ABSTRACT

Objective:

The aim of the present study was to determine the prevalence of parasitic infections in aquarium fish sold in local pet shops.

Methods:

Totally 502 fish samples from 8 species were obtained from 7 pet shops. Native preparations were prepared from the gills, fins, skin, intestines, and internal organs of fish and examined under a light microscope.

Results:

It was detected at the end of the study that 62.7% of the fishes examined were infected with one or more parasite species. Among the fish examined, 28.9% were infected with a single parasite, whereas 33.9% were infected with mixed parasites. Chilodonella sp. identified as the most common species. Other species detected included Trichodina sp., Piscinoodinium sp., Ichthyobodo sp., Ichthyophthirius multifiliis, Apiosoma sp., Epistylis sp., Vorticella sp., Gyrodactylus sp., Dactylogyrus sp., Capillaria sp., Camallanus sp., metacercariae, and nematode larvae, Argulus sp., Philodina sp., Euchlanis sp., Aelosoma sp., and Tetrahymena.

Conclusion:

The importance of the present study is that highest number of parasite species were detected in aquarium fish sold in pet shops in Türkiye. The aquarium owners should pay attention to the cleanliness of the aquarium water in order to reduce the rate of parasitic infection in fish; when new fish are purchased, they should be taken from reliable sources, and the quarantine process should be observed.

Keywords: Aquarium, arthropods, fish, helminths, protozoa

INTRODUCTION

In recent years, there has been a rapid increase in aquarium fish farming in Türkiye, and it has become an important business line. There are many enterprises that breed or sell aquarium fish in each province of Türkiye. However, people raise aquarium fish as ornamental animals in their homes and workplaces.

Parasitic diseases may spread rapidly among aquarium fish and cause significant economic losses if necessary precautions are not taken (1). There are limited number of studies on determination of parasites in aquarium fish in Türkiye. Chilodonella sp., Trichodina sp., Ichthyophthirius multifiliis, Ichthyobodo sp., Hexamita sp., Myxosporidia sp., Dactylogyrus sp., Gyrodactylus sp., Thaparocleidus sp., Centrocestus metaserkeri, Lernaea sp., Argulus sp., Camallanus sp., Capillaria sp., Ambiphyra sp., Epistylis sp., Tetrahymena, Vorticella, Philodina, Chaetonotus sp., Euchlanis sp., (2), Acanthocephala sp., Sciadicleithrum variabilum (3) species were detected in aforesaid studies (4-11).

The aim of the present study was to determine the prevalence of parasitic infections in aquarium fish sold in local pet shops.

METHODS

The fish samples used in the study were collected from pet shops located in Kırıkkale. Approvals for the collection of samples and the carrying out the study were obtained from Kırıkkale University Animal Experiments Local Ethics Committee (E-608221397-010.99-74220 letter). Fish samples were taken with the approval of the pet shop owner. Petshops were visited on a daily basis, and the dead fish in the aquariums were duly delivered to Kırıkkale University Faculty of Veterinary Medicine, Routine and Epidemiology Laboratory in separate containers. Totally 502 dead fish were collected from 7 pet shops during the study period. Such dead fish belonged to goldfish (Carassius auratus), Lepistes (Poecilia reticulata), angelfish (Pterophyllum scalare), Beta fish (Betta splendens), stringray fish (Hypostomus sp.), molly fish (Poecilia sphenops), neon tetra fish (Paracheirodon innesi) and cichlid fish (Cichlidae) species.

The preparations were prepared by taking scrapings from the gills, fins, skin, intestines, and internal organs, separately through a slide from the fish delivered to the laboratory on the same day. The preparations were examined under the light microscope and identified at the genus level using the relevant literature, which was positive for parasites (12,13).

Statistical Analysis

All data were analyzed with frequency table. SPSS (IBM SPSS for Windows ver. 22) statistical package program was used for analysis. Infection rates are calculated as a percentage.

