MASSIVE INFESTATION BY GUSSEVIA UNDULATA (PLATYHELMINTHES: MONOGENEA:
DACTYLOGYRIDAE) IN FINGERLINGS OF CICHLA MONOCULUS CULTURED IN THE
PERUVIAN AMAZON
INFESTACIÓN MASIVA POR GUSSEVIA UNDULADA (PLATYHELMINTHES: MONOGENEA:
DACTYLOGYRIDAE) EN ALEVINOS DE CICHLA MONOCULUS CULTIVADO EN LA
AMAZONÍA PERUANA
Neotrop. Helminthol., 6(2), 2012
2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1* 2 3
Patrick Mathews Delgado , John Paul Mathews Delgado & Rosa Ismiño Orbe
Suggested citation: Mathews-Delgado P, Mathews-Delgado, JP & Ismiño-Orbe, R. 2012. Massive infestation by Gussevia
undulata (Platyhelminthes: Monogenea: Dactylogyridae) in fingerlings of Cichla monoculus cultured in the Peruvian Amazon.
Neotropical Helminthology, vol. 6, N°2, pp. 231 - 237.
Abstract
Cichla monoculus (Spix & Agassiz, 1831) is a species with great potential for breeding in controlled
environments in the Peruvian Amazon. This fact that has led to semi-intensive and intensive
production intended for human consumption. However, more studies are required regarding the
population of parasites that are affecting breeding and development of the species. This study
identified a high infestation of a monogenean species, Gussevia undulata (Kritsky, Thatcher, Boeger,
1986), in semi-intensively fish farming of C. monoculus. The prevalence was 100%, with mortality of
all fish. The mean intensity and mean abundance of the parasite was 168.5 of parasites per individual.
This is the first report of high infestation by G. undulata in C. monoculus cultured from the Peruvian
Amazon.
Keywords: Cichla monoculus - fish farming - Gussevia undulata - infection - monogenea - parasite.
Resumen
Palabras clave: Cichla monoculus - Gussevia undulata - infección - monogeneo - parásito - piscicultura.
Cichla monoculus (Spix & Agassiz, 1831) es una especie con gran potencial para su crianza en
ambientes controlados en la Amazonía Peruana, hecho que ha llevado a su producción semi-intensiva
e intensiva destinada al consumo humano. Sin embargo, se necesitan más estudios sobre la población
de parásitos que afectan la producción y desarrollo de la especie. Este estudio identificó una alta
infestación de monogeneos de la especie Gussevia undulata (Kritsky, Thatcher, Boeger, 1986) en un
cultivo de C. monoculus. La prevalencia fue del 100%, con una mortalidad de todos los peces. La
intensidad media y la abundancia media del parásito fue 168,5 parásitos por pez. Este es el primer
informe de una alta infestación por G. undulata en C. monoculus cultivado en la Amazonía peruana.
*
¹ University of Strasbourg, Institute Charles Sadron, Department of Biomedical Sciences, 67034, Strasbourg, France.
patrickmathews83@gmail.com; Phone:+33 (0) 388414219; Fax:+33 (0) 388414099.
2National Institute of Amazonian Research, Department of Ecology, 69060-001 Manaus, Amazonas, Brazil.
3Research Institute of the Peruvian Amazon, Department of Aquatic Ecosystems, 265556 Iquitos, Loreto, Peru.
231
Mathews-Delgado et al.
Gussevia of Cichla monoculus cultured
In fish farming the intensive exploitation allows
the handling of high densities of organisms per unit
area. Indeed, this type of management frequently
leads to break the balance between pathogen and
host, consequently resulting in the emergence of
infectious and parasitic diseases that cause various
problems ranging from slow up growth, reduced
fertility rates, until the appearance of severe
epidemics resulting in high mortality (Thatcher,
1991; Pavanelli et al., 1998; Scholz, 1999; Cable et
al., 2002; Lemos et al., 2007; Araujo et al., 2009;
Del Rio-Zaragosa et al., 2010).
Cichlids have wide geographical distribution.
Currently there are 1533 known species, with 320
reported for South America (Kullander, 1988).
These species inhabit a wide variety of aquatic
ecosystems. Moreover, the fish represent high
economic importance, given that they are
marketed for human nutrition with a promissing
potential for intensive and extensive aquaculture
(Kullander & Ferreira, 2006; Araujo et al., 2009).
