prepared according to Amato
et al
. (1991). Te parasites were identifed according to the
specifc methodology for each taxonomic group, using the
following literature: Yamaguti (1971), Schmidt (1986),
Vicente
et al
. (1991), and Felix-Nascimento
et al
. (2020).
Te infection parameters were analyzed according to Bush
et al
. (1997). Te endoparasites identifed were deposited
in the Parasitological Collection of the Federal University
of Ceará (CPUFC; voucher: 1087 – 1112), Fortaleza,
Brazil, and their hosts in the Herpetological Collection of
the Federal University of Ceará (CHUFC; voucher: PN7C
01 – PN7C 318), Fortaleza, Brazil. We used a linear model
to verify the relationship between host size (snout-vent
length-SVL) and fnal parasite abundance.
Ethic aspects: All the procedures used in this work
comply with the ethical standards of the relevant
national and institutional guidelines on the care and
use of laboratory animals. Collection authorization
Chico Mendes Institute for Biodiversity Conservation -
ICMBio (#92796-1) and Ethics Committee on the Use
of Animals of the Federal University of Ceará (CEUA-
UFC) (#CEUA 6314010321).
36
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
Table 1
. List of endoparasites found in anuran hosts of the Sete Cidades National Park (PNSC), Piauí state, northeastern Brazil, and indication of new infection records.
N = number of hosts; NH = number of parasites; P% = prevalence; MII + R = mean intensity of infection + range; AB + SE = abundance + standard error.
Host (N
)
Parasite (NH)P%MII + AAB + SEReference
Bufonidae
Rhinella diptycha (18)
66
.
6716
.
17 (1 - 84)10
.
78 + 0
.
56
Aplectana hylambatis
(2)5.5620
.
11New record
Ochoterenella
sp
.
(1)5
.
5610
.
06
Aguiar
et al
. (2021); Benício
et al
.
(2022)
Oswaldocruzia mazzai
(157)22
.
2239
.
25 (5 - 84)8
.
72 + 3
.
29
Aguiar
et al
.
(2021); Oliveira
et al
.
(202
2)
Physaloptera
sp. (2)11
.
1110
.
11
Amorim
et al
.
(2019); Oliveira
et al.
(202
2)
Raillietnema spectans
(5)5
.
5650
.
27
Amorim
et al
. (2019); Oliveira
et al
.
(202
2)
Rhabdias
sp. (12)5
.
56120
.
67
Amorim
et al.
(2019); Aguiar
et al.
(2021); Oliveira
et al
. (202
2)
Cosmocercidae female (13)38
.
891
.
86 (1 - 3)0
.
72 + 0
.
18-
Ascarididae larva (4)5
.
5640
.
22-
Hylidae
Boana raniceps (4)
503 (1 - 5)1
.
5 + 0
.
87
Physalopteroides venancioi
(6)503 (1 - 5)1
.
5 + 0
.
87
Campião
et al
.
(2016a); Oliveira
et al
.
(202
2)
Dendropsophus minusculus (14)
14
.
294 (1 - 6)0
.
57 + 0.09
Brevimulticaecum
sp. (6)7
.
1460
.
42New record
Physocephalus
sp. (1)7
.
1410
.
07New record
Centrorhynchus
sp. (1)7
.
1410
.
07Oliveira
et al
. (202
2)
Dendropsophus minutus (33)
3
.
034 (1 - 3)0
.
12
(Continúa Tabla 1)
37
Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Centrorhynchus
sp. (3)3
.
0330
.
09Oliveira
et al
. (202
2)
Nematoda larva (1)3
.
0310
.
03-
Dendropsophus soaresi (3)
Not parasitized
Scinax fuscomarginatus (29)
17
.
244
.
8 (1 - 8)0
.
83 + 0
.
34
Cosmocerca podicipinus
(1)3
.
4510
.
03Campião
et al
. (2014)
Centrorhynchus
sp. (23)13
.
795
.
75 (5 - 8)0
.
79 + 0
.
68Aguiar
et al
. (2021)
Scinax nebulosus (3)
33
.
3310
.
33
Centrorhynchus
sp. (1)33
.
