image/svg+xml
ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
ECOLOGICAL ASPECTS OF THE INVADING TREMATODE
CENTROCESTUS FORMOSANUS
(NISHIGORI, 1924) (TREMATODA: HETEROPHYIDAE) IN THE NILE TILAPIA
OREOCHROMIS
NILOTICUS
(LINNAEUS, 1758) (PERCIFORMES, CICHLIDAE), IN THE WETLAND LOS
PANTANOS DE VILLA, LIMA, PERU
ASPECTOS ECOLÓGICOS DEL TREMÁTODO INVASOR
CENTROCESTUS FORMOSANUS
(NISHIGORI, 1924) (TREMATODA: HETEROPHYIDAE) EN LA TILAPIA DEL NILO
OREOCHROMIS NILOTICUS
(LINNAEUS, 1758) (PERCIFORMES: CICHLIDAE), EN EL HUMEDAL
LOS PANTANOS DE VILLA, LIMA, PERÚ
1
Laboratorio de Ecología y Biodiversidad Animal (LEBA). Facultad de Ciencias Naturales y Matemática (FCNM).
Grupo de Investigación en Sostenibilidad Ambiental (GISA). Escuela Universitaria de Posgrado (EUPG). Universidad
Nacional Federico Villarreal (UNFV). El Agustino, Lima, Perú.
2*
Laboratorio de Parasitología. Facultad de Ciencias Biológicas (FCB). Universidad Ricardo Palma (URP). Santiago de
Surco, Lima, Perú.
3
Laboratorio de Ingeniería Ambiental. Carrera de Ingeniería Ambiental. Coastal Ecosystems of Peru Research Group
(COEPERU). Universidad Científica del Sur, Villa el Salvador, Lima, Perú.
4
Laboratório de Sanidade de Organismos Aquáticos AQUOS, Departamento de Aquicultura, Universidade Federal de
Santa Catarina UFSC, Florianópolis, SC, Brasil.
*Corresponding author: joseiannaconeoliver@gmail.com
David Minaya: https://orcid.org/
0000-0002-9085-5357
José Iannacone: https
://
orcid.org/0000-0003-3699-4732
Lorena Alvariño: https://orcid.org/
0000-0003-1544-511X
Carla Cepeda:
https://orcid.org/0000-0001-7723-7477
Mauricio Laterça Martins:
https://orcid.org/
0000-0002-0862-6927
11,2*113
David Minaya; José Iannacone; Lorena Alvariño; Carla Cepeda & Mauricio Laterça Martins
Neotropical Helminthology
57
doi:10.24039/rnh20211511044
Neotropical Helminthology, 2021, 15(1), ene-jun:57-65.
D
D
D
ABSTRACT
Keywords
:
Centrocestus
– fish parasites –
Oreochromis niloticus
– parasite ecology – Peru
Nile tilapia
Oreochromis niloticus
(Linnaeus, 1758) is a freshwater fish native to Africa. The present
work's objective was to evaluate some ecological aspects of the invading metacercaria of
Centrocestus
formosanus
(Nishigori, 1924) (Trematoda: Heterophyidae) in
O. niloticus
in the wetlands of Pantanos de
Villa, Lima, Peru. Twenty specimens of
O. niloticus
collected in the Genesis, and Marvilla lagoons in
Pantanos de Villa's wetlands were inspected parasitologically during February and October of 2012. The
fish had an average weight and length of 221.3 g ± 111.4 and 19.6 cm ± 4.24 cm, respectively. The invasive
ectoparasite metacercariae were cataloged and evaluated using standard parasitological protocols. During
the entire sampling, a total of 130
C. formosanus
trematodes was collected, with an average abundance of
sixty percent of the Nile tilapias parasitized by
C. formosanus.
The relative condition factor (k), an
n
indicator of host fish health, was not influenced by the presence of
C. formosanus
.
