ESJ Natural/Life/Medical Sciences
Epidemiology of Gill Monogenean Parasites Infections in Nile
Tilapia Oreochromis Niloticus (Teleostei: Cichlidae) from
Agneby River, Côte d’Ivoire
Adou Yedehi Euphrasie
Research Unit on Ecology and Biodiversity, Laboratory of Ecology and
Sustainable Development, University Nangui Abrogoua, Abidjan, Côte
d’Ivoire
Blahoua Kassi Georges
Research Unit on Hydrobiology, Laboratory of Natural Environments and
Biodiversity Conservation, University Félix Houphouët-Boigny, Abidjan,
Côte d’Ivoire
Yeo Kolo
Konate Souleymane
Tiho Seydou
Research Unit on Ecology and Biodiversity, Laboratory of Ecology and
Sustainable Development, University Nangui Abrogoua, Abidjan, Côte
d’Ivoire
Doi:10.19044/esj.2021.v17n34p30
Submitted: 22 June 2021
Accepted: 15 September 2021
Published: 30 September 2021
Copyright 2021 Author(s)
Under Creative Commons BY-NC-ND
4.0 OPEN ACCESS
Cite As:
Adou.Y.E., Blahoua K.G., Yeo K., Konate S. & Tiho S. (2021). Epidemiology of Gill
Monogenean Parasites Infections in Nile Tilapia Oreochromis Niloticus (Teleostei:
Cichlidae) From Agneby River, Côte d’Ivoire. European Scientific Journal, ESJ, 17(34), 30.
https://doi.org/10.19044/esj.2021.v17n34p30
Abstract
The Nile tilapia, Oreochromis niloticus is a fast growing fish and has
a great importance for fisheries, aquaculture, and screen aquarium in Côte
d’Ivoire. Parasitic infections constitute significant economic loss in fish
production. The work based on Epidemiology of gill Monogenean parasites of
O. niloticus from the Agneby River between August to December 2020, for
the first time, was aimed to characterize the physicochemical parameters of
this River, to inventory the gill Monogenean species in Nile tilapia, to analyze
the parasitism as a function study areas and to highlight the parasite species’
distribution on the gill. A total of 102 specimens of fishes was sampled and
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examined for parasites. Gill helminthofauna of this fish consisted of
Cichlidogyrus cirratus, C. tilapiae, C. halli and Scutogyrus longicornis. Fishes
of the Agneby River at Agboville are more infested than the other ones due to
environmental conditions. The examination of the two sides of the fish
revealed that parasites species have the same affinity for the both sides of the
fish. In contrast, at the level of the gill arch, these parasites preferred median
gill arches (arches II and III).
Keywords : Parasitic Infection, Gill Monogenean, Oreochromis Niloticus,
Agneby River, Côte d’Ivoire
Introduction
The Nile tilapia Oreochromis niloticus (Linnaeus, 1758) has long been
presented as the gem of African fish farming in view of its high market
demand (Amoussou et al., 2016). This fish species is highly prized by Ivorian
consumers because of its nutritional value. It has been the subject of various
research and extension programs worldwide and in Africa (Amoussou et al.,
2016). However, this fish, like any other living organism, doesn’t escape
parasitic monogeneans. These organisms are ectoparasites whose biological
cycle is direct. These pathogens are flatworms of aquatic organisms, mainly
fish, in which they frequently infest various organs such as the gills, skins,
fins, rectal cavities and nostrils.
Their study has a triple interest : scientific, ecological and economic
(Hem and Avit, 1994). Indeed, these parasites are excellent bio-indicators,
phylogenetic, geographical and ecological indicators of host populations
(Paugy and Guégan, 1989 ; Guégan and Lambert, 1991). In addition, they
often create pathologies and behavioral changes (Lafferty et al., 2008). The
development of aquaculture has therefore led to greater attention being paid to
problems caused by parasitic gill monogeneans leading to constraint in fish
productivity. Thus, studies related to these parasites have been conducted in
order to have reference data for the subsequent monitoring investigations of
the parasitic fauna of fish and to elaborate adequate measures to assure a better
productivity. The Nile tilapia representing the most used species in
aquaculture can be confronted with parasitism problems.