Cichla monoculus (Spix & Agassiz, 1831) can
reach up to 70 cm in length and 9 kg of total weight
(Chellappa et al., 2003; Keith et al., 2000) and is a
much appreciated species with great acceptance on
the Amazonian market being regarded as a food
fish of the highest quality. Due to its zootechnical
characteristics, the C. monoculus is considered a
species with great potential for management in
controlled environments aiming human nutrition
and ornamental purposes. However, to allow the
breeding to become entirely feasible, it turns out
the necessity to solve the problem of diseases and
parasites upsurge affecting this species in
controlled environments, as a consequence of
intensive farming under inadequate management
(Varella & Malta, 1995).
Among the various groups of helminthes which
parasite fishes from freshwater, the monogeneans,
represented by many species, cause substantial
economic losses in fish farms around the world
(Jones, 2001; Marcogliese et al., 2001). An
important characteristic is that the fish parasitized
by monogeneans, show necrosis and bleeding
wounds in the integument and gills, serving as a
gateway to different pathogenic protozoa and
bacteria of very difficult controlling (Flores-
INTRODUCTION
Crespo & Flores, 1993; Harris et al., 1998; Del
Rio-Zaragoza et al., 2010). It represents, thus, a
serious concern, since monogeneans affect a huge
variety of Cichlids in tropical and semitropical
regions where parasites are favored by ecological
conditions (Martins et al., 2002; Flores-Crespo &
Flores, 2003).
Therefore, with the gradual increase of intensive
and semi-intensive fish farming in the Peruvian
Amazon, there is a need for constant monitoring of
the fish for the diagnosis and timely control of
infestations by monogeneans. In this sense, the
present study aims to evaluate the monogenean
infestation in C. monoculus bred in a fish farm in
the Peruvian Amazon.
Between September and October 2011, which
corresponds to the relative dry season, 50
individuals of the species C. monoculus were
collected with drag nets, from a semi-intensive fish
farm, located in the northeast of Loreto (Peru),
between latitudes 3° 48' 48.9'' N and 073° 19' 18.2''
W, with average annual temperature of 26.3 °C and
relative humidity of 85% at 328 masl.
The physicochemical parameters of the water were
measured three times daily (at 8 AM, noon and 4
PM) with daily checks of dissolved oxygen (5.64 ±
-1
0.8 mg L ), pH (4.83 ± 0.10), temperature (27.23 ±
-1
1.50 °C) and conductivity (106.1 ± 14.0 µs cm ) by
means of a YSI multiparameter meter (Model MPS
-1
556). Ammonium total (0.20 ± 0.10 mg L ),
-1
hardness (21.40 ± 1.80 mg L ), carbon dioxide (3.2
-1
± 0.9 mg L ) and total alkalinity (16.14 ± 0.80 mg
-1
L ) were monitored weekly and in the morning (8
AM), using a complete package for analysis of
freshwater (LaMotte AQ-2).
Fish were fed twice daily with extruded diet
-1
containing 25% crude protein and 2.6 Mcal kg of
digestible energy and feeding rate of 5% of the
biomass of the pond.
The sampled fish presented length of 5.60 ± 0.10
cm and weight of 6.60 ± 0.86 kg. Having identified
the parasite infestation, the fish were transferred to
concrete tanks covered with tiles to undergo long-
-1
term baths containing 0.5 to 2.0 mg·L of
MATERIAL AND METHODS
232
Neotrop. Helminthol., 6(2), 2012
potassium permanganate and 1% formalin during
one hour. In the absence of improvement, we
sacrificed and burned all the fish from the
respective pond. Systematically, the fish have been
previously weighed (in g), measured (in cm, total
length) and numbered; these data were collected in
individual records. Following, the fish were
sacrificed by cerebral puncture and placed in
individual containers. The research was authorized
by the Instituto de Investigaciones de la Amazonia
Peruana-IIAP and necropsy of fish was conducted
within the ethical standards.
Using a stereoscope we examined the body
surface, fins, nostrils, mouth, opercula and gills,
looking for possible injuries and excess of mucus
production. By means of a scalpel, we also
performed scraping of the skin, fins and gills to
observe possible attached parasites.