3310
.
33Campião
et al
. (2014)
Scinax similis
(32)
15
.
633
.
4 (1 - 5)0
.
53 + 0
.
09
Oxyascaris caudacutus
(6)9
.
382 (1 - 4)0
.
19 + 0
.
06New record
Cosmocercidae female (11)9
.
383
.
67 (2 - 5)0
.
34 + 0
.
11-
Scinax x-signatus (6)
33
.
331
.
5 (1 - 2)0
.
50 + 0
.
17
Ochoterenella
sp. (2)16
.
6720
.
33New record
Cosmocercidae female (1)16
.
6710
.
16-
Leptodactylidae
Adenomera juikitam (3)
33.3310
.
33
Centrorhynchus
sp. (1)33.3310
.
33New record
Leptodactylus fuscus (31)
90
.
3246
.
07 (1 - 216)41
.
61 + 1
.
12
Cosmocerca parva
(14)3
.
23140
.
45Morais (2013); Campião
et al
.
(2014)
Cosmocerca podicipinus
(21)12
.
95
.
25 (1 - 16)0
.
68 + 0
.
21Campião
et al
.
(2014)
Oswaldocruzia mazzai
(3)3
.
2330
.
1Campião
et al
.
(2014)
Oxyascaris catingae
(17)12
.
94
.
25 (2 - 8)0
.
55 + 0
.
17New record
Physaloptera
sp
.
(7)9
.
682
.
33 (2 - 3)0
.
23 + 0
.
07Morais (2013); Oliveira
et al
. (202
2)
Physalopteroides venancioi
(2)3
.
2320
.
06Campião
et al
. (2016a)
Porrocaecum
sp
.
(2)3
.
2320
.
06Campião
et al
. (2016a)
(Continúa Tabla 1)
(Continúa Tabla 1)
38
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
Raillietnema spectans
(264)22
.
5837
.
71 (16 - 57)8
.
52 + 2
.
37
Silva-Neta
et al.
(2020); Oliveira
et al
.
(202
2)
Rhabdias
sp. (3)3
.
2330
.
1Cañizales (2021); Oliveira
et al
.
(202
2)
Schrankiana schranki
(926)48
.
3961
.
73 (2 - 216)29
.
87 + 6
.
40Morais (2013); Oliveira
et al
. (202
2)
Cosmocercidae female (30)19
.
354
.
83 (1 - 16)0
.
94 + 0
.
28-
Cosmocercidae larva (3)6
.
451.50 (1 - 2)0
.
1-
Leptodactylus macrosternum (7)
10019
.
14 (1 - 27)19
.
14 + 1
.
09
Aplectana hylambatis
(5)14
.
2950
.
71New record
Brevimulticaecum
sp. (15)28
.
577
.
5 (2 - 13)2
.
14 + 1
.
17Goldberg
et al
.
(2007)
Cosmocerca podicipinus
(15)28
.
577
.
5 (3 - 12)2
.
14 + 1
.
16Campião
et al
.
(2014)
Oswaldocruzia mazzai
(4)14
.
2940
.
57
Silva-Neta
et al
. (2020); Oliveira
et al
.
(202
2)
Oxyascaris
sp. (2)14
.
2920
.
29New record
Physalopteroides venancioi
(37)71
.
427
.
4 (2 - 10)5
.
28 + 1
.
49Morais (2013); Campião
et al
.
(2016a)
Raillietnema spectans
(27)14
.
29273
.
85New record
Cosmocercidae female (4)28
.
5720
.
57-
Centrorhynchus
sp
.
(2)14
.
2920
.
29Campião
et al
.
(2014)
Oligacanthorhynchus
sp
.
(23)14
.
29233
.
28New record
Leptodactylus mystaceus (4)
754 (2 - 8)3 + 0
.
94
Cosmocerca podicipinus
(10)505 (2 - 8)2
.
5 + 1
.
38New record
Oxyascaris catingae
(2)2520
.
5New record
Leptodactylus pustulatus
(4)
802
.
5 (1 -4)2 + 0
.
34
Cosmocerca podicipinus
(3)2030,6Campião
et al
.
