image/svg+xml
ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2022, 16(1), ene-jun:-56.
49
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1
Instituto de Investigaciones de la Amazonía Peruana (IIAP). Laboratorio de Parasitologia y Sanidad Acuícola. Carretera
Iquitos-Nauta Km 4.5, Iquitos, Loreto-Peru.
2
Amazon Research Center for Ornamental Fishes - ARCOF, Asentamiento Humano 31 de mayo, Mz. 22 Lt. 2, Iquitos,
Loreto, Perú.
*Corresponding author: germantiss1106@gmail.com
Germán Augusto Murrieta-Morey: https://orcid.org/0000-0001-6244-2654
Carlos Alfredo Tuesta-Rojas: https://orcid.org/0000-0002-1961-3574
Angela María Echevarria-Matos: https://orcid.org/0000-0003-0296-0921
Carlos Tobías Chuquipiondo-Guardia: https://orcid.org/0000-0002-7979-2025
1*1
Germán Augusto Murrieta-Morey; Carlos Alfredo Tuesta-Rojas;
22
Angela María Echevarria-Matos & Carlos Tobías Chuquipiondo-Guardia
ABSTRACT
Key words:
Aquaculture – cichlids –
Clinostomum
– ornamental fish – piscivorous bird
The ornamental fish trade is one of the most important economic activities for thousands of people in the
Amazon region. Among fish that are exported from Peru,
Apistogramma
sp.,
Cichlasoma amazonarum
(Kullander, 1983) and
Pterophyllum scalare
(Schultze, 1823) are highly demanded in the ornamental fish
trade activities. To date, in Peru, studies concerning parasites that affect aquaculture activities are scarce.
The present study is first to report the occurrence of
Clinostomum
sp. parasitizing three species of cichlids
in the Peruvian Amazonia. Samples of
Apistogramma
sp.,
C. amazonarum
and
P. scalare
were collected in
a fish farming pond of the “Amazon Research Center for Ornamental Fishes (ARCOF) in Iquitos, Peru.
Analyzed samples revealed the presence of
Clinostomum
sp. parasitizing the fins of the fish. As some
species of cichlids are cultivated in the Peruvian Amazon for exportation as ornamental fish, the presence
of this trematode
could compromise the health and appearance of the fish and may cause mortalities,
either, due to susceptibility to predation by piscivorous birds or due to injuries caused by the infection of
parasites.
Neotropical Helminthology
49
doi:10.24039/rnh20221611381
METACERCARIAE OF
CLINOSTOMUM
SP.
(TREMATODA: CLINOSTOMIDAE) INFESTING
ORNAMENTAL CICHLIDS CULTIVATED IN THE PERUVIAN AMAZONIA
METACERCARIA DE
CLINOSTOMUM
SP. (TREMATODA: CLINOSTOMIDAE) INFESTANDO A
CÍCLIDOS CULTIVADOS ORNAMENTALES EN LA AMAZONÍA PERUANA
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 Afines (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.
D
D
D
D
image/svg+xml
The ornamental fish trade is one of the most
important economic activities for thousands of
people in the Amazon region (Moreau & Coomes,
2007). Nearly all Amazon fish exported from the
natural environment are obtained by local
fishermen, who transfer the fish to agents who,
later on, transfer them to exporters so as to reach
fish stores worldwide. It has been estimated that in
this transport chain, 73% of the fish die, due to
several causes (Olivier, 2001).
Cichlids are one of the major ornamental fish
families, due to the large number of species and the
demand for these fish for ornamental purposes.
This demand is explained by the variety of shapes,
extravagant colors and special behavior of the
different species that are included in this family
(Kullander & Silfvergrip, 1991; Garcia-Dávila
et
al
., 2021). According to Garcia-Dávila
et al.
(2021), in the Peruvian Amazonia, 37 species of
cichlids are commercialized as ornamental fish.
