157
Biodiversity of parasites infecting
Bothrops erythromelas
Neotropical Helminthology (Lima). Vol. 18, N
º
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Neotropical Helminthology
Neotropical Helminthology, 2024, vol. 18 (2), 157-175
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
BIODIVERSITY OF PARASITES INFECTING
BOTHROPS ERYTHROMELAS
AMARAL, 1923 (SQUAMATA, VIPERIDAE): AN ENDEMIC VENOMOUS
SNAKE SPECIES FROM THE BRAZILIAN NORTHEAST
BIODIVERSIDAD DE PARÁSITOS QUE INFECTAN A
BOTHROPS
ERYTHROMELAS
AMARAL, 1923 (SQUAMATA, VIPERIDAE): UNA ESPECIE
DE SERPIENTE VENENOSA ENDÉMICA DEL NORESTE DE BRASIL
Cicera Silvilene Leite Matias¹
,
²
,
*; Cristiana Ferreira-Silva³; Willianilson Pessoa-da-Silva¹
,
²; Maria
Beatriz de Andrade Sousa¹
,
²; Aldenir Ferreira Silva-Neta²; Robson Waldemar Ávila³;
Felipe Gobbi Grazziotin
4
& Adrian Antonio Garda¹
,
²
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20242181808
Universidad Nacional
Federico Villarreal
Volume 18, Number 2 (jul - dic) 2024
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
T e knowledge of parasitic fauna in wild animals is essential for understanding the ecological conditions that determine
the occurrence and prevalence of parasites in their hosts. Except for records of one Pentastomida (
Cephalobaena tetrapoda
Heymons, 1922) and two Nematoda (
Physaloptera
sp. And
Aspiculuris
sp.), detailed information about the helminth
fauna associated with the jararaca
Bothrops erythromelas
Amaral, 1923 is lacking. T is species has a wide distribution
in the Caatinga, with records in marginal areas of the Cerrado and Atlantic Forest. Here, we describe the patterns of
¹ Programa de Pós-graduação em Ciências Biológicas (Zoologia) Universidade Federal da Paraíba - Via Expressa Padre Zé
Jardim, Cidade Universitária, 58051001, João Pessoa, PB, Brazil;
² Laboratório de Anfíbios e Répteis, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus
Universitário, Lagoa Nova, Av. Senador Salgado Filho, 3000, 59078-900, Natal, RN - Brasil
³ Universidade Federal do Ceará (UFC), Departamento de Biologia, Centro de Ciências, Av. Mister Hull, s/n, CEP 60455-
760, Fortaleza, Ceará, Brazil
4
Laboratório de Coleções Zoológicas, Instituto Butantan, São Paulo, 05503-900, SP, Brazil
* Corresponding author
:
silvilenematias@gmail.com
Cicera Silvilene Leite Matias:
https://orcid.org/0000-0002-2812-0106
Cristiana Ferreira-Silva:
https://orcid.org/0000-0002-3087-2614
Willianilson Pessoa-da-Silva:
https://orcid.org/0000-0002-4975-5733
Maria Beatriz de Andrade Sousa:
https://orcid.org/0009-0007-9158-8928
Aldenir Ferreira Silva-Neta:
https://orcid.org/0000-0003-4245-5233
Robson Waldemar Ávila:
https://orcid.org/0000-0003-3641-8321
Felipe Gobbi Grazziotin:
https://orcid.org/0000-0001-9896-9722
Adrian Antonio Garda:
https://orcid.org/0000-0002-1178-1207
158
Neotropical Helminthology (Lima). Vol. 18, N
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Leite Matias
et al.
richness, abundance, and prevalence of helminths in
B. erythromelas,
a venomous snake from northeastern Brazil. Te
parasitized snakes were collected from six Brazilian states in the Northeast region: Bahia, Ceará, Paraíba, Pernambuco,
Piauí, and Rio Grande do Norte. We examined the gastrointestinal tract of 127 specimens and found 76 individuals
infected with at least one endoparasite, represented by 17
taxa
of helminths: two Acanthocephala, three Cestoda, and
12 Nematoda. With our results, knowledge about hidden biodiversity is expanded, particularly as this is a pioneering
study regarding the helminth fauna of
B. erythromelas.
We also describe the occurrence of the species
Physaloptera lutzi
Cristofaro, Guimarães & Rodrigues, 1976, and
Parapharyngodon hispidus
Ferreita
et al
., 2021 for the frst time in snakes.
Keywords.