(2014)
Physaloptera
sp. (1)2010
.
2Morais (2013); Oliveira
et al
. (202
2)
Nematoda larva (2)4010
.
4-
(Continúa Tabla 1)
(Continúa Tabla 1)
39
Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Centrorhynchus
sp
.
(4)2040
.
8
Oliveira
et al
. (2024);
S
antos
et al
.
(2024)
Leptodactylus troglodytes
(16)
7515
.
75 (1 - 47)11
.
81 + 0
.
61
Aplectana hylambatis
(13)6.25130,81New record
Cosmocerca podicipinus
(35)258
.
75 (5 - 19)2
.
18 + 0
.
82New record
Oxyascaris
sp
.
(2)6
.
2520
.
12New record
Raillietnema spectans
(94)31
.
2518
.
8 (5 - 47)5
.
87 + 2
.
04Oliveira
et al
. (202
2)
Physaloptera
sp. (6)12
.
53 (1 - 5)0
.
37 + 0
.
16New record
Polystoma goeldii
(1)6
.
2510
.
06New record
Cosmocercidae larva (19)12
.
59
.
5 (7 - 12)1
.
18 + 0,52-
Cosmocercidae female (19)43
.
752
.
71 (1 -9)1
.
18 + 0
.
36-
Leptodactylus vastus (18)
100331
.
61 (1 - 654)331
.
61 + 12
.
08
Aplectana hylambatis
(1533)38
.
89219 (66 - 461)85
.
17 + 27
.
11New record
Cosmocerca
sp. (49)5
.
55492
.
72New record
Oswaldocruzia mazzai
(5)11
.
112
.
5 (1 - 4)0
.
28 + 0
.
11
Silva-Neta
et al
. (2020); Oliveira
et al
.
(202
2)
Physaloptera
sp. (34)22
.
228
.
5 (2 - 19)1
.
89 + 0.69Oliveira
et al
. (202
2)
Physalopteroides venancioi
(1)5
.
5610
.
05New record
Raillietnema spectans
(2570)77
.
78183
.
57 (1 - 648)142
.
78 + 33
.
90
Benício
et al
.
(2022); Oliveira
et al
.
(202
2)
Rhabdias
sp
.
(295)55
.
5629
.
5 (1 - 102)16
.
39 + 5
.
05Oliveira
et al
.
(202
2)
Schrankiana schranki
(1454)16
.
67
484
.
67 (200 -
654)
80
.
78 + 31
.
73
Campião
et al.
(2014); Oliveira
et al
.
(202
2)
Ascarididae larva (1)5
.
5510
.
05-
Centrorhynchus
sp. (3)5
.
5530
.
17Oliveira
et al
.
(202
2)
Polystoma goeldii
(8)16
.
662
.
66 (1 - 6)0
.
44 + 0
.
17New record
(Continúa Tabla 1)
(Continúa Tabla 1)
40
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
Physalaemus cuvieri (22)
72
.
739
.
56 (1 - 25)6
.
95 + 0
.
36
Cosmocerca podicipinus
(139)59
.
110
.
70 (1 - 25)6
.
31 + 1
.
27Oliveira
et al
.
(202
2)
Oswaldocruzia mazzai
(1)4
.
5510
.
05Oliveira
et al
.
(2019)
Oxyascaris
sp. (3)4
.
5530
.
13New record
Physalopteroides venancioi
(1)4
.
5510
.
05New record
Strongyloides
sp. (4)9
.
12 (1 - 3)0
.
18Oliveira
et al
. (202
2)
Cosmocercidae larva (4)9
.
120
.
18-
Nematoda larva (1)4
.
5510
.
05-
Pleurodema diplolister (31)
35.482.91 (1 - 5)1.03 + 0.05
Ochoterenella
sp. (1)3
.
2310
.
03
Silva-
Neta
et al
.
(2020)
Oxyascaris catingae
(13)22
.
581.85 (1 - 4)0
.
42 + 0
.
12New record
Physaloptera
sp. (6)9
.
682 (1 - 4)0
.
19 + 0
.
