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B IOD I V E R S I TA S ISSN: 1412-033X

Volume 22, Number 4, April 2021 E-ISSN: 2085-4722


Pages: 1975-1980 DOI: 10.13057/biodiv/d220445

The infection of ectoparasitic protozoa on farmed Nile tilapia


(Oreochromis niloticus) at three reservoirs in Central Java, Indonesia

WALEED SULIMAN KRPOS KOLIA1,, SUNARTO1,2,3, TETRI WIDIYANI1,2


1Bioscience Graduate Program, School of Graduates, Universitas Sebelas Maret. Jl. Ir. Sutami 36A, Surakarta 57126, Central Java, Indonesia.
Tel.: +62-271-669376, Fax.: +62-271-663375, email: [email protected]
2Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Sebelas Maret. Jl. Ir. Sutami 36A, Surakarta 57126, Central Java,

Indonesia
3Department of Environmental Science, Faculty of Mathematics and Natural Sciences, Universitas Sebelas Maret. Jl. Ir. Sutami 36A, Surakarta 57126,

Central Java, Indonesia

Manuscript received: 13 February 2021. Revision accepted: 25 March 2021.

Abstract. Kolia WSK, Sunarto, Widiyani T. 2021. The infection of ectoparasitic protozoa on farmed Nile tilapia (Oreochromis niloticus)
at three reservoirs in Central Java, Indonesia. Biodiversitas 22: 1975-1980. There is an expansion of fish culture in Indonesia, but there is
a dearth of information on the parasitic infecting cultured fish. This study was conducted to investigate the occurrence of ectoparasitic
protozoans on farmed Nile tilapia (Oreochromis niloticus) at three reservoirs (i.e., Cengklik, Mulur, and Gajah Mungkur) in Central Java,
Indonesia, and to determine the prevalence, mean abundance, and mean intensity of such parasites. A total of 189 samples were collected
from different cages. The sex of the fishes was determined and their lengths and weights were measured. The gills, fins, and skin were
examined for ectoparasitic protozoa using a light microscope. Among the examined fishes, 146 samples were infected at the rate of 77.2 %.
Mulur reservoir had the highest prevalence rate with 90.4%, followed by Cengklik and Gajah Mungkur with 82.5 % and, 58.7%,
respectively. We found female fishes were more susceptible to the infection than males. Seven parasite species were identified, namely:
Tetrahymena corlissi, Apiosoma spp., Trichodina spp., Cryptobia spp., Chilodonella spp., Ambiphrya spp., and Ichthyophthirius multifiliis.
The protozoan parasite Trichodina spp. recorded the highest prevalence, mean intensity, and mean abundance among all the other protozoan
species at the three reservoirs. The results provided a significant difference at (p<0.01) in the total number of parasites among the reservoirs.
Despite the parasite infection, the physical and chemical parameters of the water of the three reservoirs were within the recommended range
for the culture of Nile tilapia under the cage systems.

Keywords: Ciliated protozoa, ectoparasitic, fish disease, floating cages, Nile tilapia, Oreochromis niloticus