Centrocestus
D
D
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58
RESUMEN
Palabras clave
:
Centrocestus
– ecología de parásitos –
Oreochromis niloticus
– parásitos de peces – Perú
La tilapia del Nilo
Oreochromis niloticus
(Linnaeus, 1758) es un pez de agua dulce endémico originario de
África. El objetivo del presente trabajo fue evaluar algunos aspectos ecológicos del tremátodo invasor
Centrocestus formosanus
(Nishigori, 1924) (Trematoda: Heterophyidae) en
O. niloticus
en los humedales
de Pantanos de Villa, Lima, Perú. Durante febrero y octubre de 2012 se inspeccionaron
parasitológicamente 20 ejemplares de
O. niloticus
recolectados en las lagunas Génesis y Marvilla en los
humedales de Pantanos de Villa, Lima, Perú. Los peces tuvieron un peso y longitud promedio de 221.3 g ±
111.4 y 19.6 cm ± 4.24 cm, respectivamente. Las metacercarias de ectoparásitos invasores fueron
catalogadas y evaluadas utilizando protocolos parasitológicos estándares. Durante todo el muestreo, se
recolectaron un total de 130 trematodos de
C. formosanus
, con una prevalencia promedio del 60% de las
tilapias del Nilo parasitadas por
C. formosanus
. El factor de condición relativo (k), un indicador de la
n
salud de los peces huéspedes, no fue influenciado por la presencia de
C. formosanus
.
Centrocestus
formosanus
se ha registrado en aves y mamíferos, incluidos los humanos, que producen heterofiosis, una
enfermedad emergente mundial en humanos transmitida por el consumo de pescado crudo.
Centrocestus
formosanus
en Perú representa un potencial impacto zoonótico en la salud pública. En adición, se registró
en branquias en un solo huésped, la presencia del ectoparásito dinozoario
Amyloodinium ocellatum
Brown & Hovasse, 1946, que puede causar alteraciones patológicas en peces marinos y ambientes salinos.
The gray tilapia
Oreochromis niloticus
(Linnaeus,
1758) (Perciformes: Cichlidae) is an endemic
freshwater fish native to Africa and the Near East; it
is a species widely distributed worldwide for
cultivation due to its relative ease of adaptation and
easy management in production in aquatic crops
(FAO, 2016; Abd El-Naby
et al
., 2019). In Peru,
starting in the 70s, this species' introduction and
cultivation began for research and commercial
cultivation purposes (Ramos & Gálvez, 2000;
Baltazar, 2007). The introduction of this species
began from Brazil in 1978 until it became an
invasive species, displacing species such as native
fish from the lower area of the Rio Grande, on the
coast of Ica, Peru (Ortega
et al
., 2007). It is
currently considered a naturalized species in
INTRODUCTION
Amazonas and Arequipa environments, to name a
few (Ortega
et al
., 2007; Cossíos, 2010).
In Peru, the nile tilapia, O. niloticus, have been
registered few jobs in relation to their
parasitofauna and other pathogens. (Amin
et al
.,
2010; Gonzales-Fernández, 2012; Chiclla-Salazar
& Tantas-García, 2015; Luque
et al
., 2016; Ortega
et al
., 2017).
Among the known adverse effects of introducing
exotic or alien species is introducing diseases
through pathogens and parasites (Davis, 2009).
One of the species mentioned as introduced alien
parasites is the trematode
Centrocestus
formosanus
(Nishigori, 1924) (Trematoda:
Heterophyidae), which has among its exotic
paratenic hosts
O. niloticus
and among its strange
intermediate hosts
Melanoides tuberculata
(OF
Neotropical Helminthology, 2021, 15(1), ene-jun
Keywords
:
Centrocestus
– fish parasites –
Oreochromis niloticus
– parasite ecology – Peru
formosanus
has been recorded in birds and mammals, including humans producing heterophils, a
worldwide emerging disease in humans transmitted by raw fish consumption.
Centrocestus formosanus
in
Peru has a potential zoonotic impact on public health. In addition, the presence of the dynozoan
ectoparasite
Amyloodinium ocellatum
Brown & Hovasse, 1946, can cause pathological alterations in
marine fish and saline environments found in gills in a single host.