Acanthocephala – Caatinga – Cestoda – Inventory – Nematoda – Parasites
RESUMEN
El conocimiento de la fauna parasitaria en animales silvestres es esencial para comprender las condiciones ecológicas
que determinan la ocurrencia y prevalencia de parásitos en sus hospedadores. Con la excepción de registros de un
Pentastomida (
Cephalobaena tetrapoda
Heymons, 1922) y dos Nematoda (
Physaloptera
sp. y
Aspiculuris
sp.), falta
información detallada sobre la fauna de helmintos asociada con la jararaca
Bothrops erythromelas
Amaral, 1923
.
Esta
especie tiene una amplia distribución en la Caatinga, con registros en áreas marginales del Cerrado y la Mata Atlántica.
Aquí, describimos los patrones de riqueza, abundancia y prevalencia de helmintos en
B. erythromelas
, una serpiente
venenosa del noreste de Brasil. Las serpientes parasitadas fueron recolectadas en seis estados brasileños de la región
Nordeste: Bahia, Ceará, Paraíba, Pernambuco, Piauí y Rio Grande do Norte. Examinamos el tracto gastrointestinal de
127 especímenes y encontramos 76 individuos infectados con al menos un endoparásito, representado por 17 taxones de
helmintos: dos Acanthocephala, tres Cestoda y 12 Nematoda. Con nuestros resultados, se amplía el conocimiento sobre
la biodiversidad oculta, especialmente porque este es un estudio pionero sobre la fauna de helmintos de
B. erythromelas.
También describimos por primera vez la ocurrencia de las especies
Physaloptera lutzi
Cristofaro, Guimarães & Rodrigues,
1976 y
Parapharyngodon hispidus
Ferreira
et al
., 2021 en serpientes.
Palabras clave:
Acanthocephala – Caatinga – Cestoda – Inventario – Nematoda – Parásitos
INTRODUCTION
Parasitological studies in reptiles have expanded in recent
years, particularly those involving snakes (Ávila
et al.,
2013; Kuzmin
et al.,
2016; Mati
et al.,
2015; Matias
et al.,
2018; Quirino
et al.,
2018; Oliveira
et al.,
2020,
2023; Araújo
et al.,
2020; Halán & Kottferová, 2021;
Oliveira
et al.
, 2023; Conga
et al.,
2024), which can serve
as defnitive or intermediate hosts for various groups of
parasites (Araújo
et al.,
2020; Oliveira
et al.,
2021; Ferreira-
Silva
et al.,
2022). Understanding the parasitic fauna of
wild animals is crucial for comprehending ecological
interactions of parasites and their hosts, including
natural history, life cycles, and evolutionary aspects
of this relationship (Silva, 2008; Matias
et al.,
2018).
Detrimental efects of parasites on host ftness include,
among others, the alteration of coloration patterns and,
consequently, negative impacts on reproductive success
(Schall & Dearing, 1987; Dunlap & Schall, 1995; Levri,
1999).
Given the importance and biological diversity of the
genus
Bothrops,
which comprises approximately 63
species worldwide (Uetz
et al.,
2023), only 14 species of
the genus have been studied in the Neotropical Region to
understand their helminth fauna:
B. alternatus
Duméril,
Bibron & Duméril, 1854,
B. asper
Garman, 1883,
B.
atrox
Linnaeus, 1758,
B. barnetti
Parker, 1938
,
B. cotiara
Gomes, 1913
,
B. erythromelas
Amaral, 1923,
B. insularis
Amaral, 1922,
B. jararaca
Wied-Neuwied, 1824,
B.
jararacussu
Lacerda, 1884
, B. lanceolatus
Bonnaterre,
1790
, B. mattogrossensis
Amaral, 1825
, B. moojeni
Hoge,
1966
, B. neuwiedi
Wagler, 1924
, B. pradoi
Hoge, 1948
(Conga
et al.,
2024), however, these studies are essential
for understanding interspecifc relationships.
In this study, we present for the frst time, a comprehensive
analysis of the helminth fauna associated with
Bothrops
erythromelas
, the Caatinga lancehead (jararaca-da-seca in
Portuguese).
Bothrops erythromelas
is widely distributed
in the Caatinga, throughout the Brazilian states of
159
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Bothrops erythromelas
Neotropical Helminthology (Lima). Vol. 18, N
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Alagoas, Bahia, Ceará, Maranhão, Minas Gerais, Paraíba,
Pernambuco, Piauí, Rio Grande do Norte, and Sergipe;
with records in marginal areas along the Cerrado and
Atlantic Forest ecotones (Campbell & Lamar, 2004;
Nogueira
et al.,
2019; Costa
et al.,
2023).