RESULTS

Among 502 fish examined during the study, 62.7% of these fish were found infected at least with one parasite types. Totally 19 parasite species were detected in these fish. Other species detected were protozoans including Chilodonella sp., Trichodina sp., Piscinoodinium sp., Ichthyobodo sp., I. multifiliis, Apiosoma sp., Epistylis sp., Vorticella sp.; helminths including Gyrodactylus sp., Dactylogyrus sp., Capillaria sp., Camallanus sp.; metacercariae, and nematode larvae; arthropods including Argulus sp., Rotifera including Philodina sp., Euchlanis sp., annelidae including Aelosoma sp., and a free-living ciliata, Tetrahymena sp. (Table 1).

Table 1

The fish which were infected with a single parasite was 28.9% of the fish examined and 46% of the fish that were positive for parasites. Among the fish samples, 18.3% were found infected with two parasite types, 7.0% were found infected with three parasite types, 5.4% were found infected with four parasites, 2.8% were found infected with five parasites, and 0.4% were found infected with six parasites. Majority of the fish that were positive for the parasite were infected with a single agent (Table 2).

Table 2

Chilodonella sp., Trichodina sp., Piscinoodinium sp., Ichthyobodo sp., Ichthyophthirius multifiliis, Gyrodactylus sp., Dactylogyrus sp., Nematoda larvae, metacercaria, Vorticella sp., Philodina sp., Euchlanis sp., and Aelosoma sp. were detected from gill samples; Trichodina sp., Piscinoodinium sp., Chilodonella sp., Capillaria sp., Camallanus sp., and nematod larvae from viscera and intestinal samples; Chilodonella sp., Trichodina sp., Piscinoodinium sp., Ichthyobodo sp., I. multifiliis, Apiosoma sp., Epistylis sp., Gyrodactylus sp., Dactylogyrus sp., Argulus sp., Philodina sp., Euchlanis sp., Tetrahymena sp. from skin scratces were detected (Figure 1).

Figure 1

DISCUSSION

Aquarium and aquarium fishing has become a hobby for people today and a sector where significant gains are made commercially. Therefore, the number of studies on aquarium fish breeding and diseases is increasing in many parts of the world as well as Türkiye. Parasitic diseases are the diseases that are emphasized a lot because they may spread in a short time in aquarium fish and cause symptoms that may lead to the death of the fish.

Studies have been carried out on parasites of aquarium fish in different parts of the world in recent years. The presence of parasites at different rates was determined in those studies. The rate of parasitic infection was found between 43.3 and 90.90% in studies conducted on aquarium fish in Türkiye (4,9). The rate of parasitic infection in ornamental fish was found between 69.1% and 100% (14,15) in Pakistan, 22.5% (16) in Brazil, and between 26.33% and 95.0% in Iran (17,18). At least one parasite species was found in 62.7% of the aquarium fish examined in our study. This rate is between the rates in studies conducted in Türkiye and in different regions of the world. Different results between studies may depend on many factors, including the number and type of fish examined, the maintenance conditions of aquariums and ornamental ponds, the administration of antiparasitic treatment, and the cleanliness of the aquarium water.

The rate of Chilodonella sp. was found between 26% and 51% in studies conducted in different regions (19-21). Chilodonella sp. was found in scratched skin samples collected from the gills, fins and scales of all fish species examined in this study. The rate of Chilodonella sp. was determined as 38.2%. Such rate is similar to those obtained in previous studies. The most common parasite detected in this study was Chilodonella sp.

Trichodina sp. are protozoan parasites which are common in aquarium and ornamental fish. Studies conducted globally detected a rate between 3% and 26.6% (4,20,21). Trichodina sp. was found in gill, skin scraping, and visceral samples of our study. The rate of Trichodina sp. detected in this study was 16.5%. Such rate is similar to those obtained in previous studies conducted on ornamental fish.

Ichthyophthirius multifiliis is one of the protozoan parasites with the highest distribution in the world (18). In our study, the rate of I. multifiliis was determined as 0.8%. The rate of I. multifiliis was reported between 2.8% and 8% in previous studies in Türkiye and the world (4,21). The reason for lower rates detected in our study when compared to previous studies may be due to the fact that the factor is well known by the producers and that protective measures are taken for it.