06New record
Raillietnema spectans
(1)3
.
2310
.
03
Silva-
Neta
et al
.
(2020)
Schrankiana schranki
(3)3
.
2330
.
1New record
Cosmocercidae female (2)6
.
4510
.
06-
Cylindrotaenia americana
(6)6
.
453 (1 - 5)0
.
19
Silva-
Neta
et al
. (2020)
Pseudopaludicola mystacalis
(34)
32
.
351
.
82 (1 - 3)0
.
59 + 0
.
04
Cosmocerca parva
(2)5
.
8810
.
06New record
Cosmocerca podicipinus
(11)23
.
531
.
38 (1 - 3)0
.
32 + 0
.
18New record
Oxyascaris
sp. (3)5
.
881
.
50 (1 - 2)0
.
09New record
Physaloptera
sp. (1)2
.
9410
.
03
Silva-
Neta
et al
. (2020)
Rhabdias
sp. (1)2
.
9410
.
03New record
(Continúa Tabla 1)
(Continúa Tabla 1)
41
Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Cosmocercidae female (1)2
.
9410
.
03-
Centrorhynchus
sp. (1)2
.
9410
.
03New record
Microhylidae
Elachistocleis piauiensis (3)
Not parasitized
Odontophrynidae
Proceratophrys cristiceps (3)
33
.
3310
.
33
Cosmocerca
sp. (1)33.3310
.
33New record
RESULTS
We analyzed 318 anuran amphibians, distributed among
21 species and four families. Of these, 142 individuals
were parasitized by at least one endoparasite species,
with an overall prevalence of 44.65% (see Table 1). A
total of 8,056 parasite specimens were counted and
identifed in 26 parasite taxa, with an average infection
intensity of 56.73 and abundance of 25.33. Among the
most abundant species found were
Raillietnema spectans
Gomes, 1964 (3,034 individuals),
Schrankiana schranki
(Travassos, 1925) (2,383 individuals), and
Aplectana
hylambatis
Baylis, 1925 (1,540 individuals).
Leptodactylidae was the family with the largest number
of parasites, with an average of seven parasite species per
host analyzed.
Leptodactylus fuscus
(Schneider, 1799) was
the species with the greatest diversity of parasite species
identifed (12 spp.). Te parasitic fauna of anurans in the
SCNP was previously composed of 13 parasite taxa, in
only four anuran species. Here, we recorded 21 additional
parasite taxa, with new infection records in 17 anuran
host species. In addition, we added 19 new parasite taxa
to the existing records for the state of Piauí, signifcantly
expanding knowledge about the region. Also analyzing the
infuence of the SVL on parasite abundance, identifying
that for the endoparasitic community, the size of the host
is an infuential factor in the expected fnal richness (R2
= 0.37; p < 0,001).
DISCUSSION
Amphibians are excellent models for studies investigating
the diversity of parasitic communities (Aho, 1990;
Campião
et al
., 2015b). Te fauna of endoparasites
associated with anurans is rich and diverse, being
characterized by a wide distribution and low host
specifcity (Campião
et al
., 2014). It has a strong tendency
to increase considerably as new areas and new available
hosts are sampled (Campião
et al
., 2015b).
According to Campião
et al
. (2014), around 90% of
Brazilian anurans have not yet been studied regarding
their parasite fauna, with anurans from the Hylidae
and Leptodactylidae families being the most frequently
studied hosts. Commonly, nematodes and trematodes are
the most recorded in these amphibians (Campião
et al
.,
2014). Campião
et al
. (2015b) claim that leptodactylids
have rich parasite communities, with a great taxonomic
diversity, mainly composed of nematodes. In our results,
leptodactylid species presented the highest prevalence,
(Continúa Tabla 1)
42
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
diversity, and parasite richness. We also observed that
most that infections were caused by nematodes, which
seems to be a pattern common to species of this family,
corroborated by several other studies (see Teles
et al
.,
2015; Oliveira
et al
., 2019, 2022).