Between these species,
Apistogramma
sp.,
Cichlasoma amazonarum
(Kullander, 1983) and
Pterophyllum scalare
(Schultze, 1823)
are highly
demanded for ornamental fish importers.
In the region of Loreto, Peru, most of the cichlids
used in the ornamental trade are captured from
natural environments while others are breed under
captivity in artificial ponds (Garcia
et al.,
2021).
El comercio de peces ornamentales es una de las actividades económicas más importantes para miles de
personas en la región amazónica. Entre los peces que se exportan desde Perú,
Apistogramma
sp.,
Cichlasoma
amazonarum
(Kullander, 1983) y
Pterophyllum
scalare
(Schultze, 1823) son muy
demandados en las actividades comerciales de peces ornamentales. A la fecha, en el Perú, los estudios
referentes a los parásitos que afectan las actividades acuícolas son escasos, es así que el presente estudio
registra por primera vez en la Amazonía peruana la ocurrencia de
Clinostomum
sp. parasitando tres
especies de cíclidos. Se recolectaron muestras de
Apistogramma
sp.,
C
.
amazonarum
y
P
.
scalare
en un
estanque de piscicultura del “Centro de Investigación de Peces Ornamentales de la Amazonía (ARCOF)
en Iquitos, Perú. Las muestras analizadas revelaron la presencia de
Clinostomum
sp. parasitando las aletas
de los peces. Como algunas especies de cíclidos se cultivan en la Amazonía peruana para su exportación
como peces ornamentales, la presencia de este trematodo podría comprometer la salud de los peces y
causar mortalidades, ya sea por susceptibilidad a la depredación por aves piscívoras o por lesiones
causadas por la infección de parásitos.
50
Neotropical Helminthology, 2022, 16(1), ene-jun
INTRODUCTION
Parasites are abundant in tropical climates, and are
one of the major causes of death and disposal of
ornamental fish, thus representing large economic
losses. Because of the small size of these fish, they
are easily affected by small numbers of parasites
(Takemoto
et al
., 2004).
Metacercariae of
Clinostomum
spp.
have the
ability to infect muscles, fins and internal organs of
fish. This parasite is usually found on the host body
wall below the integumentary tissue, causing
characteristic nodular swelling that can be easily
recognize during physical examination (Simsek
et
al
., 2018). In the life cycle of these parasites, the
first intermediate hosts are species of freshwater
snails which have been infected from eggs
deposited in the water by definitive host fish-eating
birds (Liao, 1993). Fish species act as second
intermediate hosts, manifesting the pathology
known as “yellow-grub disease” (Ramos-Alves
et
al
., 2001).
Thus, the present study registers for the first time in
the Peruvian Amazonia the occurrence of
Clinostomum
sp. parasitizing ornamental cichlids
collected from an artificial fish pond.
In a fish farming pond of the “Amazon Research
Center for Ornamental Fishes (ARCOF) in Iquitos,
RESUMEN
Palabras claves:
Acuicultura – Ave piscívora – cíclidos –
Clinostomum
–
Pez ornamental
Murrieta-Morey
et al.
MATERIAL AND METHODS
image/svg+xml
OO
Peru (03 46.433' S, 073 15.688'W), specimens of
“Apistograma tapiche” dwarf cichlid
Apistogramma
sp. with 4.30 ± 0.88 cm standard
length and 3.50 ± 0.68 g of total weight; “bujurqui”
Amazon cichlid
C. amazonarum
with 4.28 ± 0.84
cm standard length and 3.60 ± 1.03 g of total weight
and “pez ángel” wild Angelfish
P. scalare
with 7.20
± 0.57 cm standard length and 5.80 ± 0.83 g of total
weight (were observed with signs of erratic
swimming: fish swam very close to the surface,
showing difficulty in their movement). Specimens
were collected and placed in plastic bags with
water and oxygen for transportation to the
“Laboratorio de Parasitología y Sanidad Acuícola”
of the “Instituto de Investigaciones de la Amazonía
Peruana” (IIAP), Loreto, Peru.