The rate of Piscinoodinium sp. was reported as 8.8% in this study. The presence of this parasite including Oodinium and Piscinoodinium has been reported in aquarium and ornamental fish. It has been reported that 6% of Piscinoodinium is observed on the gills of guppy fish in the medan region of Indonesia (22). Kayıs et al. (9) reported that they detected P. pillulare on the skin of Beta fish for the first time in Türkiye. Florindo et al. (23) reported that the most common species in all farms was P. pillulare when they examined the ornamental fish from different breeding farms in Brazil. Furthermore, it has been reported with a rate of 16.7% in goldfish in Brazil (24). The reason for the higher prevalence of Piscinoodinium sp. in this study may be associated with the poor maintenance conditions of one of the pet shops and the higher rate of Piscinoodinium in the samples collected from this pet shop.

Ichthyobodosis which is caused by severe infections of the skin and gills of parasitic flagellates of the genus Ichthyobodo is an important parasitic disease that causes serious losses among ornamental and farmed fish worldwide (25). The rate of Ichthyobodo (Costia) sp. was found between 1.7% and 27.6% in studies conducted to date (9,19-21,26); however, it was found 8.4% in this study. The rate in our study is similar to previous studies.

Apiosoma species are resident ciliates that cause infection when present in large numbers, are located on the gills, skin and fins of fish, and are commonly detected in fish grown in ponds (27). The rate was detected 1% in our study. It has been reported that it is detected in 6% of goldfish in Brazil (24). It has been reported on the skin of aquarium fish in the Rize region of Türkiye (28). In our study, the parasite was found in samples collected from both gills and skin, and fins.

The Epistylis is a pedicellate ciliate that attaches to the skin or fins of the host (27). It has been detected in 100% of skin scrapings of goldfish in Brazil. However, it has been reported that no causative agent was found in the gills (24). Kayıs et al. (9) reported that the agent was found in gill and skin scrapings; Iqbal and Haroon (14) reported that they were found only in gills. The rate of the parasite found in the scraping preparation taken from the skin and fins was 0.2%.

Vorticella sp., a ciliate from the Ciliophora branch, has been detected in several studies conducted in Türkiye (2,10,21). The rate of Vorticella sp. in a study conducted in Tetra and stingray fish in Konya was found 1% (21) in average, and 2% in tetra fish. Isık et al. (10) reported that Vorticella sp. was detected on only the gills of discus fish. Bulguroğlu (2) reported that Vorticella sp. was detected on the skin of yellow princess, blue princess, ahli cichlid, velifera and white mole fish. In this study, Vorticella sp. was found in a gill sample of a fish.

Tetrahymena sp. is considered an important pathogen of ornamental fish and causes significant death in these fish. These parasites are known as guppy disease because they cause infection, especially in guppy fish; however, their presence was detected in different ornamental fish species other than guppies. Tetrahymena sp. was detected on the gill and skin of 7 discus fish examined in Konya province of Türkiye (10). It was found at a rate of 11 (21) in tetra fish in another study conducted in the same shade. The rate of Tetrahymena was reported 1% in the aforesaid study. The cause for that may be due to the different fish species studied and the low rate of guppies.

It is noted that the most common monogenean trematodes are Gyrodactylus sp. and Dactylogyrus sp. species. In studies carried up to date, the rate of Gyrodactylus sp. was detected between 1% and 40% (4,19-22,29), and Dactylogyrus sp. was detected between 1% and 28% (4,19-22,29). Such rates were 14.5% and 13.7%, respectively in this study. Dactylogyrus and Gyrodactylus species may spread rapidly among aquarium fish under stressful situations. Therefore, it is expected to be more common in poor care conditions, transportation, and situations that may cause stress. The reason for the different rates between studies unequal conditions in all aquariums.