Bothrops
erythromelas
is the most important species from an
epidemiological perspective, as it causes most of the life-
threatening snake bites in the Brazilian semi-arid region
(Lira-da-Silva
et al.,
2009). Additionally, the species has
a key ecological role, contributing to the population
size equilibrium of several small vertebrates in the
ecosystem (e.g., rodents, amphibians, lizards; Martins
et
al.,
2002). Currently, only three records of endoparasites
were registered for
B. erythromelas
, one Pentastomida
(
Cephalobaena tetrapoda
Heymons, 1922;
Oliveira
et al.,
2015) and two Nematoda (
Physaloptera
sp., Oliveira et
al., 2018;
Aspiculuris
sp., Batista
et al.,
2021). Terefore,
a proper appreciation of the species interaction with
parasites is crucial for understanding the occurrence and
abundance patterns of endoparasites associated with this
venomous snake, as well as the resulting medical and
ecological implications (Jorge
et al.,
2015).
MATERIALS AND METHODS
Tese parasitized snakes were sourced from four
northeastern brazilian states: Bahia (N = 7), Ceará (N =
33), Paraíba (N = 3), Pernambuco (N = 11), Piauí (N = 1),
and Rio Grande do Norte (N = 21). Specimens utilized
in this investigation were retrieved from Biological
Collections: specifcally, the Herpetological Collection
of the Regional University of Cariri - URCA (N = 20),
the Herpetological Collection of the Semiarid - UFERSA
(N = 8), the Herpetological Collection of the Federal
University of Ceará - NUROF/UFC (N = 23), and the
Herpetological Collection of the Federal University of
Paraíba - UFPB (N = 25).
We carefully examined the presence of parasites in the
gastrointestinal tract (esophagus, stomach, small and large
intestines), liver, kidneys, lungs, gallbladder, and celomic
cavity of the snakes under a stereomicroscope. Helminths
were identifed to the lowest possible taxonomic level. To
achieve this, we stained Cestodes and Acanthocephala
with alcoholic chloride carmine solution, and cleared
with eugenol, while species of and Nematoda were cleared
in lactic acid (Amato & Amato, 2010). To visualize the
internal and external morphological characters of the
helminths, we utilized an optical microscope. Following
identifcation, all helminths were deposited in the
Parasitological Collection of the Federal University of
Ceara (UFC-P).
We calculated the parasitological parameters of abundance,
richness, and prevalence following the method outlined
by Bush
et al.
(1997), using the software Quantitative
Parasitology 3.0. Richness was determined as the total
number of parasite species, while abundance represented
the total count of parasite individuals found in each of the
76 specimens of
B. erythromelas.
To assess whether parasite
richness is infuenced by the linear measure of host size
(snout-vent length: SVL), sex, and whether abundance is
infuenced by SVL, sex, and host maturity, we employed
a Generalized Linear Model (GLM). In this analysis,
predictor variables were included with interaction terms.
Given that richness and abundance data are count data,
we incorporated a Poisson error structure into the model.
Tese statistical analyses were conducted using R version
4.3.1 (R
Core Team,
2023).
Ethic aspects
: Te specimens used in this study were
collected under the approved authorization (29613-1)
conceived by Instituto Chico Mendes de Conservação da
Biodiversidade (ICMBio/SISBIO) from the Ministério
do Meio Ambiente (MMA) of Brazil. Te collecting,
hold and storage were previously revised by the Ethics
and Animal Welfare Committee from the Universidade
Regional do Cariri (#00026/2015).
RESULTS
Out of the 127 snakes analyzed, 76 specimens were
found to harbor parasites, comprising 17 helminth taxa:
two Acanthocephala (cystacanths of
Centrorhynchus
sp. and Oligacanthorhynchidae gen. sp.) with a
prevalence of 46.90%, three Cestoda (specimens
of
Oochoristica
sp. and larvae of Plerocercoid and
Cysticercoid) with a prevalence of 2.76%, and 12
Nematoda (
Brevimulticaecum
sp., Cosmocercidae gen.
sp.,
Hexametra boddaertii
Baird, 1860,
Oswaldocruzia
sp.,
Parapharyngodon hispidus
Ferreita
et al.,
2021,
Physaloptera lutzi
Cristofaro, Guimarães & Rodrigues,
1976,
Physaloptera nordestina
Matias, Morais & Ávila
,
2020,
Physaloptera
sp.,
Physalopteroides venancioi
Lent
et al
. 1946,
Physocephalus
sp.,
Strongyloides ophidiae
Pereira, 1929, and unidentifed nematode larvae) with
a prevalence of 50.34%. Te overall parasite prevalence
in
B. erythromelas
was 59.84%, with a mean infection
intensity of 13.88 ± 7.0 (range: 1–350) (Table 1, Fig. 1).
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(Continued Figure 1)
161
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(Continued Figure 1)
(Continued Figure 1)
162
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et al.