As for the low parasite prevalence found in some host
species, Chandra & Gupta (2007) highlight that habitat
characteristics can infuence the composition and structure
of the helminth fauna associated with amphibians, which
are generally associated with two types of environments
(aquatic and terrestrial). Tus, terrestrial species are more
likely to come into direct contact with infective larvae than
arboreal species, which allows a greater variety of parasites
to settle in these animals (Chandra & Gupta, 2007).
Tus, one factor that may explain this low prevalence is
the host’s use of the habitat and the direct transmission
of the parasite subcutaneously. Another point is the fact
that some species show aestivation behavior and have
explosive reproduction, which may have made it difcult
for the species to fnd infective larvae and thus infuenced
these results.
Overall, the PNSC showed a high diversity of parasitic
species infecting anurans (26 taxa). Te richness found
in this study is similar to other studies dealing with the
helminth community associated with anurans (Campião
et al
., 2016a; Graça
et al
., 2017), as well as in other
conservation areas such as the Environmental Protection
Area (APA) of Serra de Maranguape (Oliveira
et al
., 2022)
and the APA of Bica do Ipu (Silva-Neta
et al
., 2020).
However, this richness may still be underestimated due
to unidentifed species, such as the occurrence of cryptic
species, such as in Rhabdiasidae (Müeller
et al
., 2018), or
species that were not feasible to identify.
In the last decade, several studies on parasitism in
Brazilian amphibians have been carried out (Teles
et al
.,
2015; Graça
et al
., 2017; Silva
et al
., 2019; Mascarenhas
et al
., 2021; Oliveira
et al
., 2024; Santos
et al
., 2024).
Even so, for the PNSC only the species
Dermatonotus
muelleri
(Boettger, 1885),
Leptodactylus vastus
Lutz,
1930,
Rhinella diptycha
(Cope, 1862), and
Trachycephalus
typhonius
(Linnaeus, 1758) have their helminth fauna
known (Benício
et al
., 2022). According to Aguiar
et
al
. (2014), with the increase in parasitological studies,
especially in areas that have not yet been sampled and
hosts that have not been studied much, it is common
to fnd new records of parasites that have not yet been
reported for host species.
A good example is
Physalaemus cuvieri
(Fitzinger, 1826
)
,
a species widely distributed throughout Brazil (Segalla
et
al
., 2021) and well-known for parasite studies throughout
its distribution (see Santos & Amato, 2013; Aguiar
et
al
., 2015; Graça
et al
., 2017; Oliveira
et al
., 2019; Silva-
Neta
et al
., 2020; Aguiar
et al
., 2021; Sani
et al
., 2021;
Oliveira
et al
., 2022). We still present in our results the
frst record of infection of
Physalopteroides venancioi
Lent,
Freitas & Proença, 1946 and
Oxyascaris
sp. for this host.
We also presented 33 new records of parasite infection
for 14 species of new hosts and added 19 taxa to the
records already known for the state of Piauí. Our study
corroborates the results of Aguiar
et al
. (2014), that it is
common to fnd new records of parasites in widely studied
species, and highlights the need for more parasitological
work with host species throughout their distribution and
in areas that are still little known since parasite diversity
and the parasite-host relationship are still far from being
truly known.
Nematodes are diverse, abundant, generalist, and well-
distributed in the environment. Tey have a direct life
cycle and reach their hosts through oral ingestion or
active penetration of infective larvae through the skin
(Anderson, 2000). In this study, 69% of the parasites
identifed were Nematoda, following the same pattern of
infection found in other neotropical anurans (Campião
et al
., 2016a; Graça
et
al
., 2017; Oliveira
et al
., 2019;
Silva-Neta
et al
., 2020; Mascarenhas
et al
., 2021; Oliveira
et al
., 2022).