The surface of the body and fins were analyzed by
using a stereomicroscope. Parasites observed in the
fins were collected with dissecting needles and
placed in Petri dishes for counting the number of
individuals collected per infested fish. For fixation
of the parasites, alcohol-formalin-acetic acid
(AFA) was used for 24 h and then conserved in 70%
ethanol. For taxonomic identification, it was
necessary to stain the parasites with Langeron's
alcoholic Carmin. Finally, stained parasites were
observed under stereoscope and microscope.
Parasitological indices (Prevalence, mean intensity
and mean abundance) followed Bush
et al.
(1997).
Parasites were deposited in the parasitological
collection of the “Laboratorio de Parasitología y
Sanidad Acuícola” from IIAP.
Ethical disclosures
This study was developed in accordance with the
principles adopted by IIAP, and authorization from
Ethics Committee of the IIAP was carried out.
51
Neotropical Helminthology, 2022, 16(1), ene-jun
Analyzed fish revealed the presence of
metacercariae of
Clinostomum
sp. (Figs. 1 and 2)
on the fins of infested fish species. The main
characteristics observed in the parasites were:
Body linguiform with slight strangulation at the
level of ventral sucker. Oral sucker located in the
center of a circular dilation of the body. Pharynx
present with bifurcation of the intestinal cecum
extending to the posterior extremity of the body.
Large intestinal cecum with irregular contour; pre-
equatorial acetabulum; testes located between the
end of the second third and the upper region of the
last third of the body, anterior and posterior testis
with lobular triangular shape. Intratesticular and
post-equatorial ovary. Intercaecal, pre-testicular
and post-acetabular uterus. Vitelline consisting of
small, post-acetabular, intra and extracaecal
follicles.
According to site of infestation, for
Apistogramma
sp., 47% of the metacercariae were found on the
dorsal fin; 39% in the anal fin; 10% on the caudal
fin; 02% on the ventral fin and 02% on the pectoral
fin. For
C. amazonarum
, 82% of the parasites were
found on the dorsal fin; 11% on the pectoral fin;
05% on the caudal fin and 02% on the ventral fin.
For
P. scalare
, 55% of the parasites were found on
the dorsal fin; 20% on the caudal fin; 18% on the
ventral fin and 07% on the pectoral fin (Fig. 3).
Parasitological indices of
Clinostomum
sp.
reported in the three-host species are showed in
Table 1.
RESULTS
Table 1
. Parasitological indices of
Clinostomum
sp.
reported in three species of cichlids. AF = analyzed fish, PF =
parasitized fish, P% = prevalence, N = number of
C. marginatum
recorded in each host species, mI = mean intensity
of infestation, mA = mean abundance of infestation.
Species of fichlids
AF
PF
P%
N
mI
mA
Apistogramma
sp.
20
16
80
222
13.87
± 2.4
11.1
± 1.8
Cichlasoma amazonarum
33
19
57.57
55
2.89
± 0.62
1.66
± 0.44
Pterophyllum scalare
5
4
80
44
8.8
± 1.9
11
± 2.5
Infestation of
Clinostomum
sp.
image/svg+xml
Infections of
Clinostomum
spp.
have been reported
in different fish species. In Brazil:
Semaprochilodus insignis
(Jardine, 1841);
Cichla
ocellaris
Bloch & Schneider, 1801
; Crenicichla
sp
.