INTRODUCTION for aquaculture commodities including in Nile tilapia


(Oreochromis niloticus).
Aquaculture is the fastest-growing important sector in Protozoan parasites comprise one of the foremost
food production that provides a substantial contribution to pathogens negatively influencing the farmed fish especially
food security and job opportunities. The trades involved in Nile tilapia. In Nile tilapia, several protozoan parasites are
aquaculture-inputs, and products constitute resources that common to attack the fish, including Ichthyobodo necatrix,
stimulate economic growth and poverty reduction (Santos Cichlidogyrus, Gyrodactylus, Dactylogyrus, Contracaecum
et al. 2020). According to the data released by FAO, sp. Tetrahymena corlissi, Apiosoma spp., Trichodina spp.,
Indonesia is the second-largest fish producer in the world Cryptobia spp., Chilodonella spp., Ambiphrya spp., and
after China, with an estimated production of 20.9 million Ichthyophthirius multifiliis (Bruno et al. 2006; Arguedas et
tons per year. The sector contributes to 21.0% of the GDP al. 2017).
generated from agriculture, which is equivalent to 3.1 % of Parasite infestation increases in intensive culture
the national GDP and creates 6.4 million direct jobs (Tran systems due to the high density of fish, and it becomes
et al. 2017). The fish consumption per capita is increasing difficult to eradicate as the fish density increases (Kuchta et
and the country is among high fish consumers with an al. 2018). In this situation, host fish can become a pathogen
annual per capita consumption rate between 30 - 50 kg path for infection to other fishes (Suliman and Al-Harbi
(Santos et al. 2020). 2016). Moreover, protozoan parasites are among the
While the consumption of fish, including Tilapia, foremost pathogenic that infects fishes and cause mortality
continues to increase, the emergence of new diseases under poor environmental conditions and high stocking
threatens aquaculture development. In particular, the density. This problem is one of the most significant
incidence of parasitic diseases on fish is an issue that setbacks in achieving maximum production per unit area of
should be carefully considered. The ectoparasitic protozoa fish cage culture (Biu et al. 2014).
are ubiquitous in the aquatic environment and can cause Symptoms of an infestation vary greatly from one
economic loss in fish farms as a result of host mortality species of fish to another and from one parasite to another.
(Molnar et al. 2019). Such diseases have been the problems Depending on the species of parasite considered and the
1976 B I OD I V E R S ITA S 22 (4): 1975-1980, April 2021

health status of the animals, the prevalence and intensity of Collection of fish specimens
the infestation, the presence of parasites in a farm will have Fish specimens were collected from three different
different impacts (Bruno et al. 2006; Pantoja et al. 2012; zones at each reservoir using a random method. A total of
Arguedas et al. 2017; Indahsari et al. 2019). 189 specimens of Nile tilapia (O. niloticus) were collected
The pooling of protection and control methods often using scoop nets. The samples were then stored
proves to be beneficial. Exchanges information between immediately in plastic containers and transported to the
farmers, producers, and experts working in fish production Laboratory of Biology, Faculty of Mathematics and Natural
chains can be fruitful because parasite problems often have Science (FMIPA), Sebelas Maret University, Surakarta,
unknown impacts that other operators have not yet Indonesia for identification and screening of ectoparasitic
experienced. While anecdotal evidence of parasite protozoa.
problems in aquaculture is sometimes available and shared
among stakeholders, there have been limited studies to help Sex determination and measurements of fish samples
to solve such problems due to the low scientific capacity Fish samples were identified using the guide provided
and the lack of necessary infrastructure for research by Molnar et al. (2019). A ruler was used to measure the
(Mitiku et al. 2018). total length (TL) and standard length (SL) in (cm), while an
This study aims to investigate the occurrence of electronic weight balance was used to measure the weight
ectoparasitic protozoa on farmed Nile tilapia (O. niloticus) of the fish samples in grams. The sex of the fish was
at three reservoirs in Central Java, Indonesia, and to determined by external examination and internal
determine the prevalence, mean abundance, and mean examination of the testes and ovaries as described by
intensity of such parasites. Bruno et al. (2006).

Preparation of the samples and examination for Ecto-


MATERIALS AND METHODS protozoan parasites
The external parts of the fish samples (fins, skin, and
Study period and area gills) were carefully examined and smears were taken from
The study was conducted from July to November 2020 these parts and spread on a dry clean glass slide. Then the
at three different reservoirs in Central Java Province, smears were dried in the air and then fixed with absolute
Indonesia namely; Cengklik, Mulur, and Gajah Mungkur. methanol alcohol for 10 minutes. After that, the smears
The Cengklik reservoir is located in Boyolali District at were stained with freshly prepared Giemsa stained for 30
geographical coordinates of S 07°31’1.11" and E minutes. Then smears were rinsed under tap water and left
110°43’58.22". The Gajah Mungkur reservoir is located in to air dry. Smears were examined for ectoparasitic protozoa
Wonogiri District at S 07°85’50.76" and E 110°91’19.74". under a light microscope connected with a camera Nikon.
The Mulur reservoir is located in Sukoharjo District at S The identification of parasites was carried out following the
07°68’86.13" and E 110°87’73.51". protocol prescribed by Bruno et al. (2006) and Kuchta et al.
(2018).