For examination of the gills, the samples were
separated and placed in glass containers with a
1:4,000 formalin solution. After one h, the gills
were stirred in the liquid and then removed from
the container. Helminths were allowed to settle on
the bottom and were subsequently collected with
the aid of a small probe and a dissecting
microscope (Nikon SM-30). The identification of
the parasites was based on the methodology of
Kritsky et al. (1989) and Thatcher (2006). The
specimens were deposited in the collection of
invertebrates from Ecosystem Aquatic Program,
Research Institute of the Peruvian Amazon and
thereafter some specimens shall be deposited in the
collection of Helminths of Instituto Nacional de
Pesquisas da Amazônia (INPA).
To study the monogeneans, permanent slides were
prepared with total parasites assembly according to
the method HYP (Hundred Year Permanence). For
the study of sclerotized structures, parasites were
fixed in a solution of ammonium picrate glycerine
(GAP) and mounted in Canada balsam according
to Malmberg (1957). Some specimens were
mounted unstained in Gray and Wess' medium. To
visualize internal structures, parasites were fixed in
hot formaldehyde solution (4%) for staining with
Gomori's trichrome. The parasitic indexes
calculated for assessing the level of infestation of
parasites in the fish were prevalence, mean
intensity and mean abundance (Margolis et al.,
1982; Bush et al., 1997).
The necropsy of fingerlings from C. monoculus
bred in controlled environments in the Peruvian
Amazon evidenced the infestation by the
monogenean Gussevia undulata (Kritsky,
Thatcher and, Boeger, 1986) in the gill filaments of
the fish.
Indeed, the totality of the examined fish showed a
high parasitic infestation by G. undulata. The mean
intensity was equal to the mean abundance,
provided that the number of parasitized fish was
the same as those examined (Table 1).
233
RESULTS
Table 1. Parasitic indexes of Gussevia undulata in fingerlings of Cichla monoculus cultured in the Peruvian
Amazon.
Parasitic indexes Gussevia undulata
Prevalence (%) 100
Abundance (count)
9864
Mean abundance (count) 168.5
Mean intensity (count) 168.5
234
Mathews-Delgado et al.
Gussevia of Cichla monoculus cultured
Even though in the ponds of cultivated C.
monoculus the physical and chemical parameters
of the water were within the expected range of
values for tropical species, massive infestation of
monogenean was found. However, the increment
of parasitic infections in artificial environments
has been associated with low quality of water and
inadequate management (Thoney & Hargis, 1991).
Several studies report the parasitism of neotropical
cichlids by monogeneans belonging to the genus
Gussevia Kohn and Paperna 1964 (Kritsky et al.,
1989; Vidal-Martinez et al., 2001; Yamada et al.,
2010; Mendoza-Franco et al., 2010). For South
America, thirteen species of Gussevia have been
described for eight species of cichlids (Kritsky et
al., 1986, 1989), evidencing a high specificity of
the genus Gussevia in parasitizing cichlids.
In the Central and Peruvian Amazon several
species of monogeneans of the genus Gussevia
have been reported parasitizing cichlid of
economic importance for human nutrition and
ornamental purposes. Among the species of
monogeneans, Gussevia asota and G. astronoti
have been described in parasitizing freshwater
Astronotus ocellatus, G. spiralocirra
(Pterophyllum scalare), G. elephus and G. obtusa
(Uaru amphiancanthoides), G. alioides, G. dispar
and G. disparoides (Heros severus and
Cichlasoma amazonarum), G. longihaptor and G.
undulata (Cichla monoculus), G. tucunarense, G.
longihaptor, G. disparoides, G. arilla, G. dispar
and G. undulata parasitizing Cichla ocellaris
(Kritsky et al., 1989; Mendoza-Franco et al., 2010;
Azevedo et al., 2010). Despite, any parasitism by
the monogenean G. undulata in C. monoculus has
been reported. In our study we report for the first
time the parasitism by the G. undulata in
fingerlings of C. monoculus bred in controlled
environments in the Peruvian Amazon.
In the study described herein, the fingerlings of C.
monoculus presented high levels of parasitism by
the monogenean G. undulata. Parasites that have a
direct life cycle, such as monogeneans, are more
frequently found in lentic environments.