(Castelo, 1984; Thatcher, 1991);
Hoplosternum
littorale
(Hancock, 1828)
(Sao Clemente
et al
.,
1998);
P. scalare
(Ramos-Alves
et al
., 2001)
;
Synbranchus marmoratus
Bloch, 1795
(Isaac
et al
.,
2004);
Geophagus brasiliensis
(Quoy & Gaimard,
1824) (Paraguassú
et al.,
2005);
Pygocentrus
nattereri
Kner, 1858 (Morais
et al
., 2011);
Colossoma macropomum
(Cuvier, 1816)
(Murrieta-Morey & Malta, 2016);
52
DISCUSSION
Neotropical Helminthology, 2022, 16(1), ene-jun
Pterygoplichthys pardalis
(Castelnau, 1855) (De
Souza
et al
., 2020a);
Gymnotus coropinae
Hoedeman, 1962,
Gymnorhamphycthys petiti
Géry
& Vu, 1964,
Brachyhypopomus brevirostris
(Steindachner 1868) and
Microsternarchus
bilineatus
Fernández-Yépez, 1968 (De Souza
et
al.,
2020b). In the present study,
Apistogramma
sp.,
C. amazonarum
and
P. scalare
are cited for the first
time as hosts of
Clinostomum
sp. metacercariae
and therefore, we constitute the first study in the
Peruvian Amazon related to infestations of
trematodes in fish species cultivated.
The fact that the dorsal and anal fins were the most
common locations of the parasites is probably due
to low movements of those fins, therefore
Figure 1.
Metacercariae of
Clinostomum
sp. A. Ventral view showing the complete body. B. Anterior part of the body. C.
Posterior part of the body. os = oral sucker, f = pharynx, ic = intestinal caecum, a = acetabulum, u = uterus, at = anterior testes, o =
ovary, pt = posterior testes. Scale bar: A = 2 mm, B, C = 300 µm.
Murrieta-Morey
et al.
image/svg+xml
53
Neotropical Helminthology, 2022, 16(1), ene-jun
Figure 2.
Esquematic design of metacercariae of
Clinostomum
sp. A. Ventral view showing the complete body. B. Anterior
part of the body. C. Posterior part of the body. os = oral sucker, ph = pharynx, ic = intestinal caecum, a = acetabulum, u =
uterus, at = anterior testes, o = ovary, pt = posterior testes. Scale bar: A = 2 mm, B, C = 300 µm.
facilitating the contact with the invasive cercariae.
On the other hand, the low value found for the
infection in the caudal fin, as compared with the
other fins, is likely to be due to the more intense
movements of the caudal fin; therefore, making
difficult the penetration by the cercariae into the
body of
Apistogramma
sp. Similar report are
present by Eiras
et al.
(1999) where infected
loricarids present more metacercariae of
C.
marginatum
attached into dorsal and anal fins
compared with the caudal fin that presented low
levels of infection.
Metacercariae of trematodes may change the
behavior of their second intermediate fish host,
enhancing the chance to be eaten by the final host
(Szidat, 1969; Simsak
et al
., 2018). As an adaptive
strategy,
Clinostomum
spp. are able to infect the
Infestation of
Clinostomum
sp.
image/svg+xml
54
Neotropical Helminthology, 2022, 16(1), ene-jun
Figure 3.
Metacercariae of
Clinostomum
sp.
parasitizing the fins of ornamental cichlids. A. Lateral view of
Pterophyllum scalare
showing metacercariae in dorsal and pectoral fins. B. Pectoral fin of
P. scalare
with metacercariae. C. Lateral view of complete
body of
P. scalare
with metacercariae on dorsal and pectoral fins. D. Dorsal fin of
Cichlassoma amazonarum
with trematodes. E.
Anal fin of
Apistogramma
sp. with encysted metacercariae. F. Dorsal fin of
Apistogramma
sp. with encysted metacercariae Scale
bar A, C, D = 5 mm; B, E, F = 3 mm.
Murrieta-Morey
et al.
image/svg+xml
Bush, A O, Lafferty, K D, Lotz, J M. & Shostak W
A. 1997.
Parasitology meets ecology on its
own terms: Margolis
et al.
revisited
. The
Journal of Parasitology, vol. 83, pp.
575–583.
Castelo, F P. 1984.
Ocorrência de
Clinostomum
marginatum
Rudolphi, 1819 “Yellow-Spot
Disease” em filé de jaraqui
(
Semaprochilodus insignis
Shomburgk,
1814).
Acta Amazonica, vol. 13, pp. 325-
326.