Mt. Merbabu

1. Cengklik
Mt. Merapi
Surakarta city
Mt. Lawu

2. Mulur

3. Gajah Mungkur

Figure 1. Map of Indonesia in the top and the study area at three reservoirs in Central Java, Indonesia. 1. Cengklik Reservoir, 2. Mulur
Reservoir and 3. Gajah Mungkur Reservoir
KOLIA et al. – Infection of ectoparasitic protozoa on farmed Nile tilapia 1977

Analysis of water physical and chemical parameters RESULTS AND DISCUSSION


Water samples were collected from the depth of 60 cm
from the surface using a water sampler. Water quality The measures on physical and chemical parameters of
parameters such as dissolved oxygen, water temperature, water show that there are no significant differences among
conductivity, transparency, and pH were measured at the the three reservoirs in terms of dissolved oxygen (DO), pH,
same places where fish samples were collected using multi- water temperature, and ammonia concentration (Table 1).
purpose probes. The dissolved oxygen (mg/L) was On the other hand, there is a significant difference at
measured using a digital oxygen meter (OXYGEN p<0.01 in terms of conductivity and transparency with
METER, Model DO-5510) while the water temperature Cengklik reservoir had the highest conductivity and
(°C) was measured by a thermometer. To measure the transparency with 251.00 μ s/cm and 84.67 cm,
transparency, the Sachi disk was used (cm). Electrical respectively. Overall, the mean values of physical and
conductivity (μ s/cm) was determined using a digital chemical parameters are within the permissible range for
conductivity meter (Conductivity STARTER 300c, Nile tilapia fish culture in the cage systems APHA (2017).
OHAUS). Water pH was measured using a pH meter (pH We found that among 189 examined fish samples (63
meter STARTER, OHAUS, version 300). A 600 ml of samples from each reservoir), there were 110 females and
water sample was collected from each zone then and 79 males (Table 2). The results on the examination of
transported to the chemical laboratory for total ammonia parasite infection show that Mulur reservoir had the highest
level analysis (mg/L) using the standard method for water total prevalence of infected fish with 90.4% of the fish
analysis APHA (2017). were infected by parasites, while Gajah Mungkur reservoir
had the lowest prevalence with 58.7% (Table 2).
Data analysis Accordingly, the Mulur reservoir had the highest total
The obtained data were summarized in Microsoft Excel. number of parasites with 1762, while Gajah Mungkur had
The SPSS statistics program v. 21.0 was used for the the lowest with 391 parasites in total.
comparison. Analysis of variance (ANOVA) followed by The results of the measurement on fish size show that
the least significant difference (LSD) test was employed to no statistically significant differences among the mean
compare the data from the three reservoirs. Statistical values of measurements of total length, standard length,
significance was set at (p<0.01). The number of each and weight taken from male or female fishes (Table 3). The
parasite species and the total number of all parasites in each results of the measurements of fishes show that males in
reservoir was calculated to determine the prevalence, mean Mulur reservoir had the highest mean total length of 20.33
abundance, and mean intensity, by using the mathematical cm., while females in Gajah Mungkur reservoir had the
calculations formulated by (Bush et al. 1997) as follows. lowest mean total length of 18.89 cm (Table 3). The results
of the bodyweight of fishes show that males in the
Cengklik reservoir had the highest mean body weight of
165.24 gram. Meanwhile females in the Gajah Mungkur
reservoir had the lowest mean body weight of 149.21 gram
(Table 3).

Table1. The results of physical and chemical parameters of water (mean ±SD) at three reservoir sites in Central Java, Indonesia

Reservoir site
Parameters
Cengklik Mulur Gajah Mungkur Significant
DO (mg/L) 8.13±0.73 7.63±0.38 7.63±0.38 NS
Temperature (0C) 28.07±0.32 28.70±0.26 28.70±0.26 NS
Ammonia (mg/L) 0.48±0.26 1.13±0.08 1.13±0.44 NS
Conductivity (μ s/cm) 251.00±18.50 147.90±4.28 147.90±4.28 **
Transparency (cm) 84.67±2.33 59.00±1.73 59.00±1.73 **
pH 7.48±0.29 7.10±0.08 7.10±0.08 NS

Table 2. Comparison of parasitological data from the three reservoirs in Central Java, Indonesia

Reservoir EF Male Female IF/ non-IF TP (%) TNP


Gajah Mungkur 63 22 41 37 /26 58.7 391
Mulur 63 29 34 57 /6 90.4 1762
Cengklik 63 28 35 52 /11 82.5 1638
Total 189 79 110 146/43 3791
1978 B I OD I V E R S ITA S 22 (4): 1975-1980, April 2021

*Note: EF: Examined fish, IF Infected fish, TP (%): Total prevalence, TNP: Total number of parasites.
Table 3. The size of fish in terms of weight and length (mean ±SD) of males and females at the three reservoirs in Central Java,
Indonesia

Reservoir/ No. of samples TL (cm) SL (cm) FW (g)


Cengklik male (n=28) 19.78±0.49 16.20±0.41 165.24±10.63
Cengklik female (n=35) 19.72±0.46 16.22±0.41 173.60±11.71
Mulur male (n=27) 20.33±0.52 16.69±0.44 176.84±10.68
Mulur female (n=34) 19.69±0.55 16.21±0.47 167.96±11.52
Gajah Mungkur male (n=22) 19.36±0.40 16.08±0.32 153.60±8.26
Gajah Mungkur female (n=41) 18.89±0.42 15.53±0.29 149.21±8.33
Significant NS NS NS
*Note: TL: total length, SL: standard length, FW: fish weight, NS: no significant differences

Table 4. The number of parasite infections (mean ±SD) in gills, fins, and the skin of examined fishes across sexes at the three reservoirs
in Central Java, Indonesia

Reservoir/ no. of samples Gills Fins Skin Total


Cengklik male (n=28) 2.20±0.58 3.20±8.78 11.07±3.55 16.47±4.94
Cengklik female (n=35) 4.86±2.55 8.83±2.83 19.43±6.45 33.11±8.58
Mulur male (n=27) 4.41±1.54 4.33±1.23 11.37±3.14 20.11±4.34
Mulur female (n=34) 3.56±1.01 4.65±1.76 27.21±10.18 35.41±11.84
Gajah Mungkur male (n=22) 1.00±0.47 1.59±0.73 1.64±0.74 4.23±1.31
Gajah Mungkur female (n=41) 1.85±0.75 2.73±1.28 2.68±0.90 7.27±2.20
Significant NS NS ** **
*Note: n: number of examined fish 63/ reservoir, **: significant differences at P<0.01, NS: no significant differences

Table 5. The species of parasite, and the prevalence, mean intensity and mean abundance of each parasite at the three reservoirs in
Central Java, Indonesia

Reservoir
Parasites species Gajah Mungkur Mulur Cengklik
P (%) MI MA P (%) MI MA P (%) MI MA
Tetrahymena corlissi 0 0 0 11.1 1.8 0.2 0 0 0
Apiosoma spp. 17.4 1.5 0.26 1.2 1.6 0.23 7.9 1.4 0.1
Trichodina spp. 50.7 11 5.6 82.5 32.7 27 73 34.8 25.4
Ichthyophthirius multifiliis 0 0 0 0 0 0 15.8 1.6 0.2
Cryptobia spp. 6.3 1.7 0.1 3.1 3 0.09 3.1 2 0.06
Chilodonella spp. 4.7 4.3 0.2 12.6 3.2 0.4 7.9 1.2 0.09
Ambiphrya spp. 0 0 0 0 0 0 4.7 1.6 0.07
*Note; P: Prevalence, MI: Mean intensity, MA: Mean abundance, TNP: Total number of parasites

The results found that there is no significant difference A detailed examination of the prevalence of parasite
(p<0.01) in the number of parasitic infections in gills and infections is presented in Table 5. We found that
fins of males and females across the three reservoirs (Table Trichodina spp. was the most prevalent parasite across the
4). Conversely, there was a significant difference (p<0.01) three reservoirs. A similar result was shown by Indahsari et
in the number of parasitic infections in the skin and the al. (2019) on cultured Nile tilapia in Indonesia that
total number of parasites between males and females from Trichodina spp. was the most common parasite among the
the three reservoirs. The results of the mean values of the other parasite species in their study. In our study, the
total number of parasites show that females in Mulur prevalence of Trichodina spp. was the highest at the Mulur
reservoir had the highest mean values of the total number reservoir (82.5%) with a mean intensity of 32.7 and a mean
of parasites 35.41, while males in the Gajah Mungkur abundance of 27 (Table 5). The second-highest prevalence
reservoir had the lowest mean values of the total number of was recorded at the Cengklik reservoir (73%) with a mean
parasites 4.23 (Table 4). Accordingly, the females had the intensity and mean abundance of 34.8 and 25.4,
highest mean values of parasites than males in the three respectively. The lowest prevalence was recorded in the
reservoirs in gills, fins, and skin with 4.86, 8.83, and 27.21 Gajah Mungkur reservoir (50.7%) with a mean intensity of
respectively. 11 and a mean abundance of 5.6.
KOLIA et al. – Infection of ectoparasitic protozoa on farmed Nile tilapia 1979

Human activities in and around the reservoirs might recorded prevalence was higher than the recorded
cause poor water quality due to the accumulation of high prevalence of 3% in the dry season and lower than the
organic matter load which favors the reproduction and recorded prevalence of 61% in the rainy season by
proliferation of Trichodina spp. The protozoan parasite (Arguedas et al. 2017).
Trichodina spp. in water bodies is an indicator of poor The protozoan Ambiphrya spp. was recorded only at the
water quality. Thus, further seasonal studies should be done reservoir Cengklik from the gills of Nile tilapia. The
in those reservoirs considering abiotic and biotic factors recorded prevalence was 4.7%, with a mean intensity of
such as stocking fish density, nutrients, and other water 1.6, and a mean abundance of 0.07. A similar species of
quality parameters. this parasite was isolated from the same host Nile tilapia in
The protozoan Apiosoma spp. was observed at the three Saudi Arabia (Abdel-Baki et al. 2014). Moreover, this
reservoirs from the gills of the Nile tilapia. This ciliated parasite also was recorded from Nile tilapia in Egypt
protozoan was recorded at the Gajah Mungkur reservoir (Ashmawy et al. 2018). However, this is the first record of
with a prevalence of 17.4%, and mean intensity and mean this parasite from cultured Nile tilapia in Central Java.
abundance of 1.5 and 0.26, respectively. At Cengklik The flagellated protozoan Cryptobia spp. was recorded
reservoir, it was recorded with the prevalence of 7.9%, in all three reservoirs from the gills, skin, and fins. The
mean intensity and mean abundance of 1.4 and 0.1, recorded prevalence was 6.3%, 3.1% and 3.1% at Gajah
respectively. The lowest prevalence (1.2%) was recorded at Mungkur, Mulur and Cengklik, respectively. The mean
Mulur reservoir with a mean intensity of 1.6 and a mean intensity recorded were 1.7 at Gajah Mungkur, 3 at Mulur,
abundance of 0.23. The infection by Apiosoma spp. in gills and 2 at Cengklik. While the mean abundance recorded
could result in disrupting gas exchange through the were 0.1, 0.09, and 0.06 at Gajah Mungkur, Mulur, and
respiratory epithelium, and then mortalities following Cengklik. However, some species of this parasite are
massive colonization of the gills. However, the recorded pathogenic for fish, especially fingerling (Bruno et al.
prevalence in this study was lower than that reported for 2006). Thus, further attention should be given to control
the same host grown in Costa Rica with a prevalence of this parasite.
84% in the dry season and 100% in the rainy season The ciliate protozoan Tetrahymena corlissi was
(Arguedas et al. 2017). Moreover, the recorded observed just in the Mulur reservoir from the gill of the
prevalence's in this study was lower than that reported Nile tilapia. The recorded prevalence was 11.1% with a
prevalence with 28.2% % from freshwater fish in West mean intensity of 1.8 and a mean abundance of 0.2.
Azerbaijan, northwest of Iran by (Ebrahimi et al. 2018). However, this parasite has been reported from a variety of
The ciliated protozoan Ichthyophthirius multifiliis was freshwater fish species, and the infection may cause
observed only at the Cengklik reservoir in the gills and the general debilitation, skin hemorrhage, and exophthalmia to
skin with a prevalence of 15.8%, a mean intensity of 1.6, both tropical and temperate species (Bruno et al. 2006).
and a mean abundance of 0.2 (Table 5). Generally, this In this study seven species of ectoparasites were
parasite infects the gills and skin of fish and causes ‘Ich’ or identified namely: Tetrahymena corlissi, Apiosoma spp.,
white spot disease and causes high mortality rates in both Trichodina spp., Cryptobia spp., Chilodonella spp.,
cultured and wild populations of fish. Poor water quality Ambiphrya spp., and Ichthyophthirius multifiliis from the
and fish stress are critical factors for the spread of this gills, fins, and skin of Nile tilapia. The output from the
parasite on Nile tilapia. The current investigation revealed study showed a significant difference at p<0.01 in the total
that this parasite was recorded from the gills and skin of the number of parasites among the reservoirs. The total number
fish that weighed between 220-245g and total length of ectoparasitic protozoa was the highest at Mulur reservoir
between 23-25cm. A similar study was recorded by Alves compared to the other two reservoirs (Cengklik and Gajah
et al.(2000) who indicated I. multifiliis isolated from gills Mungkur). That means the location of the reservoir affects
of O. niloticus was positively correlated with weight and the occurrence of ectoparasitic protozoa. The water in the
lengths of fish. However, the differences in the occurrence reservoir Mulur was not suitable for drinking because of
of this parasite for the same host between the different human activities around the reservoir in contrast to the
reservoirs may be due to the balance between the Gajah Mungkur reservoir. Although the physical and
performance of the parasites and the host immune system. chemical parameters were within the optimum range for
Chilodonella spp. was found at all three reservoirs from Nile tilapia culture under the cage system, controlling
the skin and gills of Nile tilapia. Furthermore, this parasite water quality could be challenging in open waters.
recorded the highest prevalence at reservoir Mulur (12.6 Sustainable management for fishes should consider abiotic
%) with a mean intensity of 3.2 and a mean abundance of factors such as water quality conditions and other biotic
0.4. This was followed by a prevalence of 7.9 % at factors to maintain the health of Nile tilapia. The
Cengklik reservoir with a mean intensity of 1.2 and mean infestation level of ectoparasitic protozoa in this study
abundance of 1.2. Meanwhile, the lowest prevalence (4.7 arguably will not pose a significant threat to the Nile tilapia
%) was recorded at reservoir Gajah Mungkur with a mean in the cages since no fish mortality was observed.
intensity of 4.3 and a mean abundance of 0.2. However, the However, critical attention should be given to the cages by
recorded prevalence by Chilodonella spp. in this study was employing good management practices to prevent disease
lower than the recorded prevalence by (Banu and Khan outbreaks caused by the protozoan parasites. Hence, the
2004) who indicated that the prevalence of Chilodonella findings from this research can be used for more effective
spp. was 24.2% in July and 16.7% in June. Moreover, our
1980 B I OD I V E R S ITA S 22 (4): 1975-1980, April 2021

control measures of parasitic infestation in cage systems at Biu AA, Diyaware MY, Yakaka W, Joseph E. 2014. Survey of parasites
infesting the Nile tilapia (Oreochromis niloticus) from. Niger J Fish
these reservoirs. Aquac 2: 6-12.
Bruno DW, Nowak B, Elliott DG. 2006. Guide to the identification of fish
protozoan and metazoan parasites in stained tissue sections. Dis
ACKNOWLEDGEMENTS Aquat Org 70 (1-2): 1-36.
Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets
ecology on its terms: Margolis et al. Revisited. J Parasitol 83 (4): 575-
The authors thank the head of the Bioscience 583. DOI: 10.2307/3284227.
Department, Laboratory of Biology, MIPA Integrated Lab., Ebrahimi M, Nematollahi A, Samiei A, Golabi M. 2018. Ectoparasitism
and Central Lab at the Sebelas Maret University, Indonesia on freshwater fish in West Azerbaijan, northwest of Iran. Comp Clin
Pathol 27 (2): 353-356. DOI: 10.1007/s00580-017-2598-9.
for providing necessary laboratory facilities. We also Indahsari M, Kismiyati, Ulkhaq MF. 2019. Prevalence and Intensity of
gratefully acknowledge the financial assistance from KNB ectoparasites of Tilapia (Oreochromis niloticus) in ponds with low,
Scholarship (M.Sc. scholarship) awarded to Waleed Krpos. medium, and high stocking density. IOP Conf Ser: Earth Environ Sci
We are very grateful to Balai Besar Wilayah Sungai 236 (1): 012108. DOI: 10.1088/1755-1315/236/1/012108.
Kuchta R, Basson L, Cook C, Fiala I, Bartošová-Sojková P, Řehulková E.
Bengawan Solo (BBWSBS) staff for providing the 2018. A systematic survey of the parasites of freshwater fishes in
necessary facilities to collect the fish samples. Africa. In: Scholz T, Vanhove MPM, Smit N, Jayasundera Z, Gelnar
M (eds). A Guide to the Parasites of African Freshwater Fishes. Abc
Taxa, Belgium.
Mitiku MA, Konecny R, Haile AL. 2018. Parasites of Nile tilapia
REFERENCES (Oreochromis niloticus) from selected fish farms and Lake Koftuin
central Ethiopia. Ethiopian Vet J 22 (2): 65. DOI: 10.4314/evj.v22i2.6
Abdel-Baki AAS, Gewik MM, Al-Quraishy S. 2014. First records of Molnar K, Szekely C, Lang M. 2019. A Field Guide to Warm Water Fish
Ambiphrya and Vorticella spp. (Protozoa, Ciliophora) in cultured Nile Diseases in Central and Eastern Europe, the Caucasus, and Central
tilapia (Oreochromis niloticus) in the central region of Saudi Arabia. Asia. FAO Fisheries and Aquaculture Circular, Ankara, Turkey.
Saudi J Biol Sci 21 (6): 520-523. DOI: 10.1016/j.sjbs.2014.01.002. Pantoja WM, Neves RL, Dias RM, Marinho GR, Montagner D, Tavares-
Alves DR, Luque JL, Paraguassú AR. 2000. Ectoparasitos da Tilápia dias M. 2012. Protozoan and metazoan parasites of Nile tilapia
nilótica Oreochromis niloticus (Osteichthyes: Cichlidae) da Estaçâo Oreochromis niloticus cultured in Brazil. Rev MVZ Córdoba 17 (1):
de Piscicultura da UFRRJ. Rev Univ Rural Ciênc Vida 22: 81-85. 2812-2819.
APHA, AWWA, WEF. 2017. 3120 B. Inductively Coupled Plasma (ICP) Santos R, Pabon A, Silva W, Silva H, Pinho M. 2020. Population structure
method. Standard Methods for the Examination of Water and and movement patterns of blackbelly rosefish in the NE Atlantic
Wastewater, American Public Health Association, Washington DC. Ocean (Azores archipelago). Fish Oceanogr 29 (3): 227-237. DOI:
Arguedas CD, Ortega SC, Martínez CS, Astroza CA. 2017. Parasites of 10.1111/fog.12466.
Nile Tilapia larvae Oreochromis niloticus (Pisces: Cichlidae) in Suliman EAM, Al-Harbi AH. 2016. Prevalence and seasonal variation of
concrete ponds in Guanacaste, Northern Costa Rica. UNED Res J 9 ectoparasites in cultured Nile tilapia Oreochromis niloticus in Saudi
(2): 313-319. DOI: 10.22458/urj.v9i2.1904. Arabia. J Parasit Dis 40 (4): 1487-1493. DOI: 10.1007/s12639-015-
Ashmawy K, Hiekal F, AboAkadda S, Laban N. 2018. The inter- 0717-6.
relationship of water quality parameters and fish parasite occurrence. Tran N, Rodriguez UP, Chan CY, Phillips MJ, Mohan CV, Henriksson
Alexandria J Vet Sci 59 (1): 97-106. DOI: 10.5455/ajvs.299584. PJG, Koeshendrajana S, Suri S, Hall S. 2017. Indonesian aquaculture
Banu ANH, Khan MH. 2004. Water quality, stocking density, and futures: An analysis of fish supply and demand in Indonesia to 2030
parasites of freshwater fish in four selected areas of Bangladesh. Pak J and role of aquaculture using the AsiaFish model. Mar Policy 79: 25-
Biol Sci 3 (1028-8880): 436-440. DOI: 10.3923/pjbs.2004.436.440. 32. DOI: 10.1016/j.marpol.2017.02.002.

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