Monoxenous parasites such as
R. spectans
,
S. schranki
, and
A. hylambatis
were the most abundant species. However,
Cosmocerca podicipinus
Baker & Vaucher, 1984,
R.
spectans
, and
Oswaldocruzia mazzai
Travassos, 1935 were
the species that most infected diferent hosts. According
to Anderson (2000), parasites with direct life cycles have
low specifcity and a simple mode of transmission, which
can occur through the ingestion of eggs or penetration
of larvae through the host’s skin. Te high abundance
of some parasite species may be associated with parasite
self-infection due to the reproduction of these parasites in
their hosts (Anderson, 2000). In addition, these species
have been recorded infecting several Neotropical anurans
(Campião
et al
., 2014; Teles
et al
., 2015; Alcantara
et al
., 2018; Oliveira
et al
., 2019). Possibly the wide
distribution of these parasites and their generalist habitats
in terms of host selection (Campião
et al
., 2014, 2015b;
Oliveira
et al
., 2019, 2023) are also responsible for the
high infection rates.
A signifcant number of parasitic larvae have been found
in the small and/or large intestines of various host species.
Larvae of this type are commonly found in amphibian
species (Campião
et al
., 2014; Oliveira
et al
., 2022),
43
Endoparasites of anurans in the seven cities national park
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
and this larval stage may be associated with the parasite’s
monoxenic cycle (Anderson, 2000), as well as a possible
recent infection and/or reproduction of the adult parasites
in the host. As for the large number of unidentifed female
specimens, this is due to the lack of taxonomic characters
that would enable identifcation, often caused during the
fxation of the hosts previously. In addition, the lack of
taxonomic studies is also a limiting factor for the accurate
identifcation of some parasite species distributed in the
region studied (Felix-Nascimento
et al
., 2020).
Te species of
Centrorhynchus
and
Oligacanthorhynchus
are heteroxenous and generally have mammals
and/or birds as defnitive hosts (Smales, 2007;
Richardson
et al
., 2014), with amphibians being
paratenic hosts (Yamaguti, 1963). In South America,
Oligacanthorhynchus
sp. has been recorded infecting
Odontophrynus americanus
(Duméril & Bibron, 1841)
(Campião
et al
., 2014),
Pleurodema diplolister
(Peters,
1870) (Silva-Neta
et al
., 2020), and
L. vastus
(Oliveira
et
al
., 2022). In the present study,
Oligacanthorhynchus
sp.
was recorded parasitizing
Leptodactylus macrosternum
Miranda-Ribeiro, 1926.
I
n amphibians, only the ascarid species
Brevimulticaecum
sp. and
Porrocaecum
sp. are recorded for these hosts
(González & Hamann, 2013; Campião
et al
., 2016a).
We identifed 21 individuals of
Brevimulticaecum
sp. parasitizing the species
L. macrosternum
and
Dendropsophus minusculus
(Rivero, 1971), and two
individuals of
Porrocaecum
sp. infecting
L. fuscus
.
Ascarids of this type have been reported parasitizing
fsh, reptiles, and amphibians (Vieira
et al
., 2010).
However, these parasites have crocodilians, freshwater
rays, and teleosts as their defnitive hosts in the life cycle
(Goldberg et al., 2007; Reyda, 2008), while amphibians
function as intermediate hosts. Tis is the frst record
of
Brevimulticaecum
sp. infection in
D. minusculus
(Rivero, 1971), however, due to the larval stage of this
parasite, it was not possible to identify it at the species
level.
Te
Strongyloides
Grassi, 1879 genus has a low specifcity
and has already been reported for a variety of anurans
such as
Boana raniceps
(Cope, 1862),
Physalaemus
albonotatus
(Steindachner, 1864),
Physalaemus cuvieri
Fitzinger, 1826,
Pithecopus gonzagai
Andrade, Haga,
Ferreira, Recco-Pimentel, Toledo & Bruschi, 2020,
Pristimantis relictus
Roberto, Loebmann & Ávila, 2022,
Scinax x-signatus
(Spix, 1824),
T. typhonius
,
Leptodactylus
gracilis
(Duméril & Bibron, 1841),
Rhinella dorbignyi
(Duméril & Bibron, 1841),
Rhinella icterica
(Spix, 1824),
and
Proceratophrys ararype
Mângia, Koroiva, Nunes,
Roberto, Ávila, Sant’Anna, Santana & Garda, 2018
(Campião
et al
., 2014; Mascarenhas
et al
., 2021; Oliveira
et al
., 2022). Although its biology is not detailed, it is
known that these parasites commonly have a direct life
cycle; infection occurs through dermal penetration and
ingestion of infected prey (Mati & Melo, 2014; Sulieman
et al
., 2015). However, even though these parasites are
capable of infecting several anuran species (Campião
et
al
., 2014), they generally show low infection rates, as
observed in this study for
P. cuvieri
.