In Africa, most of the studies have been done on Monogeneans
parasites focused on inventory and taxonomy (Pariselle and Euzet, 2009).
Little study concerning epidemiology of these parasites infections was carried
out. But, this is very necessary to understand the processes involved in the
structure and maintenance of parasite communities (Zharikova, 2000) in order
to fight against these pathogens. Indeed, epidemiological data on infection by
these parasites allow the use of adequate methods for effective control of these
pathogens, especially in fish farming. These studies also provide important
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information on their host (Zharikova, 2000). Unfortunately, studies related to
gill Monogenean parasites of fish from freshwater such as rivers are scarce,
while parasites have an impact on the dynamics of fish stocks. In Côte d'Ivoire,
except for the works carried out in the artificial lake (Blahoua et al., 2016), no
studies have been done on the epidemiology of O. niloticus parasitic infection
by Monogenean in the Agneby River where, strong anthropogenic pressures
are exerted. It’s well known that these pressures can modify biodiversity in
general and parasite biodiversity in specially. The present investigation was
aimed to study some ecological aspects of gill Monogeneans parasites of O.
niloticus in the Agneby River.
Materials and methods
Study sites
The Agneby River (Figure 1) is located in southern Côte d'Ivoire
between 3°50′ and 4°41′ W longitude and between 5°10′ and 6°08′ N latitude
(Goula et al., 2009). With a length of 217 km, this river is a continuum which
takes its source near the villages of Affery and Agoua in the department of
Bongouanou and flows towards the Ebrie lagoon by throwing itself in that one
in the town of Dabou (Goula et al., 2009). Its watershed covers an area of
approximately 8900 km² (Savané, 2010) and is located East of the TiassaléDimbokro-M'bahiakro line. The Agneby River also shows signs of
eutrophication and the water body is invaded by aquatic plants, particularly
Eichornia crassipes. Its course is entirely under forest type vegetation.
Plantations of coffee, cocoa, banana and oil palm are developped around this
River.
Two stations, Agneby-Agboville and Agneby-village were selected for
this study. The Agneby-Agboville station (4°12′ W - 5°56′ N) is characterized
by a substrate composed of a mixture of clay, mud, and foliage. The canopy is
almost non-existent except in a few places on the border. The river is
constantly receiving waste water and garbage from the said city. Furthermore,
the Agneby-village station (4°20′ W - 5°19′ N) is characterized by a type of
swamp forest, with mangroves and bamboo. In addition to fishing, this water
is used for household activities (washing up, laundry) and for domestic waste
(waste water, garbage, faeces).
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Figure 1. Study area and location of sampling sites on the Agneby River
Host sampling and parasitological examination
From August to December 2020, a total of 102 Oreochromis niloticus
individuals from the two study stations were collected. The fishes were
captured with gillnets (mesh size 8 to 90 mm). They were identified following
the Teugels and Thys van den Audenaerde (2003) keys. The four left and right
gill arches were removed by scissors and forceps and preserved in ice (0°C).
In the laboratory, each of the gill arches was separated and placed in Petri
dishes containing water. They were numbered from I to IV from the anterior
part of the gill arch under the operculum to the posterior part. Each gill arch
was put under a binocular microscop (Olympus SZ 60) for examination of
parasites. They were collected, mounted between slide and coverslip in a
micro-drop of ammonium picrate-glycerin. They were determined up to the
species with the Pariselle and Euzet (2009) keys.