Capillaria sp. is one of the most common nematode parasites of aquarium fish. The rate was reported 0.9% (4) in previous studies conducted in Türkiye. Dewi et al. (22) detected in the abdominal cavities of guppy and goldfish as 8% and 4%, respectively, in Indonesia. In a study conducted in Iran, Capillaria sp. rate was reported as 0.33% in aquarium fish (18). Adult female parasite and Capillaria sp. egg were detected in 2 (0.4%) of 502 fish examined in our study. The rate of Capillaria sp. detected in our study is similar to the studies conducted in Ankara and Iran.

The rate of Camallanus sp. was detected as 0.4% (4) in Türkiye. However, it was reported that Camallanus was detected in a guppy fish in Afyon (30). It was reported in Brazil that adult C. cotti (31) parasites were found in guppy and beta fish, and adult C. maculatus parasite in plati fish (32). In this study, adult Camallanus sp. was found in the gut of one fish (0.2%).

Aeolosoma sp. is a freshwater annelid. The causative agent was found in the gill samples of two (0.4%) fish examined in this study. In a previous study conducted in the Konya region on total tetra and stingray fish, it was found only in one stingray fish with a rate of 1% (21). It was considered that the different number and species of fish examined may have caused these rates to differ from each other.

Whether rotifers are true parasites are debatable. It was reported in studies conducted on aquarium and ornamental fish that rotifera were rarely detected. In this study, the rate of Euchlanis sp. was 4.6%, whereas the rate of Philodina sp. was found 12.7%. Euchlanis sp. and Philodina sp. were found in gill and skin samples. Philodina species were previously found in the gills of discus fish in Türkiye (10). Euchlanis sp. was reported as 5% in the study conducted on tetra and stingray fish (21). The rate of Euchlanis sp. was found similar to previous studies. However, Philodina sp. was detected higher than previous studies. The reason for that was thought to be the cleanliness of the aquarium water and the poor maintenance conditions.

Argulus sp. is known as fish lice. It parasitizes on both marine and freshwater fish, and it is an arthropod that may cause infestations with higher morbidity and mortality under severe infections. The presence of A. japonicus species was reported in three goldfish in Texas (33). It was reported that A. foliaceus was found in the same fish species in Iran (34) and Pakistan (14). It was reported that A. foliaceus species was found in the skin and gills of an astronaut fish (Astronotus ocellatus) (7), A. japonicus species was found in 33% (35) koi fish and 28% in telescope fish (36) in Türkiye. One adult Argulus sp. was detected in only one (0.2%) of 502 fish samples examined in our study. It was considered in our study that the reason for the low incidence of the agent was recognition of the agent by the aquarium owners because they could see it macroscopically and started to struggle as soon as they saw it.

In our study, at least one and at most 6 different parasite species were found on the infected fish. It was determined that most of the fish that were positive for parasites were infected with a single parasite species (28.9%). This was followed by the fish infected with two (18.3%), three (7.0%), four (5.4%), five (2.8%), and six (0.4%) different parasite species. Doganay et al. (4) reported in their study conducted in Ankara that there were fish infected with at most 5 species at the same time, and they also reported that the fish they examined were generally infected with a single species (21.4%). Moyses et al. (24) reported in their study on goldfish in Brazil that 30% (9/30) of the fish had 2 or 3 parasite species, 40% (12/30) had 4 parasite species, and 30% (9/30) 5 had multiple infestations in the gills and/or skin, with one or more parasite species.

CONCLUSION

Consequently, the rate of parasitic infection was found higher in the fish examined in our study. The aquarium owners should pay attention to the cleanliness of the aquarium water in order to reduce the rate of parasitic infection in fish; when new fish are purchased, they should be taken from reliable sources, and the quarantine process should be observed.

* Ethics

Ethics Committee Approval: Approvals for the collection of samples and the carrying out the study were obtained from Kırıkkale University Animal Experiments Local Ethics Committee (E-608221397-010.99-74220 letter).

Informed Consent: A patient consent form is not required as the study was conducted on dead or dying fish.

Peer-review: Internally and externally peer-reviewed.

* Authorship Contributions

Surgical and Medical Practices: S.G., G.N.A., S.A., Concept: S.G., G.N.A., S.A., Design: S.G., G.N.A., S.A., Data Collection or Processing: S.G., G.N.A., S.A., Analysis or Interpretation: S.G., G.N.A., S.A., Literature Search: S.G., G.N.A., S.A., Writing: S.G.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.