Minaya
et al.
image/svg+xml
59
Müller, 1774) (Ximenes
et al
., 2017). It is found in
the form of metacercaria in the gills of freshwater
fish. It is of aquaculture sanitary importance due to
the damage it can cause to the gill filaments, which
can end up being destroyed, thus reducing the
surface area of the respiratory epithelial tissue
(Sumuduni
et al
., 2018; Leibowitz
et al
., 2019;
Pace
et al
., 2020). This trematode has caused the
death of high populations of fish in hatcheries,
causing severe economic losses and the death of
wild fish and becoming a threat to those in danger
of extinction (Mitchell
et al
., 2005).
Other risk factors that make
C. formosanus
a vital
species is its zoonotic capacity because it can cause
heterophiosis, an emerging global disease in
humans transmitted by the consumption of raw
fish, which in some cases can cause significant
heart disease, brain and spinal cord, being often
fatal in these organs (Lima dos Santos & Howgate,
2011). Despite infecting humans, it is only
considered an accidental host of
C. formosanus
since birds and wild mammals associated with
freshwater bodies are those that play the role of
definitive hosts (Pinto & Melo, 2012; Leibowitz
et
al
., 2019).
One of the ideal settings for the establishment and
development of the biological cycle of
C.
formosanus
is the Pantanos de Villa wildlife refuge
in Lima, Peru, since part of the fauna of this
wetland harbors
M. tuberculata
(Torres-Zevallos
et
al
., 2020) and
O. niloticus
, both documented hosts
of the immature forms (redia, cercaria and
metacercaria), and species of wild piscivorous
birds, both migratory and resident (Iannacone
et
al
., 2010) available as definitive hosts for
C.
formosanus
.
Due to the above, this work aims to evaluate the
ecological aspects of the invasive trematode
C.
formosanus
in the Nile tilapia
O. niloticus
, in the
wetlands of Pantanos de Villa, Lima, Peru.
Collection of material and processing of
samples
Twenty specimens of
O. niloticus
were necropsied
MATERIALS AND METHODS
between February and October 2012 at the Los
Pantanos de Villa Wildlife Refuge, Lima, Peru (12
° 12′49 ″ S; 76 ° 59′20 ″ W) to study its community
of metazoan parasites (Eiras
et al
., 2006). Ten
specimens were obtained from Génesis lagoon in
February-2012 and ten from Marvilla lagoon in
October-2012. The fish were collected using
gillnets with 25 mm internode meshes. The nets
were placed randomly and crosswise in each
lagoon for ten hours, and were checked every 60
min and then relocated to the site (UNMSM -
MINAM, 2014). The average physical-chemical
characteristics of both lagoons of the wetlands of
Villa, Lima, Peru evaluated
in situ
were:
temperature of 25 ± 5.2 ° C, pH of 8.42 ± 0.03,
-
Electrical conductivity (EC) of 5.67 ± 0.61 mS·cm
1
, surface dissolved oxygen (DO) of 3.19 ± 1.58
-1
mg·L, background dissolved oxygen (DO) of 1.88
-1
± 1.66 mg·L, using a multiparametric HANNA@
(HI98130, Solitec, Lima, Peru) and likewise, the
transparency of the water was 37.91 ± 17.37 cm,
which was evaluated using the Secchi disk.
Fish
were anesthetised in a benzocaine solution (50
–1
mg·L) and a two mL blood sample was taken from
the caudal vein using a syringe containing a drop of
10% EDTA solution (Jerônimo
et al
., 2011).
Two
hematological parameters were evaluated:
hematocrit (Ht) and total red cell count (RBC). Ht
(%) determinations were made by the
6-1
microhematocrit method and the RBC (x 10·uL)
was carried out in a Neubauer chamber (Blaxhall &
Daisley, 1973). We measured total weight (0.1 g
sensitivity) and full length (TL) (0.1 cm
sensitivity). All fish underwent a systematic
external and internal examination of tissues,
including skin, fins, gills, eyes (lens and vitreous
humor), body cavity, mesentery, and visceral
organs (stomach, intestine, liver, swim bladder,
heart, and gonads). The recovered parasites were
fixed and preserved using commonly applied
methods (Özer
et al
., 2016).