Water quality
Parameters (temperature, dissolved oxygen, pH and conductivity)
were measured in water surface, with a scientific portable multi-parameter
probe (multiparameter HANNA 9828). The transparency was measured using
a Secchi disk. Water samples were collected and preserved at 4°C for
subsequent analyses of nutrients: nitrate–nitrogen, nitrite–nitrogen and
ammonia–nitrogen using DR\2010 spectrophotometer. The results of analysis
were expressed as mg/liter except for temperature and conductivity which
were measured as °C and microsiemens (µS/cm), respectively.
Data analysis
The prevalence and mean intensity as defined by Bush et al. (1997)
were calculated. Species classification was done by prevalence data according
to the scale of Valtonen et al. (1997). Parasitic species are frequent if the
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prevalence is greater than 50%, they are less frequent if the prevalence is
ranged between 10 and 50% and rare if the prevalence is less than 10%. Mean
intensity (MI) is high if its value is greater than 100, average if its value varies
from 50 to 100, low if its value varies from 10 to 50 and very low if its value
is less than 10 (Bilong Bilong and Njiné, 1998).
Statistical analysis
The nonparametric tests of Kruskal-Wallis (K) and Mann Whitney (U)
were used to determine whether the variability of parasite intensity is
significant. STATISTICA 7.1. Software was used for data analysis and results
were considered significant at the 95 % level (p < 0.05).
Results
Monogenean parasite species composition
The observation of Oreochromis niloticus’s gills from Agneby River
revealed the presence of four Monogenean species belonging to genera
Cichlidogyrus Paperna, 1969 and Scutogyrus Pariselle & Euzet, 2003 (Table
1). These Monogeneans are Cichlidogyrus tilapiae, C. halli, C. cirratus and
Scutogyrus longicornis.
In both study stations (Agneby-village station and Agneby-Agboville
station), the prevalence values of the Monogenean parasites Cichlidogyrus
cirratus and C. halli were greater than 50%. Thus, they were classified as
common or core species of this community. In addition, the prevalence value
of parasite C. tilapiae was between 10 and 50% while the prevalence value
was less than 10% for the parasite Scutogyrus longicornis. These two
Monogeneans were classified as secondary and rare species of this
community, respectively. Except for the low mean intensities of C. cirratus
and C. halli observed in the Agneby-Agboville station, the other parasite
species mean intensities were very low in the two study stations.
Spatial distribution of Monogenean species of Oreochromis niloticus
The prevalence and mean intensity of Monogenean species on the gills
of Nile tilapia from Agneby River’s two stations (Agneby-Agboville station
and Agneby-village station) are shown in Table 1. The analysis of these data
revealed that, generally, the epidemiological indices values were higher in
fishes captured in the first station than those captured in the second one.
In the first Agneby River station, the highest prevalence (92%) was
noted for the species Cichlidogyrus cirratus while the lowest one (9.61%) was
recorded for the species Scutogyrus longicornis. In the second Agneby River
station, the highest and the lowest prevalence of these parasite species were
78% and 6%, respectively. For each parasite, the prevalence values differences
observed were not statiscally different between the two Agneby River stations
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(X2 = 1.41 and 1.28 ; ddl = 1 ; p = 0.23 and 0.09 > 0.05, respectively). Thus,
based on the rate of infestation, the Monogeneans C. cirratus and S.
longicornis were partitioned equally between the fishes captured from two
study stations.
In Agneby-Agboville and Agneby-village stations, the highest values
of mean parasite intensity (12.13 ± 1.6 and 6.05 ± 0.2 respectively) were noted
for Cichlidogyrus halli and C. cirratus. The lowest values (3 ± 0.01 and 2.33
± 0.02) were recorded for Scutogyrus longicornis. The intensity values of each
parasite species were statiscally different between the two Agneby River
stations (p = 0.02 < 0.05). Thus, in term of number of parasites, the fishes
captured in the Agneby-Agboville station were the most infested.
Table. 1 Prevalence (%) and mean intensity of Cichlidogyrus and Scutogyros species
according to study stations of Agneby river
Branchial repartition of Monogenean species
The intensity of parasites species as a function of the gills of Nile
tilapia from Agneby River’s two stations are shown in Table 2. It shows that
Monogenean species Cichlidogyrus cirratus (n = 120) and C. tilapiae (n = 43)
were more abundant on the left gills of the fish, while the Monogeneans C.
halli (n = 49) and Scutogyrus longicornis (n = 4) were more concentrated on
the right gills at the Agneby-village station. Except for Monogenean C.
cirratus (n =280) which was more abundant on the right gills, the other species
C. halli (n = 263), C. tilapiae (n = 76) and Scutogyrus longicornis (n = 8) were
more accumulated on the left gills at the Agneby-Agboville station. There was
no preference in the distribution of parasites species between the left and right
gills of Oreochromis niloticus (p = 0.06 > 0.05).
The intensity of the parasitic species as a function of the gill arch is transcribed
in Table 3. It indicates that Monogeneans C. cirratus, C. halli and Scutogyrus
longicornis were more concentrated on gill arch II (n = 180, 171 and 5
respectively) and the gill arch III (n =185, 177 and 5 respectively) (p = 0.01 ˂
0,05) at the Agneby-Agboville station. In addition, Monogenean C. tilapiae
was more accumulated on gill arch II (n = 59) and the gill arch I (n = 44).
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Furthermore, all parasite species C. cirratus, C. halli, C. tilapiae and
Scutogyrus longicornis preferred the gill arch II (n= 92, 34, 29 and 3
respectively) at the Agneby-village station and the gill arch III (n= 95, 31, 30
and 2 respectively) at the Agneby-village station (p = 0.02 ˂ 0,05).
Table 2. Intensity of parasites species as a function to host side of Oreochromis niloticus in
Agneby river
Table 3. Intensity of parasites species as a function to the gill arch of Oreochromis niloticus
Water quality
Water quality parameters were shown in Table 4. The minimum and
maximum of temperature values were respectively as 27.34°C and 30.83°C at
Agneby-village station. The median value of this parameter in this station was
28.38 °C. It varied from 27.64 to 31.45°C with a median value of 28.57°C at
Agneby-Agboville station. These different values did not reveal any
significant difference between the two stations. The temperature values were
practically the same between the two study stations
The minimum and maximum of oxygen level values were respectively
as 2.75 and 4.45 mg/l at Agneby-village station. The median value of dissolved
oxygen level measured at this station was 1.84 mg/l. These data ranged
between 1.12 and 2.3 mg/l with a median value of 0.83 mg/l at AgnebyAgboville station. Dissolved oxygen level showed that there was significant
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difference between the two stations (p = 0.001 < 0.05). The Agneby River
waters at Agboville station were the least oxygenated.
The pH of water varied from 6.50 to 8.44 at Agneby-village station and
from 6.49 to 7.75 at Agneby-Agboville station. Mediaan values were 7.18 and
7.46, respectively. The analysis of the Mann-Whitney U test indicated no
significant variation of this parameter between stations (p = 0.1 ˃ 0,05). The
pH values were practically the same between the two study stations.
The water transparency fluctuated between 54 and 165 cm with a
median value of 64.26 cm at Agneby-village station. The values ranged from
39 to 82 cm with a median value of 35.2 cm at Agneby-Agboville station. The
statistical analysis test (p = 0.01 ˂ 0.05) revealed that the Agneby River at the
village station was more transparent than the Agneby River at the Agboville
station. In other words, the Agneby River waters at Agboville station were the
least transparent.
The conductivity varied between 62 and 618.33 μS/cm at Agnebyvillage station. It ranged from 167 to 361 at Agneby-Agboville station. The
corresponding median conductivities were 93.4 and 244.5μS/cm. MannWhitney U test showed significant variation of this parameter between stations
(p = 0.02 < 0.05) with the highest conductivity recorded at Agneby-village
station and the lowest obtained at Agneby-Agboville. This means that the
Agneby River waters at Agboville station were the richest in dissolved solids.
The minimum and maximum of ammonium values were respectively
0.01 and 0.06 mg/L at village station. The median value of this parameter in
this station was 0.025 mg/L. It varied from 0.02 to 0.09 mg/ L with a median
of 0.05 mg/L at Agboville station. The ammonium showed significant
difference between the two stations (p = 0.001 < 0.05). The nitrate of the water
varied between 0.16 and 0.37 mg/L at village station and from 0.32 to 0.6
mg/L at Agboville station. Median values were 0.2 et 0.48 mg/L respectively.
The analysis of the Mann-Whitney U test indicated significant variation of this
parameter between stations (p = 0.001 < 0,05). The Agneby River waters at
Agboville station were the most mineralized in ammonium and nitrate ions.
The nitrite fluctuated between 0.004 and 0.06 with a median value of 0.005
mg/L at village station. The values ranged between 0.001 and 0.003 mg/L with
a median value of 0.002 mg/L at Agboville station. This parameter showed
significant difference between the two stations (p = 0.002 < 0.05). The Agneby
River waters at Agboville station were the most mineralized in nitrite ions
too. These observations reflect sources of nutrient input through agropastoral
activities that are developed on both banks.
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Table 4. Physical and chemical parameters of Agneby river (Village and Agboville stations)
Discussion
Four Monogenean parasites species, Cichlidogyrus halli, C. tilapiae,
C. cirratus and Scutogyrus longicornis were recorded on the gill filaments of
Oreochromis niloticus caught in the Agneby River. These results are different
from the findings of Blahoua et al. (2016) who had observed six Monogenean
species belonging to the genera Cichlidogyrus and Scutogyrus in the gills of
the same fish. Comparatived to previous studies, the low number of parasite
species observed in Agneby River could be explained by the fact that the River
flow could made this environment unfavorable to the development of certain
Monogeneans species. Indeed, in flowing rivers, infesting larvae can be
washed away by the water current before they infest their host. This result
could suggest the difficulty for these four parasites species to survive in the
Agneby River. These results are in consistency with Zharikova (2000) who
had highlighted that the parasite richness related to habitat type. According to
this author, with specific ecological conditions, each area presents specific
groups of parasite species in composition and abundance.
Moreover, this study revealed a polyparasitism with predominance of
Cichlidogyrus species on the gills of O. niloticus collected at Agneby River.
Such results have been already noted by some authors. It is the case of Blahoua
et al. (2016, 2020) with Oreochromis niloticus. The permanent presence of
vacant niches on the gill biotope due to the low mean intensities of the four
gill Monogenean obtained in the two study stations would explain its
colonization by several parasite species. Our results agree with the findings of
Simkova et al. (2006). According to these authors, the generally low parasitic
load observed is attributed to the low host density in the natural environment.
Indeed, under such conditions, many parasites do not reach their target because
of their death due to the strong water flow and thus there was the low infective
larvae. According to Simkova and Rohde (2013), interspecific competition for
space is not possible since vacant niches are available on fish gills. Thus,
despite the polyparasitism observed in the present study, the low parasitic
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loads found exclude the hypothesis of interpecific competition as a factor
governing the structuring of gill communities of Nile tilapia, O. niloticus. This
study corroborates with the findings of Lo and Morand (2000) who stated that
there is no interspecific competition in the distribution of Stegastes nigricans
congeneric ectoparasites.
Specific parasitic load varied according to the study stations.
Monogenean species mostly parasitized specimens of O. niloticus caught in
the Agneby River at Agboville station. This could be attributed to the
environmental conditions of the Agneby River at Agboville station (AguirreMacedo et al., 2007). Indeed, the physico-chemical parameters measured in
the two stations showed that the Agneby River waters at Agboville station are
less oxygenated, poorly transparent and rich in nutrients compared to those of
the Agneby River at village. In fact, the dissolved oxygen level is almost zero
(0.83 mg/l) and this value is lower than the limit value of 2 mg/l below which
fish mortality is common as indicated by Francis-Floyd (2003). Also, this
decrease in dissolved oxygen level is accompanied by high nutrient values
recorded (nitrate, ammonium) at this station. This is due to the fact that the
Agneby River at Agboville station is located in the middle of town and
receives all the wastewater of the local population. In addition, it’s the place
where washermen do their laundry and children and animals also defecate in
and around the river. Taking into account the above-mentioned assertion, the
Agneby River waters at Agboville are polluted and dangerously affect the
health of fish. This situation could reduce the immune capacity of the fish
which favors a high infection. Thus, the present results agree with the findings
of Adou (2018)] who showed that the high nitrate, nitrite and ammonium
concentrations indicate the poor water quality and were positively correlated
with the intensity infection. This implies that there is a large quantity organic
material in this environment which could be due to the high density of
particules in suspension and this would favor the transport of eggs/infesting
stages to the fish, thus promoting their high infection. These findings
concurring with Cone et al. (1993), Marcogliese (2005) and Blanar et al.
(2009) who found that the increase in the transmission of the parasites and the
decrease of their population could be caused by ecological conditions of the
water.
The right and left body sides of Oreochromis niloticus were similarly
infected. Some authors have found a similar distribution of Monogeneans on
both sides of the gills of fishes. This is the case of Blahoua et al. (2016) with
O. niloticus and Lim et al. (2016) with species of the genus Oreochromis. The
parasite body symmetry is often involved in the choice of parasite for a
specific site of the host as suggested by Rohde (1979). The equitable
distribution on both sides of the gills of parasites of the genus Cichlidogyrus
and Scutogyrus are due to the presence of bilateral symmetry of their
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morphology as well as similar exposure to the water current. In contrast, an
asymmetric distribution is known for the monogenean Bothithrema bothi
parasite of the Bothidae on Scophthalmus aquosus (Hendrix, 1990). This
phenomenon is probably related to the body of Bothidae which is flat and
dissymetric as suggested by Dessouter (1992). In the present study, the
bilateral symmetry of O. niloticus and its gill Monogeneans could be due the
equitable distribution of these pathogens on both sides of the gills.
In O. niloticus, the Monogeneans mostly accumulated on middle
arches II and III. Similarly, Blahoua et al. (2016) found that Cichlidogyrus
halli and Scutogyrus longicornis were more attached to gill arches II and III
of the same fish. This finding is in consistency with Le Roux et al. (2011) who
had highlighted that the Monogenean Cichlidogyrus philander was
concentrated on the median arches of Pseudocrenilabrus philander philander.
Among environmental factors that determine the microhabitat choice of
Monogeneans, the water current is considered to be the most important factor
(Madanire-Moyo et al., 2010). This reinforces the idea that for many parasites
that have free-living stages (egg or larvae) and whose behavioral responses
depend on the ambient environment, oncomiracidia attachment could be
influenced by water currents (Echi and Ezenwaji, 2009). The other explanation
is that, the middle arches offer a hydrodynamically protected habitat and better
oxygenated conditions as suggested by Yao and Nie (2004). Indeed, the
median part of the gill arches receiving the strongest current of water thus the
high water quantity could provide a high number of parasites (Jerônimo et al.,
2013). The preference of parasites for median arches could also be due to the
large areas they offer to parasites as a habitat (Koskivaara et al., 1991). In the
present study, the synergy of the two factors "heterogeneity of the branchial
system and the flow pattern of the respiratory water " would explain the
parasitic abundances levels on the gill arches.
Conclusion
The present study emerged four (4) Monogenean parasite species on
the gills of Oreochromis niloticus fom Agneby River. Fish infection was
related to the measured physico-chemical parameters of water of study areas.
Fishes captured in the Agneby River at the Agboville station were more
infested because of the poor water quality due to the numerous anthropic
activities that are carried out there. The study also highlighted that
Monogenean species prefferred the middle arches II and III.
Acknowledgments
The authors are grateful to the local fishermen for the data collecting
on the study area.
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