De Souza, D C, De Sousa, L F, Coelho, T A. &
Corrêa L L. 2020a.
Host–parasite
interaction between trematode,
Clinostomum marginatum
(Clinostomidae)
and armoured catfish,
Pterygoplichthys
pardalis
(Loricariidae) from Brazilian
Amazon.
Annals of Parasitology, vol. 66,
pp. 243-249.
De Souza, D C, Nogueira, A. & Corrêa L L. 2020b.
Parasitism by
Clinostomum marginatum
(Clinostomidae) in neotropical electric fish
(Gymnotiformes) in the Brazilian Amazon.
Annals of parasitology, vol. 66, pp. 101-
106.
Eiras, J, Dias, M L, Pavanelli, G C. & Machado M
H. 1999.
Histological studies on the effects
of
Clinostomum marginatum
(Digenea,
Clinostomidae) in its second intermediate
host
Loricariichthys platymetopon
(Osteichthyes, Loricariidae) of the upper
Paraná River, Brazil. Acta Scientiarum.
Biological Sciences, vol. 21, pp. 237-241.
García-Dávila, C, Estivals, G, Mejia, J, Flores, M,
Angulo, C, Sánchez, H, Nolorbe, C,
Chuquipiondo, C, Castro-Ruiz, D, García,
A, Ortega, H, Pinedo, L, Oliveira, C, Römer,
U, Mariac, C, Duponchelle, F, Renno, J F.
2021.
Peces Ornamentales de la Amazonía
Peruana.
Instituto de Investigaciones de la
Amazonia Peruana (IIAP). 503 p.
Isaac, A, Guidelli, G M. & De França J G. 2004.
Composição e estrutura das
infracomunidades endoparasitárias de
Gymnotus
spp. (Pisces: Gymnotidae) do rio
Baía, Mato Grosso do Sul, Brasil.
Acta
Scientiarum, Biological Sciences, vol. 26,
pp. 453-462.
Kullander, S. & Silfvergrip A. 1991.
Review of the
fins of the fish, causing difficulty for swimming
and therefore be more susceptible to predation by
piscivorous birds (Eiras
et al.
, 1999; Simsak
et al.
,
2018). Additionally, in infected fish, metacecariae
induce to present slight degeneration of the muscle
fibers and the destruction of the fat cells of the fins,
making the movements and the ability to response
to stimulus slower than in non-infected specimens
(Eiras
et al
., 1999). In the present study, the
location of the metacercaria on the fins of cichlids
may be a strategy to induce to erratic swimming,
susceptibility to swimming closer to the surface of
the water and to cause other disturbs for running
away from their predators.
According to Lo
et al
. (1982), when a large amount
of cercariae of
Clinostomum
spp. penetrate the fish
body at the same time they may cause irritation and
lesions to fish tissue, which may induce mortality
of small fish. Furthermore, specimens may become
weak and grew more slowly than healthy fish,
dying during transportation (Lo
et al
., 1982). As
“Apistograma tapiche”
Apistogramma
sp.,
C.
amazonarum
and
P. scalare
are cultivated in the
Peruvian Amazon for exportation as ornamental
fish, the presence of
C. marginatum
could
compromise the health of the fish and to cause
mortalities, either due to susceptibility to predation
by piscivorous birds or due to injuries caused by the
infection of parasites. In that way, to prevent also
economic losses, prophylactic measures should be
taken into consideration: avoid the presence of
aquatic snails and piscivorous birds near the
breeding ponds.
Molecular studies will be necessary to be able to
identify at the species level the metacercariae of
Clinostomum
collected from the analyzed cichlids.
This, in order to guarantee the correct taxonomic
identification based not only on morphological
characters, but also based on the genetic sequence
of the parasites.
55
Neotropical Helminthology, 2022, 16(1), ene-jun
The authors thank the Amazon Research Center for
Ornamental Fishes (ARCOF), Perú, for providing
the samples used in the present study.
ACKNOWLEDGEMENTS
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