Sample analysis
The ecological approach of the metazoan parasite
community was made at the component and
intracommunity levels (Esch
et al
., 1990). For the
case of parasitic species with prevalences higher
than 10% (Esch
et al
., 1990), the dispersion indices
(DI) were used to determine the type of spatial
distribution of the parasitic populations, the Poulin
discrepancy (PDI), and the K of the negative
binomial equation with its respective Chi-square
Neotropical Helminthology, 2021, 15(1), ene-jun
Invading Trematode
Centrocestus formosanus
image/svg+xml
60
2
value (X) to determine the degree of aggregation
(Bego & Von-Zuben, 2010). The calculations were
performed using the statistical package
Quantitative Parasitology 3.0 (Rózsa
et al
., 2000;
Reiczigel
et al
., 2019).
Relative condition factor (K)
n
The theoretically expected weight for a given
length was calculated using the estimated weight
(W) -total length (LT) ratio curve. Then, the
relative condition factor was obtained by the
relationship between the observed weight (W) and
the expected weight (We) as shown below: K =
n
W/We. In this way, K's mean values for fish
n
infected by a particular parasite alone were
calculated (Özer
et al
., 2016).
A student's t-test was
performed to compare k deals between parasitized
n
and non-parasitized and between the two lagoons
evaluated, after analysis of the Levene test for the
homogeneity of the variances Shapiro-Wilk test for
normality (Zar, 2014).
Pearson's correlation coefficient (r) was used to
p
indicate the relationship between the host's total
length and the abundance of parasites. The
Spearman rank correlation coefficient (r) was
s
calculated to determine a possible correlation
between the host's full size and the parasite's
RESULTS
prevalence, with the anterior arcsine
transformation of the prevalence data (Zar, 2014;
Bautista-Hernández
et al
., 2013). The ecological
terminology used follows Bush
et al
. (1997). The
level of statistical significance was evaluated at p ≤
0.05. The SPSS version 25.0 statistical package
was used for all descriptive and inferential
statistics calculations.
Ethic aspects:
The authors indicate that all the
ethical requirements of the country and
international were met.
The fish had an average length of 19.6 cm ± 4.24
(13 cm - 30.6 cm) and a weight of 221.3 g ± 111.4
(99 g - 486.5 g). Two parasites were found:
C.
formosanus
(Trematoda) and
Amyloodinium
ocellatum
(Alveolata). It was observed that 60% of
the total population of
O. niloticus
were parasitized
by the metacercariae of
C. formosanus
in the
branchial area. Likewise, this parasite records an
aggregate type distribution according to the
dispersion indices according to the variance/mean
Descriptors
Total
G
é
nesis
lagoon
Marvilla l
agoon
Parasitized fish
12
4
8
Prevalence
(P) %
60
40
80
Medium abundance
(
M
A
)
6.5
± 1.
74
4.5
±
2.81
8.5
±
1.99
Medium intensity
(M
I
)
10
.
83
±
2.24
11.25
±
4.44
10.63
±
2.23
type of strategy
Core
Sec
o
ndary
Core
Variance / mean ratio
(
D
I
)
9.27
17.49
4.66
Poulin's discrepancy
Index
(
P
DI
)
0.5
8
0.72
0.35
Negative binomial exponent
k
NA
0.15
NA
Total length
(
T
L
)
(
cm)
19.9
±
4
.24
22.
9
±
5.18
18.6
±
5.18
Weight
(W)
(g)
247.8
±
111.39
264
±
133.56
226.7
±
133.56
K
n
1.12
±
1
1.23
±
1
1
±
1
Student's t between k
n
between
lagoons
t = 2.12, p=0.06
K
n
for parasitized and non
-
parasitized
K
n
parasitized
0.86 ± 0.36
K
n
not parasitized
1.07 ± 0.26
Student's t between parasitized
k
n
and non
-
parasitized k
n
t = 1.48, p=0.15
Table 1.
Ecological descriptors of
Centrocestus formosanus
parasites of the Nile tilapia
Oreochromis niloticus
collected in Pantanos de Villa, Lima, Peru.
K = Relative condition factor. NA = cannot calculate maximum likelihood estimate of k.
n
Neotropical Helminthology, 2021, 15(1), ene-jun
Minaya
et al.
image/svg+xml
61
relationship (DI = 9.27) and Poulin's discrepancy
Index (PDI = 0.58). Compared to the two lagoons,
it is observed that in the Marvilla lagoon, the P and
AM are higher than in Genesis lagoon, except for
the MI, where the opposite occurs. In the type of
distribution of
C. formosanus
, for the two
environments, they are classified as aggregate or
contagious (Table 1).