References

Timur G, Timur M. Balık Hastalıkları. İstanbul Üniversitesi Su Ürünleri Fakültesi, Yayın no: 5, İstanbul, Türkiye; 2003.

Bulguroğlu SY. Bazı akvaryum balıkları (Cichlidae ve Poecilidae)’nda rastlanılan ektoparaziter enfestasyonların araştırılması. Yüksek Lisans Tezi, Akdeniz Üniversitesi Fen Bilimleri Enstitüsü, Türkiye. 2014.

Onal U, Celik I, Tokşen E, Sepil A, Caydan E. Early infection of discus Symphysodon aequifasciatus altricial larvae by Sciadicleithrum variabilum (Monogenea). J Fish Biol 2011; 78: 647-50.

Doganay A, Bozan H, Oge S. Parasitological examination of some aquarium fishes in Ankara. Ankara Univ Vet Fak Derg 1989; 36: 795-806.

Koyuncu CE. The infection of Trichodina sp. in some of the aquarium fishes (Carassius auratus L., 1758) in Mersin district. Ege J FAS 2006; 23: 327-30.

Koyuncu CE, Dönmez AE. The infection of Lernea cyprinaceae (Linnaeus, 1758) in some of aquarium fishes (Poecilidae) in Mersin district. Ege J FAS 2006; 23: 265-7.

Toksen E. Argulus foliacesus (Crustacea: Branchiura) infestation on oscar, Astronotus ocellatus (Cuvier, 1829) and its treatment. Ege J FAS 2006; 23: 177-9.

Kayıs S, Ozcelep T, Capkın E, Altınok I. Protozoan and metazoan parasites of cultured fish in Turkey and their applied treatments. Isr J Aquac 2009; 61: 93-102.

Kayıs S, Balta F, Serezli R, Er A. Parasites on different ornamental fish species in Turkey. J Fishsci.com 2013; 7: 79-85.

Isık N, Güclü F, Ceylan O. Parasites detected in discus fishes (Symphsodon discus). Eurasian J Vet Sci 2016; 32: 200-3.

Şahin Taner G. Türkiye’ye ithal edilen bazı tatlısu akvaryum balıklarının parazitleri: Hastalık profilleri ve risk analizi. Doktora Tezi, Ankara Üniversitesi Fen Bilimleri Enstitüsü, Türkiye. 2019.

Ricci C, Melone G. Key to the identification of the genera of bdelloid rotifers. Hydrobiologia 2000; 418: 73-80.

Noga EJ. Fish disease: diagnosis and treatment. 2nd ed. A John Wiley & Sons, Inc, Publication; 2010.

Iqbal Z, Haroon H. Parasitic infections of some freshwater ornamental fishes imported in Pakistan. Pakistan J Zool 2014; 46: 651-6.

Iqbal Z, Noreen F. Parasitic infection in an imported fish fantail, a variety of goldfish, Carassius auratus L. in Pakistan. Pakistan J Zool 2014; 46: 1679-83.

Hoshino ÉM, Hoshino MDFG, Tavares-Dias M. Parasites of ornamental fish commercialized in Macapá, Amapá State (Brazil). Rev Bras Parasitol Vet 2018; 27: 75-80.

Adel M, Ghasempour F, Azizi HR, Shateri MH, Safian AR. Survey of parasitic fauna of different ornamental freshwater fish species in Iran. Vet Res Forum 2015; 6: 75-8.

Rahmati-Holasoo H, Marandi A, Mousavi HE, Mirghaed AT. Parasitic fauna of farmed freshwater ornamental fish in the northwest of Iran. Aquac Int 2022; 30: 633-52.

Salemi S, Naghavi NS, Abedi S. Detection of Chilodonella as the predominant skin parasite infecting Poecilia reticulate (Guppy) in Iran, 2014 and a biological control approach for infection in laboratory scale. Indian J Fundam Appl L Sci 2015; 5: 62-7.