Figure 1.
Helminth species parasitizing
Bothrops erythromelas
-
Acanthocephala: a -
Centrorhynchus
sp.,
b -
Oligacanthorhynchidae gen. sp.,
Cestoda: c -
Oochoristica
sp. (mature proglottids),
d -
Plerocercoid Larvae,
e -
Cisticercoid
Larvae,
Nematoda: f -
Brevimulticaecum
sp. (anterior end of the larvae),
g -
Cosmocercidae gen. sp. (female adult),
h
and I -
Hexametra boddaertii
(anterior end and tail of the male, respectively),
j
and
k -
Oswaldocruzia
sp. (anterior end
and posterior end of the female, respectively),
l
and
m -
Parapharyngodon hispidus
(anterior end and tail of the male,
respectively),
n
and
o -
Physaloptera lutzi
(anterior end and tail of the male, respectively) and
p -
Physaloptera nordestina
(male’s tail),
q -
Physaloptera
sp.,
r -
Physalopteroides venancioi
(anterior end of the female),
s
and
t -
Physocephalus
sp.
(anterior end and posterior end of the larvae, respectively),
u
and
v -
Strongyloides ophidiae
(panoramic view and eggs of
the female, respectively),
w
and
x -
Nematoda not identifed (anterior end and posterior end of the larvae, respectively).
(Continued Figure 1)
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Among the parasites found, the cystacanth of
Oligacanthorhynchidae was the most abundant, with
350 individuals, followed by
Physaloptera
sp., with
239. Te rarest species, with only one individual
found, were
Brevimulticaecum
sp.,
Oswaldocruzia
sp.,
and
Physocephalus
sp. Parasite richness was positively
infuenced by the SVL of the hosts, with no efect of sex
or interaction between them (Table 2, Fig. 2). Parasite
abundance was also positively infuenced by SVL.
Additionally, females tended to have higher parasite
abundance than males, and both sexes tended to have
higher abundance with increasing SVL (Table 3, Fig. 3).
Table 1.
Parasitological indices of endoparasites in
Bothrops erythromelas
(equivalent to hosts infected with at least one
species of parasite). Development stage (DS), Larvae (L), Adut (A), Prevalence values (P%), number of endoparasites
(NE), mean intensity of infection and standard deviation (MII ± SD), mean abundance (MA), site of infection (SI) Sto=
stomach; Igi= large intestine; Smi= small intestine, Per= Peritoneum. Northeastern Brazilian state where the host was
collected: Bahia (BA), Ceará (CE), Paraíba (PB), Pernambuco (PE), Piauí (PI), and Rio Grande do Norte (RN). * New
record for
B. erythromelas
and ** new record for snakes.
EndoparasitesDSP%NEMII±SDMASIStates
Acanthocephala
Centrorhynchus
sp.*L13.2565.6 ± 2.525Per, Sto CE, PE, RN
Oligacanthorhynchidae gen. sp.*
L75.0350 6.1 ± 4.046 Per, Sto, Igi, SmiBA, CE, PB, PE, PI, RN
Cestoda
Oochoristica
sp.*A2.6 31.5 ± 1.5 1 Igi, SmiBA, CE
Plerocercoid larvae*L 1.3 22.0 ± 2.0 - PerRN
Cisticercoid larvae*L1.3 1313.0 ± 13.0 - Sto CE
Nematoda
Brevimulticaecum
sp.*L 1.3 1 1.0 ± 1.0-PerCE
Cosmocercidae gen. sp.*A 2.6 94.5 ± 4.5 7 Smi, Per CE, RN
Hexametra boddaertii*
A9.2223.1 ± 1.09Per, Sto, IgiCE, RN
Oswaldocruzia
sp.*A1.311.0 ± 1.0-StoCE
Parapharyngodon hispidus
**
A1.388.0 ± 8.0-StoCE
Physaloptera lutzi
**
A13.2414.1 ± 3.513Per, Igi, Sto, SmiCE, RN
Physaloptera nordestina*
A2.631.5 ± 1.51Per, StoPE, RN
Physaloptera
sp.L22.423914.1 ± 9.065Smi, Sto, Per,IgiBA, CE, PE, RN
Physalopteroides venancioi*
A2.6168.0 ± 8.06Igi, StoBA, CE
Physocephalus
sp.*L1.311.0 ± 1.0-StoPE
Strongyloides ophidiae*
A7.921736.2 ± 30.580Sto, Per, Smi, CE, RN
Nematoda (not identifed)L22.4734.3 ± 2.017Per, Smi, IgiBA, CE, PE, RN
Table 2.
GLM model testing how parasite richness varies as a function of host body condition index (SVL), sex, and
their interactions.
Variables EstimateStandard errorvalue ZValue P
Intercepto-0.4680.555-0.8440.398
SVL0.0030.0012.188
0.028
Sex0.3641.0090.3610.718
SVL:Sex-0.0010.002-0.4460.655
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Table 3.
GLM model testing how parasite abundance varies as a function of host body condition index (SVL), sex, and
their interactions.
VariablesEstimateStandard errorValue ZValue P
Intercept
0.5640.2022.7880.005
SVL
0.0050.00011.849<0.001
Sex-0.0340.438-0.0780.938
SVL: Sex0.0000.001-0.2550.798
Figure 2.
Species richness of parasites in relation to the body condition index (SVL) of
Bothrops erythromelas
specimens.
Figure 3
. Parasite abundances in relation to the body condition index (SVL) for males and females of
B
othrops
erythromelas
species.
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Neotropical Helminthology (Lima). Vol. 18, N
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DISCUSSION
Bothrops erythromelas
exhibited a high prevalence of
helminths (59.84%), similar to other species of snakes
in the Viperidae family:
Bothrops moojeni
N = 50 (68%;
Barrella & Silva, 2003) and
Crotalus durissus terrifcus
Linnaeus, 1758 N = 12 (66%; Dias
et al.,
2004), but
contrasting with
Crotalus tzabcan
Klauber, 1952 N = 50
(14%; Carbajal-Márquez
et al.,
2018). Tese comparative
data support the idea that describing the helminths of a
particular species is crucial to achieve a more complete
comprehension of hidden patterns of parasite biodiversity.
Te phylum Acanthocephala exhibits an indirect
life cycle, engaging in trophic interactions with both
invertebrates and vertebrates (Crompton & Nickol,
1985). Incidentally, snakes act as paratenic hosts for
acanthocephalans (Travassos, 1917; Pizzatto & Madi,
2002; Pizzatto & Marques, 2006; Smales, 2007a; Matias
et al.,
2018). In these cases, encysted larvae reside in
the body cavity of snakes until they are ingested by
the defnitive host (Nickol, 1985). Typically, birds and
mammals serve as defnitive hosts, arthropods act as
intermediate hosts, and snakes serve as paratenic hosts
of the family Oligacanthorhynchidae (Schmidt, 1972;
Nickol & Dunagan, 1989; Kennedy, 2006). Birds and
mammals are potential predators of snakes, (Cardoso
& Santos, 2012; Fraga
et al.,
2013; Marques &
Medeiros, 2018), including those of the genus
Bothrops
(Sazima, 1922; Oliveira & Santori, 1999; Martins
et
al.,
2003), Tus, we suggest that parasites may use
snakes to reach their defnitive hosts. Representatives of
Oligacanthorhynchidae are known to infect snakes such
as
Boa constrictor
Linnaeus, 1758
, Boiga dendrophila
Boie,
1827
, Bothrops jararacussu, Bothrops neuwiedi, Clelia clelia
Daudin, 1803
, Erythrolamprus aesculapii
Linnaeus,1758
E. miliaris
Linnaeus,1758
, E. poecilogyrus
Wied-
Neuwied, 1824
, Macrovipera lebetina obtusa Linnaeus,
1758, Mastigodryas bifossatus
Raddi,1820,
Micrurus
corallinus
Merrem, 1820
, Philodryas olfersii
Lichtenstein,
1823
, P. patagoniensis
Girard, 1858,
Xenodon merremii
Wagler, 1824
,
and
X. histricus
Jan, 1863 (Travassos,
1917; Pizzatto & Madi, 2002; Pizzatto & Marques,
2006; Smales, 2007a; Smales
et al
., 2020).
Besides species of Oligacanthorhynchidae, we also found
Centrorhynchus
sp. in
B. erythromelas
, an acanthocephalan
from family Centrorhynchidae. Te genus
Centrorhynchus
infects birds of the Falconiformes and Strigiformes
orders as defnitive hosts and has invertebrates as
intermediate hosts, with reptiles and amphibians serving
as paratenic hosts (Torres & Puga, 1996). Cystacanths
of
Centrorhynchus
have been recorded in snakes of the
genera
Ahaetulla, Bothrops, Clelia, Chironius, Dipsa,
Echinanthera, Imantodes, Helicops, Leptophis, Liophis,
Mastigodryas, Tropidonotus,
and
Philodryas
(Travassos,
1926; Vizcaíno, 1993; Smales, 2007a; Smales, 2007b;
Lamas & Lunaschi, 2009; Silva & Muller, 2012; Araújo-
Filho
et al.,
2018; Araújo
et al.,
2020; Yudhana
et al.,
2023; Conga
et al.,
2024). In the present study, we only
found cystacanths, suggesting that
B. erythromelas
acts
as paratenic hosts, and the acanthocephalans use them
to reach their defnitive hosts, since Falconiformes and
Strigiformes have already been reported preying on
snakes (Martins
et al.,
2003; Costa
et al.,
2009; Cardoso
& Santos, 2012). Species-level identifcation of the
acanthocephalans was not possible due to the immature
condition of the specimens (cystacanths), which have not
yet developed the reproductive system that is fundamental
for species identifcation.
For Cestoda, we identifed the presence of
Oochoristica
sp.
and Plerocercoid larvae and cysticercoid. Diferent species
of snakes have been recognized as hosts of Cestoda, such
as
Bothrops alternatus, B. jararaca, B. moojeni, Coluber
sp.,
Corallus caninus
Linnaeus, 1758,
Erythrolamprus miliaris,
Micrurus corallinus, Philodryas olfersii, Pseudoboa nigra
Duméril, Bibron & Duméril, 1854
,
and
Tamnophis
sp. (Silva
et al.,
2001; Silva
et al.,
2006; Chambrier
et
al.,
2010; Matias
et al.,
2018; Araújo
et al.,
2020). Te
genus
Oochoristica
has been reported in
Echis carinatus
Schneider, 1801, another Viperidae (Farooq
et al.,
1983).
In
B. erythromelas
, Cestoda were found only in early
developmental stages, making species-level identifcation
impossible.
We were able to identify most of the nematodes only at
the Phylum level (Nematoda, 17 hosts), excepting one
identifcation at the family level (Cosmocercidae gen. sp.,
2 hosts), four at the genus level (
Brevimulticaecum
sp.,
Oswaldocruzia
sp.,
Physocephalus
sp., and
Physaloptera
sp.), due to the immature stage of the parasites, and six at
the species level (
Hexametra boddaertii, Parapharyngodon
hispidus, Physaloptera lutzi, Physaloptera nordestina,
Physalopteroides venancioi,
and
Strongyloides ophidiae
). In
terrestrial snakes, the richness of Nematoda tends to be
higher, as observed in
Crotalus durissus terrifcus
(7 spp.;
Dias
et al.,
2004) and
Crotalus mitchelli
Cope, 1861 (5
spp.; Goldberg
et al.,
2013), and
Pseudoboa nigra
(3 spp.;
Matias
et al.,
2018). Our results corroborate this tendency,
since the nematode fauna in
B. erythromelas
includes at
least 12 nematode taxa, encompassing distinct species
and larval stages. Tese results support previous studies
(Brouat
et al.,
2007), indicating that the dominance of
nematodes in terrestrial snakes may be related to the
habitat of their hosts.
166
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Leite Matias
et al.
Te family Cosmocercidae is frequently reported
infecting species of amphibians and reptiles (Rizvi,
2009; Ávila & Silva
,
2010; Rizvi & Bursey, 2014; Bursey
et al.,
2015; Araújo
et al.,
2020; Draghi
et al.,
2020).
Immature individuals of
Brevimulticaecum
sp. have been
reported in fsh, amphibians, and reptiles (Sprent, 1979;
Moravec & Kaiser, 1994; Moravec
et al.
, 1997; Vieira
et al.,
2010; Silva
et al.,
2018; Souza
et al.,
2020). Te
genus
Oswaldocruzia
is commonly found in amphibians,
although it has also been reported in reptiles, with some
records for snakes (Durette-Desset
et al.,
2006; Goldberg
& Bursey, 2007; Anderson
et al.,
2009; Campião
et al.,
2014; Teles
et al.,
2015; Oliveira
et al.,
2017; Oliveira
et al.,
2019; Flowers & Beane, 2023).
Physocephalus
uses snakes as paratenic hosts, coleopteran insects as
intermediate hosts, and mammals as defnitive hosts
(Ryzhikov, 1952; Kirillov & Kirillova, 2021). Te genus
Physocephalus
has been found in the following North
American species of Viperidae:
Crotalus atrox
Baird &
Girard, 1853
, C. molossus
Baird & Girard, 1853
, C.
Pyrrhus
Cope 1866
, C. scutulatus
Kennicott, 1861
,
and
Sistrurus tergeminus
Say, 1823 (Goldberg
et al.,
2001;
Goldberg
et al.,
2002; McAllister
et al.,
2004; Goldberg
et al.,
2013). Morphologically, it was not possible to
identify
Brevimulticaecum
sp. and
Physocephalus
sp. at
the species level due to the immature developmental
stage of the larvae. Only female specimens were recorded
for Cosmocercidae gen. sp. and
Oswaldocruzia
sp.,
consequently, the identifcation at species level was not
possible because the main morphological characteristics
for Cosmocercidae species identifcation are only present
in males.
Nematodes of the genus
Physaloptera
are common in
birds, amphibians, mammals, and reptiles (Ortlepp,
1922; Chabaud, 1975; Anderson
et al.,
2009; Pereira
et al.,
2012a; Maldonado Jr.
et al.,
2019). Nine species
of
Physaloptera
are known to occur in Brazilian reptiles,
with four reported for snakes:
P. monodens Molin, 1860,
P. liophis Vicente & Santos, 1974, P. obtusissima Molin,
1860
, and
P. nordestina
(Matias
et al.,
2020). Until now,
Physaloptera lutzi
was described only in lizards (Brito
et
al.,
2014; Maia-Carneiro
et al.,
2018), and this is the
frst record of the species occurring in a snake.
Bothrops
erythromelas
is a generalist in terms of diet, feeding mainly
on lizards, frogs, centipedes and mammals (Martins
et al.,
2002; Silva-Soares
et al.,
2022). Given that nematodes
possess a cuticle resistant to stomach acids, we suggest
that these helminths are associated with the ingestion of
the host.
Physaloptera nordestina
was already described
for the following northeastern Brazilian snakes:
Oxybelis
aeneus
Wagler, 1824
, Xenodon merremii
, and
Pseudoboa
nigra
(Matias
et al.,
2020).
Hexametra boddaertii
is a common nematode in
Squamata (Ávila & Silva, 2010; Bursey & Brooks, 2011),
known to infect
Bothrops
sp.,
Crotalus durissus, Oxyrhopus
trigeminus
Duméril, Bibron & Duméril, 1854,
Philodryas
baroni
Berg, 1895,
P. patagoniensis,
and
Pseudoboa nigra
(Skrjabin, 1916; Sprent, 1978; Hartdegen & Gamble,
2002; Pinto
et al.,
2010; Matias
et al.,
2018). Te genus
Parapharyngodon
has a close association with lizards,
mainly of the genus
Tropidurus
, with only one species
described for amphibians (Ávila & Silva, 2010; Anjos
et
al.,
2013; Araújo-Filho
et al.,
2015; Ferreira
et al.,
2021).
Parapharyngodon hispidus
was described in
Tropidurus
hispidus
Spix, 1825 (Ferreira
et al.,
2021), and the present
record is the frst for snakes. Since only one specimen of
B. erythromelas
was found with
P. hispidus,
we suggest that
the infection is accidental, likely due to ingestion during
the snake feeding.
Physalopteroides venancioi
is the only species of the genus
recorded in South America, found mainly in lizards and
amphibians (Ávila & Silva, 2010; Campião
et al.,
2014).
We recorded
P. venancioi
in the small intestine of two
snakes, suggesting that the infection occurred accidentally,
as suggested for the snakes
Platyceps ventromaculatus
Gray
1834,
P. nigra
, and
P. olfersii
(Al-Moussawi, 2016; Matias
et al.,
2018; Araújo
et al.,
2020).
Te genus
Strongyloides
parasitizes birds, mammals,
amphibians, and reptiles (Graham
et al.,
2024). In
response to infection, animals may exhibit diarrhea,
bronchopneumonia, alveolar hemorrhage, interstitial
infammation, altered breathing, enterocyte hyperplasia,
and ulceration or squamous metaplasia of mucosal
epithelium, depending on the worm life stage (Uzal
et al.,
2016; Tamsborg
et al.,
2017; Graham
et al.,
2024). In
reptiles, including snakes,
Strongyloides
infections cause
respiratory difculties and pneumonia (Walden
et al.,
2020; Graham
et al.,
2024). Five species of
Strongyloides
are documented in snakes:
S. gulae
Little, 1966
, S. serpentis
Little, 1966
, S. ophidiae, S. natricis
Navarro & Lluch,
1993, and
S. mirzai
Singh, 1954 (Graham
et al.,
2024).
Strongyloides ophidiae
has been observed in the following
Brazilian snakes:
Crotalus durissus, Erythrolamprus
miliaris, Oxyrhopus guibei
Hoge & Romano, 1977, and
Philodryas olfersii
(Pereira, 1929a; Santos
et al.,
2009; Mati
& Melo, 2014; Mati
et al.,
2015; Araújo
et al.,
2020).
Transmission of
S. ophidiae
occurs through cutaneous or
oral routes, signs of infection are visible after 7 days, and
the species has a direct life cycle (Mati & Melo, 2014).
Tis is the frst record of
S. ophidiae
acting as a parasite of
the species
B. erythromelas.
167
Biodiversity of parasites infecting
Bothrops erythromelas
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Te establishment of parasite populations and
communities can be infuenced by phylogenetic factors
or host characteristics (Poulin, 2004; Kamiya
et al.,
2014a, 2014b). In the present study, the body condition
index (SVL) of the snake
B. erythromelas
was positively
related to the richness and abundance of helminths.
Te host’s body is considered the habitat of the parasite,
such that a larger specimen can provide a greater area for
exploration, colonization, and nutrients to endoparasites
(Aho, 1990). Another relevant factor is that individuals
with greater longevity experience prolonged exposure to
parasitic agents (Aho, 1990; Korallo
et al.,
2007; Pereira
et al.,
2012b). Tis same pattern has been documented
for other reptiles (Brito
et al.,
2014; Araújo-Filho
et al.,
2016; Silva-Neta & Ávila, 2018; Amorim & Ávila, 2019;
Teixeira
et al.,
2018; 2021; Silva
et al.
, 2023).
Of the 30 species of the genus
Bothrops
that occur in
Brazil (Costa
et al.,
2023), 12 (40%) species have been
studied regarding their parasites (Conga
et al.,
2024). Te
most studied species were:
B. jararaca
(10 studies: Pereira,
1929b; Rodrigues, 1968; Santos & Rolas, 1973; Fabio,
1979; Correa
et al.,
1990; Vicente
et al.,
1993; Scherer
et al.,
1996; Grego
et al.,
2004; Silva, 2005; Siqueira
et
al.,
2009),
B. moojeni
(7 studies: Travassos, 1926; Pereira,
1929b; Caubisens Poumarau, 1965; Sprent, 1979; Pinto
et al.,
2012; Müller
et al.,
2021), and
B. neuwiedi
(6
studies) (Travassos & Freitas, 1941; Ruiz & Leão, 1942;
Silva
et al.,
2001; Barrella & Silva 2003; Pinto
et al.,
2012; Morais
et al.,
2017; Müller
et al.,
2021). Tis is
the third study on the helminth fauna of
B. erythromelas.
Our fndings indicate that among all helminth species
found in our analysis, only
Physaloptera sp.
is not a new
record for
B. erythromelas,
while the species
P. lutzi
and
P.
hispidus
are described for the frst time in snakes.
Tus, our results expand the knowledge of parasite
hidden biodiversity, particularly as this study represents
pioneering research on the helminth fauna of
B.
erythromelas,
a venomous snake species endemic to the
Caatinga.
ACKNOWLEDGEMENTS
We thank Conselho Nacional de Desenvolvimento
Científco e Tecnológico (CNPq) for granting a doctoral
scholarship, modality GD to CSLM (#141143/2021-
5). CFS and RWA thank to CNPq (#150125/2023-2;
307722/2021-0) and thank Fundação Cearense de Apoio
ao Desenvolvimento Científco e Tecnológico (FUNCAP
#FC3-0198-00006.01.00/22) for research funding. FGG
is supported by grants from CNPq (312016/2021–2
and 405518/ 2021–8) and from Fundação de Amparo à
Pesquisa do Estado de São Paulo (FAPESP 2022/12660–
4). AAG thanks CNPq for fnancial support through
his productivity research grant (307643/2022-0). Te
research was permitted under license from the Chico
Mendes Institute for Biodiversity Conservation (ICMBio)
SISBIO (#82300-1).
Author contributions: CRediT (Contributor Roles
Taxonomy)
CSLM =
Cicera Silvilene Leite Matias
CFS =
Cristiana Ferreira-Silva
WPS =
Willianilson Pessoa-da-Silva
MBAS =
Maria Beatriz Andrade de Sousa
AFSN =
Aldenir Ferreira Silva-Neta
RWA =
Robson Waldemar Ávila
FGG =
Felipe Gobbi Grazziotin
AAG =
Adrian Antonio Garda
Conceptualization:
CSLM, CFS, FGG, AAG
Data curation:
CSLM, CFS, RWA
Formal Analysis:
CSLM, WPS, MBAS, AFSN
Funding acquisition:
CSLM, FGG, AAG
Investigation:
CSLM, CFS, WPS
Methodology:
CSLM, CFS
Project administration:
CSLM, AAG
Resources:
CSLM, AAG
Software:
CSLM, MBAS, AFSN
Supervision:
AAG
Validation:
CSLM, RWA, FGG, AAG
Visualization:
CSLM, CFS, RWA, FGG, AAG
Writing – original draft:
CSLM
Writing – review & editing:
CSLM, CFS, WPS,
MBAS, AFSN, RWA, FGG, AAG
168
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Leite Matias
et al.
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