According to the Relative Condition Factor (K),
n
the fish parasitized by
C. formosanus
did not show
the loss or low levels of weight about the total
population of fish (infected and not infected); on
the contrary, the factor was above 1 (K = 1.12 ± 1)
n
indicating a satisfactory health condition
concerning weight (Table 1).
No significant
differences were observed in kn between lagoons
and between parasitized and non-parasitized
(Table 1).
The degree of association between the
morphological parameters of
O. niloticus
(TL and
W) was sought about the ecological descriptors of
C. formosanus
(prevalence, mean abundance and
mean intensity of infection), were an only
significant association of TL with relation to the
mean abundance (Table 2).
Table 2
. Correlation between the total length (TL) and weight (W) of
Oreochromis niloticus
and the prevalence,
abundance, and mean intensity of infection of
Centrocestus formosanus
in the Pantanos de Villa wildlife refuge,
Lima, Peru.
r
p
T
L
vs
P%
*0.11
1.00
T
L
vs
M
A
**0.96
0.04
T
L
vs
M
I
**0.81
0.19
W
vs
P%
*0.60
0.23
W
vs
M
A
**0.82
0.09
W
vs
M
I
**0.15
0.81
TL = Total length, P% = Prevalence, MA = mean abundance, MI = mean intensity,
W = Weight. r = Correlation coefficient, * Spearman, ** Pearson p = significance.
About
A. ocellatum
, this dinoflagellate was found
only in one individual parasitizing a single host of
Nile tilapia in the gills (5% prevalence) from the
Genesis Lagoon. This parasite was found in the
trophont stage of development, and an MA and MI
of 0.05 and 1, respectively, were observed. Due to
the low prevalence, this species was considered
rare.
Table 3 shows the physical-chemical parameters
(temperature, pH, dissolved oxygen, and water
transparency) of the two lagoons (Génesis and
Marvilla) that make up the Pantanos de Villa
wildlife refuge Lima, Peru.
Table 3.
The Génesis and Marvilla lagoons' physical-chemical parameters make up the Pantanos de Villa wildlife
refuge, Lima, Peru.
Physico
-
chemical parameters
Génesis
lagoon
Marvilla
lagoon
Temperature
(°C)
29
21.6
pH
8.4
8.4
Electric Conductivity
(
µS
·
cm
-
1
)
6.1
5.2
D
O
(mg
·
L
-
1
) (
surface
)
4.31
2.1
D
O
(
mg
·
L
-
1
) (
bottom
)
3.05
0.7
B
O
D
(
mg
·
L
-
1
)
(
surface
)
1.26
9.6
Transparency
(Secchi)
(
cm
)
50.40
25.4
Two hematological parameters in Nile tilapia,
hematocrit (Ht) and total red cell count (RBC)
presented mean values of 30.04 ± 5.41 % and 3.83
6-1
± 0.47 (x 10·uL), respectively.
Neotropical Helminthology, 2021, 15(1), ene-jun
Invading Trematode
Centrocestus formosanus
image/svg+xml
62
The parasite community in the Nile tilapia was
limited to one metazoan parasite species, the
metacercariae of the trematode
C. formosanus
as
the dominant species. Similar studies have also
addressed the registration of ecological
descriptors, as in Aguilar–Aguilar
et al
. (2009),
where they found prevalence values of 100% and a
mean abundance of 182.2, in
Cyprinella lutrensis
(Baird & Girard, 1853). On the contrary, Pinto
et al.
(2014) mentions low values of P = 31.9% (19/61),
AM = 1.03 and IM = 3.42 in
O. niloticus
.
Fish age, behavior, and resistance to parasitism are
factors that can influence the prevalence and
intensity of trematode infection in Nile tilapia
(Pinto
et al
., 2014). On the other hand, different
authors from other countries (Kalantan
et al
., 1999;
Ramadan
et al
., 2002; Chi
et al
., 2008) also
recorded low intensities of infection by
C.
formosanus
in
O. niloticus
. Pinto
et al
. (2014)
suggest that the Nile tilapia has a relative resistance
to the parasitosis of
C. formosanus
. They even offer
that resistance to parasites is one reason why tilapia
is chosen as a fish for culture; however, this study
shows the high susceptibility to this trematode.