Kerek G. Konya bölgesinde yetiştirilen akvaryum balıklarından, Lepistes (Poecilia Reticulata) ve Japon balıklarında (Carassius Auratus) patolojik ve parazitolojik incelemeler. Yüksek Lisans Tezi, Selçuk Üniversitesi Sağlık Bilimleri Enstitüsü, Türkiye. 2016.

Durgun B, Ozdemir O. Pathological and parasitological investigations on Stingray fish (Hypostomus sp.) and Tetra fish (Characidae sp.) from aquarium fish. MJAVL 2021; 11: 145-57.

Dewi RR, Desrita, Fadhilla A. The prevalence of parasites in ornamental fish from fish market in Medan. International Conference on Agriculture, Environment, and Food Security. IOP Conf Ser: Earth Environ Sci 2018; 122: 012110.

Florindo MC, Jeronimo GT, Steckert LD, Acchile M, Gonçalves ELT, Cardoso L, et al. Protozoan parasites of freshwater ornamental fish. Lat Am J Aquat Res 2017; 45: 948-56.

Moyses CR, Spadacci-Morena DD, Xavier JG, Antonucci AM, Lallo MA. Ectocommensal and ectoparasites in goldfish Carassius auratus (Linnaeus, 1758) in farmed in the State of São Paulo. Rev Bras Parasitol Vet 2015; 24: 283-9.

Isaksen TE. Ichthyobodo infections on farmed and wild fish - Methods for detection and identification of Ichthyobodo spp. PhD thesis. University of Bergen, Norway. 2013.

Thilakaratne ID, Rajapaksha G, Hewakopara A, Rajapakse RP, Faizal AC. Parasitic infections in freshwater ornamental fish in Sri Lanka. Dis Aquat Organ 2003; 54: 157-62.

Klinger RE, Floyd RF. Introduction to Freshwater Fish Parasites 1. CIR716. 2013. https://fisheries.tamu.edu/files/2013/09/Introduction-to-Freshwater-Fish-Parasites.pdf

Kayıs S, Er A, Kacar ZZ. The investigation of external protozoan parasites on some fish sampled from Rize. JAES 2016; 2: 44-7.

Koyuncu CE. Gill ectoparasites of goldfish (Carassius auratus) imported from Syria. Advanced Underwater Sciences 2021; 1: 8-10.

Erez MS, Göksu A, Kozan E. Camallanus spp. in aquarium fish (Poecilia reticulata). Kocatepe Vet J 2017; 10: 37-9.

Menezes RC, Tortelly R, Tortelly-Neto R, Noronha D, Pinto RM. Camallanus cotti Fujita, 1927 (Nematoda, Camallanoidea) in ornamental aquarium fishes: pathology and morphology. Mem Inst Oswaldo Cruz 2006; 101: 683-7.

Martins ML, Garcia F, Piazza RS, Ghiraldelli L. Camallanus maculatus n. sp. (Nematoda: Camallanidae) in an ornamental fish Xiphophorus maculatus (Osteichthyes: Poeciliidae) cultivated in São Paulo State, Brazil. Arq Bras Med Vet Zootec 2007; 59: 1224-30.

Wafer LN, Whitney JC, Jensen VB. Fish Lice (Argulus japonicus) in Goldfish (Carassius auratus). Comp Med 2015; 65: 93-5.

Noaman V, Chelongar Y, Shahmoradi A. The First Record of Argulus foliacesus (Crustacea: Branchiura) Infestation on Lionhead Goldfish (Carassius auratus) in Iran. Iran J Parasitol 2010; 5: 71-6.

Koyuncu CE. Argulus japonicus (Thiele, 1900) infestation in Koi (Cyprinus carpio, Linnaeus, 1758) culture. Acta Aquat Turc 2020; 16: 66-70.

Koyuncu CE. The first record of Argulus japonicus Thiele, 1900 infestations on Telescope fish (Carassius auratus) of Mersin in Turkey. Advanced Underwater Sciences 2021; 1: 16-20.

A Parasitological Examination on Aquarium Fish Sold in Petshops in Kırıkkale