Te Cestoda
Cylindrotaenia americana
Jewell, 1916
has been recorded in several amphibians in Brazil
(Toledo
et al
., 2013; Oliveira
et al
., 2019, Silva-Neta
et
al
., 2020; Oliveira
et al
., 2022). In the Caatinga, the
frst record of
C. americana
was made for
Physalaemus
cicada
Bokermann, 1966 (Oliveira
et al
., 2019), later
in
P. diplolister
in high-altitude swamps inserted in
the Caatinga (Silva-Neta
et al
., 2020). In our results,
we recorded
C. americana
parasitizing
P. diplolister
in Cerrado areas. In Brazil, there are few records of
monogeneans, the majority being reported for the genus
Polystoma
Zeder, 1800 (Santos & Amato, 2012). Tis
is the best-known genus among the Polystomatidae
(Sinnappah
et al
., 2001), with a direct life cycle that can
be completed in the gills of young tadpoles or inside the
urinary bladder of adult frogs (Bentz
et al
., 2006). Here,
we report specimens of
Polystoma goeldii
Sales, Du Preez,
Verneau & Domingues, 2023 infecting
Leptodactylus
troglodytes
A. Lutz, 1926 and
Leptodactylus vastus
A.
Lutz, 1930, this being the frst record for the host
species and the expansion of the parasite’s distribution
area (Pará state) to the state of Piauí.
Several studies report that host body size can infuence
the establishment of parasite communities (Campião
et
al
., 2015a; Silva-Neta
et al
., 2020). Larger individuals
generally ofer larger colonization areas, providing
adequate resources for parasite development and
reproduction (Campião
et al
., 2015a; 2016b). However,
Oliveira
et al
. (2023) report that host size is only
infuential when there is signifcant size variation among
individuals. In the present study, the size of anuran hosts
was a determining factor in parasite abundance; this fact
may be related to the larger surface area available for
colonization (Toledo
et al
., 2017).
In our study, we demonstrated that the endoparasites
composition of anurans from the PNSC follows the
common pattern described for Neotropical amphibians,
presenting high species richness and prevalence, with a
strong relationship between abundance and host size.
We also expanded the parasitological knowledge for
44
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Uchôa
et al.
the region and added new parasite taxa to the existing
records for the Piauí state, highlighting the importance
of amphibians as models for parasite studies. In addition,
we reafrm the importance of parasite inventories for
host species in poorly studied regions, considering the
need to signifcantly expand knowledge about parasitism
in amphibians.
ACKNOWLEDGMENTS
We would like to thank the Fundac
̧
a
̃
o Cearense de
Apoio ao Desenvolvimento Cienti
́
fco e Tecnolo
́
gico
for a postdoc fellowship granted to CRO (FUNCAP/
CNPq FPD-0213-00385.01.00/23). JSU thanks the
Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior - Capes for the master’s scholarship.
Author contributions: CRediT (Contributor Roles
Taxonomy)
JSU
= Jacilene de Sousa Uchôa
CRO
= Cicero Ricardo de Oliveira
EBA
= Etielle Barroso de Andrade
DMBN
= Diva Maria Borges-Nojosa
Conceptualization
: JSU
Data curation
: CRO, DMBN
Formal Analysis
: JSU, CRO
Funding acquisition
: DMBN, EBA
Investigation
: JSU, CRO, EBA, DMBN
Methodology
: JSU, CRO, EBA, DMBN
Project administration
: JSU
Resources
: DMBN, EBA
Software
: JSU, CRO, EBA, DMBN
Supervision
: DMBN, EBA
Validation
: JSU, CRO, EBA, DMBN
Visualization:
JSU, CRO
Writing – original draft
: JSU, CRO, EBA, DMBN
Writing – review & editing
: JSU, CRO, EBA, DMBN
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