These differences can be influenced by
environmental aspects (temperature, humidity,
luminosity) that each locality presents (Lo & Lee,
1996).
The type of distribution was classified as
aggregated in the three indices, which is expected
in populations of parasites with prevalence above
10% because aggregation is the predominant
pattern in all-natural systems of parasites- host
(Bego & Von-Zuben, 2010). In the case of the
negative K index, it has not been possible to
estimate the degree and type of aggregation for the
total populations and the population of Laguna
Marvilla; probably the reason could be (among
others) that there is very little data or that are not
aggregated at all (Reiczigel
et al
., 2019).
The association of the morphological parameters
of
O. niloticus
and the parasitological indices did
not show any degree of association except in the TL
and the mean abundance of
C. formosanus,
which
showed a significant positive association. Poulin
(2011) suggests that larger body size hosts can
DISCUSSION
deliver a greater supply of nutrients to parasites
and, consequently, be the most susceptible to
increased parasite infection.
Negative effects caused by pathogenic parasites
can be expected on their hosts; however, it is
difficult to define or quantify whether these effects
directly caused any alteration in the health of the
fish, this measure has been applied to individuals
and, although in limited quantities, to varieties of
parasites co-infecting their hosts (Özer
et al
.,
2016). Health status based on the relative condition
factor of
O. niloticus
was not affected by the
individual presence of
C. formosanus
. Ht and RBC
were within the expected range for Nile tilapia
(Hah-Von-Hessberg
et al
., 2011; Jerônimo
et al.,
2011).
Previously,
Centrocestus
sp. in the Green Terror
Andinoacara rivulatus
(Günther, 1860), and in the
Swordtail
Xiphophorus hellerii
(Heckel, 1848),
both reported in the department of La Libertad,
Perú (Luque
et al
., 2016). These are the only
records that exist of the genus
Centrocestus,
so that
this study would be the first report of the species
C.
formosanus
for the Pantanos de Villa life refuge for
Lima's department and Peru.
It should also be considered that this trematode can
not only cause pathologies in fish or their definitive
hosts, birds and aquatic mammals (Pinto & Melo,
2012; Leibowitz
et al
., 2019), but is also
responsible for zoonotic diseases, being able to
produce in the human heterophiosis, which is
emergent and transmitted to man due to the
consumption of raw fish. This disease can be fatal
in cases where it significantly affects the heart,
spinal cord or brain (Lima dos Santos & Howgate,
2011).
In aquaculture,
A. ocellatum
has also been
considered an important pathogen of marine and
freshwater fish because it causes (amyloodyniosis)
can be devastating and deadly in crowded and
closed systems (Francis-Floyd & Floyd, 2011), as
is the free-living refuge Pantanos de Villa. It is also
known that the host range for this ectoparasitic
dinoflagellate is quite wide, even reaching a group
of teleost and elasmobranch fish (Alvarez-
Pellitero, 2008). This generalist ability of the
parasite can endanger the other fish species that
accompany
O. niloticus
in Pantanos de Villa, such
Neotropical Helminthology, 2021, 15(1), ene-jun
Minaya
et al.
image/svg+xml
63
as the White Liza
Mugil curema
Valenciennes,
1836, which is also present in the same
environment.
The extremely low prevalence of
A. oncellatum
could be because the parasite is still beginning to
adapt to this environment and subsequently
colonize fish populations. Therefore, it is essential
to keep monitoring and reviewing possible
intermediate hosts shortly. To ensure the health of
the fish and its ecosystem of the swamps, since the
loss of water resources such as fish could lead to
imbalances in this environment's trophic chain and
the organism's dependent on them.
Amin, O, Heckmann, RA, Peña, C & Castro, T.
2010.
On the larval stages of
Polymorphus
spindlatus
(Acanthocephala:
Polymorphidae) from a new fish host,
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Neotropical Helminthology, 2021, 15(1), ene-jun
Invading Trematode
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