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Seasonal Distribution of Metazoan Parasites on Kura Barbell (Barbus lacerta) in Eastern Anatolia, Turkey.

Byline: Mustafa Koyun, Mehmet Ulupinar and Abdurrahman Gul

Abstract

This study was conducted to determine the frequency of metazoan parasitic infections of Kura barbell (Barbus lacerta) in Murat River in Eastern Anatolia, Turkey. A total of 110 host fish were collected, from March

2008 to February 2010. There were 1122 metazoan parasites recorded in collected samples. Four species of Monogenea (701 Dactylogyrus goktschaicus, 2 Dactylogyrus lankorani, 27 Dogielius mokhayeri and 40 Gyrodactylus sp.), one species of Digenea (72 Allocreadium isoporum), two species of Cestoda (5 Bothriocephalus acheilognathi, 3 Caryophylleous laticeps), two species of Nematoda (46 Rhabdochona denudata, 7 Contracaecum sp.) and two species of Copepoda (121 Lemproglena pulchella and 98 Eergasilus sieboldi) observed respectively.

According to their prevalence; D. goktschaicus (67.3%), D. lankorani (0.2%), D. mokhayeri (0.4%), Gyrodactylus sp. (12%), A. isoporom (0.7%), B. acheilognathi, (0.5%), C. laticeps (0.2%), R. denudata (15%), Contracaecum sp. (0.2%), L. pulchella (40%) and E. sieboldi (22%) were observed. Among these parasites D. goktschaicus, and D. mokhayeri are the first record on Kura barbell (B. lacerta) and in fish parasite fauna of Turkey.

Key Words: Barbus lacerta, Dactylogyrus goktschaicus, Dogielius mokhayeri, Bothriocephalus acheilognathi, Caryophylleous laticeps, Rhabdochona denudata, Lemproglena pulchella, Ergasilus sieboldi

INTRODUCTION

Metazoan parasites are a big group, inhabiting almost every organ of the host fish, which cause morphological, pathological, physiological, and biochemical, changes in the infected tissues and affect host physiology, thus inducing stress in the hosts animal (Cheng, 1974; Chubb, 1977; Pardeshi et al., 2012). Metazoan parasites represent an important component of freshwater ecosystems and in some cases are recognized as fish pathogens (Wyatt and Kennedy, 1989). Most of these parasites are pathogenic and virtually lead to weakening of the host fish. They also affect host survival and reproduction, alter fish behavior and migration patterns, and they can even regulate fish populations and affect fish community structure (Gordon and Rau, 1982; Poulin and Fitz Gerald, 1987; Garnick and Margolis, 1990; Barber and Poulin, 2002).

Metazoan parasites mostly cause direct or mortality though sub lethal pathogenic effects, such as destruction of gill lamellae (Kagel and Taraschewski, 1993). There have been numerous studies on metazoan parasites in Turkey inland waters (Becer and Kara, 1998; Aydogdu et al., 2001a,b, 2003, 2008; Kir et al., 2004; Tekin Ozan and Kir, 2005, 2008; