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Profile of ectoparasites and biometric condition of snakehead (Channa striata Bloch 1793) collected from different habitats

1 Department of Fisheries Resources Utilization, Faculty of Marine and Fisheries, Universitas Syiah Kuala, Banda Aceh 23111, Indonesia 2 Department of Biology, Faculty of Science and Technology, Universitas Islam Negeri Ar-Raniry Banda Aceh 23111, Indonesia. 3 Center for Aquatic Research and Conservation (CARC), Universitas Islam Negeri Ar-Raniry Banda Aceh 23111, Indonesia. 4 Graduate School of Mathematics and Applied Science, Universitas Syiah Kuala, Banda Aceh 23111, Indonesia. 5 Department of Aquaculture, Faculty of Fisheries, Abulyatama University, Aceh Besar 23372, Indonesia. 6 Department of Aquaculture, Faculty of Marine and Fisheries, Universitas Syiah Kuala, Banda Aceh 23111, Indonesia


Introduction
Snakehead (Channa striata Bloch 1793) is a freshwater fish with high economic value for Indonesian (Cahyanti et al., 2021). In addition to the high selling price (from IDR 35,000 to IDR 75,000 per kg), this fish also has a delicious taste and high nutritional content compared to other freshwater fish. The nutritional content in snakehead reported consists of 19.71-19.85% protein, 0.44-2.56% fat, albumin, mineral, and essential amino acids (Chasanah et al., 2015). Rahayu et al. (2016) suggested that snakehead also contains bioactive proteins that can accelerate the formation of new cells during postoperative wound healing.
The ability of snakeheads to defend against parasites is highly dependent on their health and environmental conditions (Ode, 2014). The poor environmental condition might cause stress in fish, impacting the body's decreased defense mechanisms and being vulnerable to parasitic infections. Nova et al. (2015) stated that parasitic infection in fish could occur due to the interaction of three components: weak hosts, virulent pathogens, and poor environmental quality.
According to Mulia (2007), ectoparasite infection can traverse to an acute death without preceding symptom. Besides, ectoparasite infection is also one of the predisposing factors for other more lethal organisms. The chronic level of ectoparasite infection irritates external organs such as the gill and skin. The alteration of fish gill due to ectoparasites infection causes a disturbance in respiration and osmoregulation processes. In addition, ectoparasites infection on the skin has decreased the fish immunity and led to the intrusion of other parasitic organisms. If this condition continues, it will adversely impact the lower growth rate, even death (Mood et al., 2011).
To date, studies related to the comparison of ectoparasites that infect snakeheads from different habitats and their relationship to biometric conditions have not been optimally investigated. Paddy fields, swamps, and ditches are habitats for snakeheads that have different characteristics. Specifically, the swamp has puddle fluctuating conditions for a certain period, and the paddy field has streams/puddles that have been mixed with agricultural fertilizers and pesticides. At the same time, a ditch is identically used as a place for waste disposal, especially household waste. Thus, this present study aimed to investigate the prevalence, intensity, dominance, and predilection of ectoparasites on snakehead fish collected from ditches, paddy fields, and swamps and correlate them with biometric conditions. This study has provided valuable information as a part of the preventive and responsive efforts to monitor snakehead health.

Fish sample preparation and ectoparasite identification
A total of 30 samples of snakehead fish were collected from each habitat through direct purchases from local fishermen. The fish samples were kept in labeled plastic and then transported into the laboratory for further identification. The physicochemical parameters of water in each habitat were measured, including temperature, pH, dissolved oxygen, and ammonia. The temperature and dissolved oxygen were measured using DO meter (Lutron YK-2005WA; Taiwan), and pH was measured using the digital pH meter (ATC pH-2011; Romania). Ammonia was measured using Wastewater Treatment Photometer (HANNA HI-83214; United States of America).
The observation of ectoparasite was carried out in the skin, fins, and gill of snakehead based on Fautama et al. (2019) protocol. Briefly, the fish was sacrificed by pinning with a needle in the neurocranium part of the fish. The mucus from the lateral body of the fish was taken by using a Depik Jurnal Ilmu-Ilmu Perairan, Pesisir dan Perikanan Volume 10, Number 3, Page 284-292 Zulfahmi et al. (2021) scrapping method. In addition, ectoparasites in the fins were observed by placing a slice of the fish fin (dorsal, caudal, ventral, and pectoral fin) into an object-glass that has been dripped with distilled water. The observation of ectoparasites in the gill was performed after separating the gill filament from the operculum. Ectoparasites were observed under a light microscope with a slight magnification (40x) to a large magnification (100x). The identification of ectoparasites found was done by comparing the similarity of ectoparasite morphology with several related references such as Kabata (1985), Noble and Noble (1989), and Nurcahyo (2014).

Research parameters
The parameters observed in this research were ectoparasite profile and biometric condition of fish. The ectoparasite profile parameters included prevalence, intensity, dominance, and predilection of organ.. Meanwhile, the parameters of the biometric conditions were the length-weight relationship, the distribution of length and weight classes, and condition factors. The prevalence, intensity, and dominance were calculated as follow (Kabata, 1985): The length-weight relationship and condition factor of fish were measured with Linear Allometric Model (LAM) approach based on Effendie (1997) as follow: W is the weight of fish (g), L is the total length of fish (mm), a is constant, and b is an exponential expressing the relation between length and weight. The condition factor (K) was measured based on the following formula (Okgerman, 2005):

Data analysis
The data were separated based on the habitat and condition of fish (healthy fish, infected fish, and total fish). The infection and infestation level (prevalence dan intensity) of parasites in each habitat was determined based on Williams and Williams (1996). Besides, the biometric condition was analysed descriptively.

Ectoparasites profile
Five Species of ectoparasites were identified up to the genus level, including Tetrahymena sp., Epistylis sp., Trichodina sp., Dactylogyrus sp., and Gyrodactylus sp. (Figure 2). Taxonomically, the ectoparasites found are divided into two phyla (Platyhelminthes and Protozoa), two classes (Trematoda and Ciliata), four orders (Gyrodactylidea, Dactylogyridea, Petrichida, and Hymenostomatida), and five familiae (Gyrodactylidae, Dactylogyridae, Trichodinidae, Tetrahymenidae, and Epistylidae). Tetrahymena sp. is an ectoparasite included in ciliated protozoa. This parasite possesses an oval body shape surrounded by cilia that are helpful in movement. The body is transparent so that the cell organelles are easily visible (Figure 2A). Ectoparasite Epistylis sp. is a protozoan with a cylindrical shape, like stemmed bell, and a transparent body ( Figure 2B). Trichodina sp. has a perfectly round transparent body shape like a plate that constantly rotates in the middle and is filled with serrations. The outermost layer of the body of Trichodina sp. is filled with cilia ( Figure 2C). Dactylogyrus sp. is an ectoparasite included in Platyhelminthes. It possesses a round, flat and elongated body shaped. It has a plate at the posterior used to attach to the host and has a sucker located near the anterior end. ( Figure 2D). Gyrodactylus sp. was found to have a body shape identical to Dactylogyrus sp. But, Gyrodactylus sp. has hooks on the anterior part, which attach themselves to the host (Figure2E).

Prevalence and intensity of ectoparasites based on the habitat
The total ectoparasites infecting snakehead in the three habitats amounted to 573 individuals. The ditch habitat has the highest prevalence value by 76.7%, while paddy field habitat has the lowest prevalence value by 53,3% (Table 1). Based on the criteria of ectoparasite prevalence level referring to Williams and Williams (1996), ditches and swamps habitat are in moderate infection and infestation (70-89%). Meanwhile, the paddy field habitat is classified as the most frequent infection and infestation (50-69%).
Ectoparasites intensity values in the three habitats range from 5.75 ectoparasites/fish up to 15.4 ectoparasites/fish. Ditch habitat has the highest intensity value, followed by swamp habitat and ditch habitat, which are 15.4, 6.05, and 5.75 ectoparasites/fish, respectively, as shown in Table 1 below. Nevertheless, based on the criteria for the intensity level of ectoparasites infection, Williams and Williams (1996) suggest ditch and swamp habitats are within the moderate infection category (6 -55 ectoparasites/fish). In contrast, the ectoparasite infection at paddy field habitat is within the low category (<6 ectoparasites/fish).

Dominance of ectoparasites based on the habitat
Of the five identified ectoparasites, four were found in swamp habitats, while only three species were found in ditch and rice field habitats. Tetrahymena sp. and Epistylis sp. ectoparasites were detected in all habitats. Trichodina sp. ectoparasite was detected at ditch and paddy field habitats, while, Gyrodactylus sp. and Dactylogyrus sp. ectoparasites were only found in swamp habitat. The highest dominance of ectoparasites in each habitat included Tetrahymena sp. in ditch and swamp habitats and Epistylis sp. in the paddy field habitat. In the ditch habitat, the highest ectoparasite species dominance was 85.59%. Meanwhile, in the paddy field and swamp habitat, the dominance value was under 50%, Depik Jurnal Ilmu-Ilmu Perairan, Pesisir dan Perikanan Volume 10, Number 3, Page 284-292 Zulfahmi et al. (2021) which were 34.78% and 49.61%, respectively (Table  2).

Predilection of ectoparasites
Out of the three organs observed, the gill was the most vulnerable organ. All types of ectoparasites were detected to infect the gill. In comparison, the skin and fin were only infected by two species of ectoparasites, namely Tetrahymena sp. and Dactylogyrus sp. (infecting skin) and Trichodina sp. and Epistylis sp. (infecting fins). Tetrahymena sp. became the most dominant ectoparasites attacking the gills and skin, with 270 and 128 individuals, respectively. Likewise, Epistylis sp. ectoparasite became the most dominant ectoparasite attacking the fins (Table 3). Dactylogyrus sp. ectoparasites were the fewest found, as many as four individuals. There were no ectoparasites that simultaneously infected the three organs observed (skin, fins, and gills).

Biometric condition
A total of 60 (66.7%) snakehead examined was infected with ectoparasites. The average weight and length of infected snakehead fish were 161.9±31.3 g and 250.33±52.5 mm, respectively. While, for the healthy snakehead fish were 165.3±36.8 g and 251.28±63.3 mm. Healthy and infected snakehead had almost identical condition factor values, which were 1.006 and 1.011, respectively (Table 4). All snakehead collected from various habitats (both healthy and infected) had negative allometric growth patterns (b<3). However, in general, infected snakehead had a lower b coefficient value. Only infected snakehead fish from ditch habitats have a coefficient b value identical to healthy snakehead. The coefficient b value of healthy snakehead fish ranged from 2.321 to 2.537. Whereas, the coefficient b value of snakehead infected with ectoparasites was in the range of 2.163 -2.535. The lowest b coefficient value of snakehead infected with ectoparasites was observed in the paddy field habitat, which was 2.163. In contrast, the highest b coefficient value of the healthy snakehead was observed in the swamp habitat, which was 2,535. (Figure 3).    Zulfahmi et al. (2021) and 15 individuals, respectively ( Figure 4B-D). The lowest number of infections was obtained in snakehead with a weight range of 177.2-207.2 g and a length range of 188.5-198.5 mm. Similar results were also recorded in each habitat where snakehead with a weight range of 115.2-145.2 g had the highest infection rate compared to other weight size ranges. The predominat snakehead infected with ectoparasites in paddy field was in the length range of 258.5-268.5 mm, while in ditch and swamp habitats were in the range of 218.5-228.5 mm ( Figure 4A-C).

Physical and chemical parameters of waters
The analysis of physico-chemical parameters of the waters showed that temperature, pH, dissolved oxygen, and ammonia content in the three habitats were respectively in the range of 30.5±0.3-32.3±0.2 o C, 6.9±0.15-8.2±0.15, 2.2±0.15-4.5±0.1 mg/L, and 0.5±0.01-1.05±0.05 mg/L. Three of four parameters of the waters measured in the ditch habitat have exceeded the tolerance range for snakehead, including temperature, pH and dissolved oxygen. Meanwhile, in the paddy field and swamp habitats, there are no parameters were exceeded the ideal value range ( Table 5). The highest values of temperature, pH, ammonia and lowest dissolved oxygen levels were detected in the ditch habitat, which was 32.3±02 o C, 8.2±0.15, 1.05±0.05 mg/L, and 2.2±0.15 mg/L, respectively.

Discussion
Five species of ectoparasites identified in this study (Tetrahymena sp., Epistylis sp., Trichodina sp., Dactylogyrus sp., and Gyrodactylus sp.) were also reported to infect various freshwater fish, brackish water fish to seawater fish. Several of them were catfish (Clarias gariepinus) (Fautama et al., 2019), panga (Pangasius hypophthalmus) (Islami et al., 2017), goldfish (Carassius auratus) (Anshary, 2008), nile tilapia (Oreochromis niloticus) (Rahmi, 2012), milkfish (Chanos chanos) (Riko et al., 2012) and tiger grouper (Epinephelus fuscoguttatus) (Siswoyo and Hendrianto, 2011). Hardi (2015) asserts that several factors affecting the abundance and diversity of parasites in the waters include poor water quality, carrier vectors, and unhealthy cultivation media management. From the five ectoparasites identified, four of them (Trichodina sp., Dactylogyrus sp., Epistylis sp. and Gyrodactylus sp.) were also reported to infect snakehead fish in many regions in Indonesia. Trichodina sp. also infected snakehead fish from irrigation habitat in Aceh Besar Regency (Umara et al., 2014). Dactylogyrus sp. and Gyrodactylus sp. infested snakehead from paddy fields, swamps, and cultivation media in Yogyakarta area (Fitriani et al., 2019). Epistylis sp. ectoparasite had been found in snakehead from tributary habitats in Sidoarjo area (Salam and Hidayati, 2017). Only Tetrahymena sp. have not been previously reported to infect snakehead from other regions in Indonesia. However, this ectoparasite has been reported to infect several different fish species, such as tiger grouper (Epinephelus fuscoguttatus) and goldfish (Carrasius auratus) (Siswoyo and Hendrianto, 2011;Haryono et al., 2016). In this study, Dactylogyrus sp. and Gyrodactylus sp. are only recorded at swamp habitat. Consequently, swamp habitats have a higher diversity of ectoparasites compared to other habitats. Several studies inform that monogenean parasites are more commonly found in wetland areas (including swamps) with still water and low pollution levels (Krause et al. 2010;Morales-Serna et al., 2019). Ansyari et al. (2020) also revealed a similar result where Dactylogyrus sp. was only observed in swamp areas compared to other sampling locations such as a river. This might occur due to stream water conditions in, rivers and ditches, while the swamp has a stagnant water condition.
To date, studies related to ectoparasites in snakehead fish, mainly from Indonesia's territory, are still limited. Thus, this opens up opportunities for the discovery of various other types of ectoparasites. Tetrahymena sp. has a high potential to infect snakehead fish due to its wide distribution and breed rapidly. In this study, the presence of Tetrahymena sp. is suspected to be caused by environmental factors that support their proliferation and growth. Moreover, Tetrahymena sp. became the dominant ectoparasite infecting snakehead from ditch and swamp habitats with values of 85.59% and 49.61%, respectively. The ditch habitat had a higher prevalence and intensity of ectoparasites than other two habitats. This is assumed to be highly correlated with the value of water's physical and chemical parameters in the ditch habitat. Ditch habitats have temperatures, pH, dissolved oxygen levels exceeding the optimum snakehead survival and growth range. The poor quality of water in the ditch is strongly affected by household waste input. According to Sumantri and Cordova (2011), household waste originating from cleaning materials such as detergents, soaps, and shampoos contains inorganic nitrogen (NH3, NH4OH, NO2, NO3), which can be a source of ammonia in the waters. Therefore, high levels of ammonia can increase the pH value and decrease the dissolved oxygen value (Monalisa and Minggawati, 2010). Leibowitz et al. (2005) revealed that poor water quality can improve the susceptibility of fish to parasitic infections. High ammonia content can reduce fish immunity, while the high content of organic matter becomes nutrients for parasites growth. The study by Faggio et al. (2014) and Dawood et al. (2021) proves that exposure to ammonia can decrease the value of blood protein, albumin, and globulin, affecting the decrease of fish immunity levels. In fact, low immunity is one factor that facilitates the parasite to infect fish.
Furthermore, snakehead gills are the most vulnerable organs to ectoparasite infection compared to fins and skin. Similarly, it was also reported in catfish (Clarias gariepinus) and hairtail fish (Trichiurus lepturus) (Fautama et al. 2019;Rahmat et al., 2020). This might occurs due to several factors, including 1) Gill is one organ with great contact with the environment. 2) During the respiration process, the gills actively filter water that enters the oral cavity so that it has the potential to attach to ectoparasites. 3) In the gills, there are blood vessels that become a source of nutrition for ectoparasites. On the one hand, ectoparasite infection caused gill degeneration characterized by hemorrhage, excessive mucus production, and histopathology (Iwanowicz, 2011;Suliman et al., 2021). Additionally, gill morphological changes due to infection of ectoparasites can disturb the respiration's performance, adversely impacting fish growth (Nisa et al., 2021).
Infected snakehead tend to had a lower average weight and length value than healthy snakehead. Based on habitat, swamps had more parasites species with moderate infection rates. Therefore the negative effect of parasitic infection on the growth coefficient of snakeheads was more visible than normal fish. To date, studies related to the impact of parasites infection on fish growth coefficients are still rare. This study indicates that besides the intensity rate, the type of parasite that infects might also affect fish's growth rate. Based on their size, snakehead fish with low weight and longer size tends to be more vulnerable to ectoparasite infection compared to other sizes. This is also in line with the finding of Finley and Forrester, 2003;Muchlisin et al., 2014, where Coryphopterus glaucofraenum fish with lower weight and Tor tambra fish with longer size were also most infected by ectoparasite. In addition, Hardi (2015) stated that fish that have not yet reached the adult stage (generally identical to low body weight) have an immature immune system, so they are more susceptible to ectoparasite infection. Adversely, in terms of length, ectoparasite infection probably correlates with the attachment area on the fish body, where longer fish provides more space for parasites to infect (Alifuddin et al., 2003).

Conclusion
A total of 573 ectoparasites were detected infecting snakehead from the three habitats. Of the five types of ectoparasites that have been identified A C D B Depik Jurnal Ilmu-Ilmu Perairan, Pesisir dan Perikanan Volume 10, Number 3, Page 284-292 Zulfahmi et al. (2021) as Tetrahymena sp., Epistylis sp., Trichodina sp., Dactylogyrus sp., and Gyrodactylus sp, Tetrahymena sp. infection in snakehead fish was firstly reported. The ditch habitat had the highest prevalence level by 76.7%, whereas the paddy field habitat had the lowest one by 53.3%. The ectoparasite intensity values in the three habitats were ranging from 5.75 to 15.4 ectoparasites/fish. Ditch habitat had the highest intensity value, followed by swamp habitat and ditch habitat. The ectoparasites of Tetrahymena sp. and Epistylis sp. were detected in all habitats. Ectoparasite of Trichodina sp. detected at ditch and paddy field habitats. In contrast, Gyrodactylus sp. and Dactylogyrus sp. were only found in swamp habitats. All types of ectoparasites were detected to infect the gills, while the skin and fins were only infected by each of the two types of ectoparasites. Regression analysis showed that infected snakehead tend to have a lower growth coefficient compared to healthy snakehead. Snakehead with a weight range of 115.2-145.2 g and a length range of 258.5-268.5 mm tend to be more vulnerable to ectoparasite infection compared to other sizes. Further research related to the impact of ectoparasite infection on physiological performance and its relationship to snakehead growth is highly recommended.