Moreover, this type of environment favors the
transmission of these parasites (Flores-Crespo et
al., 2003; Azevedo et al., 2007), which justifies the
fact that the fish had elevated parasite infection,
since the same are confined to their culture in
earthen ponds where water circulation is almost
negligible or nonexistent.
In natural aquatic environments with low levels of
dissolved oxygen, fish undergo stress and end up
susceptible to intense parasitic infestation
(Pavanelli et al., 2004; Hogue & Swig, 2007). In
confined environments where fish are raised this
situation is aggravated as a result of the capture,
transport, inadequate nutrition, low amount of
dissolved oxygen, temperature and pH with large
variations and poor installations (Malta et al.,
2001; Hogue & Swig, 2007). Under these
conditions, monogeneans can cause large bias and
even death, as these parasites induce the gills to
produce an excessive amount of mucus, which
difficult breathing and consequently prejudice the
fish growth. According to Buschmann (2001) and
Mariano et al. (2010), intensive fish farming
generates a large accumulation of organic matter
on the pond bottom produced from the excreta,
dead matter and the fraction of uneaten food. This
organic matter produces hypoxia and anoxia that
creates an unbalance in the homeostasis of the fish,
eventually leading to the increase of the oxidative
stress of biomolecules, promoting thus various
physiological and biochemical alterations, causing
cell impairment and death (Sherry, 2003; Van der
Oost et al., 2003). Therefore, these adverse effects
of poor water quality reduce the self resistance of
the fish, which turns out as a favorable condition to
the parasite proliferation. This fact may justify the
high parasitic infestation by G. undulata in C.
monoculus from fish farming.
The results described herein are in accordance with
Kritsky et al. (1989) and Yamada et al. (2011), who
found the monogenean G. undulata parasitizing
gills of two species of cichlid, C. ocellaris and C.
kelberi respectively, being common the setting of
this kind of monogenoide parasite in this organ
(Kritsky et al., 1989). Indeed, several studies report
the parasitism of G. disparoides in gills of H.
severus, C. amazonarum and C. ocellaris and all
these fish species are currently being raised in
confined environments in the Peruvian Amazon.
Furthermore, in a study with C. kelberi, captured
from the wild, Yamada et al. (2011) found 18.42%
of prevalence and mean intensity of one and four
DISCUSSION
235
Neotrop. Helminthol., 6(2), 2012
monogeneans of G. tucunarense. However, the
results differ from our study where we found a
prevalence of 100% and mean intensity of 50 and
100 parasites of G. tucunarense. A possible reason
for the low levels of infestation reported by
Yamada et al. (2011) may be fact that the fish
originate from nature. Nevertheless, Kritsky et al.
(1989) found 100% prevalence of G. undulata in
C. ocellaris, although without informing other
parasitic indexes.
Parasites of the genus Gussevia are considered
specific for cichlids and therefore may show low
susceptibility when present in favorable breeding
conditions. This is the first report of G. undulata
parasitizing C. monoculus in fish farming in the
Peruvian Amazon. The high parasitism turns out as
an important reason according to which the fish
stopped taking food, occasionally leading to
mortality.
The results of this study and studies addressing
various aspects of parasite in other species bred in
the same region (Iannacone & Luque, 1991;
Mathews et al., 2007; Dinis et al., 2007; Mathews
et al., 2011) confirm the necessity of constant
monitoring of fish, seeking the diagnosis and
timely control of infestations by monogeneans, in
order to eradicate, once installed in cropping
systems, the use of highly toxic products that cause
mortality of the host or leave unviable the fish
farming intended for human consumption. The
present study reports thus, a serious pathological
problem that resulted in the mortality of most fish
and alerts to the need for preventing actions.
The authors thank Omar Mertins for reviewing this
manuscript and Salvador Tello Martin for
providing all the facilities in the Programa de
Ecosistemas Acuaticos/ Instituto de
Investigaciones de la Amazonia Peruana.
ACKNOWLEDGMENTS
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Correspondence to author/ Autor para
correspondencia:
Patrick Mathews Delgado
University of Strasbourg, Institute Charles
Sadron, Department of Biomedical Sciences,
67034, Strasbourg, France.
Phone:+33 (0) 388414219;
Fax:+33 (0) 388414099.
E-mail/ correo electrónico:
patrickmathews83@gmail.com
Received September 10, 2011.
Accepted December 3, 2012.
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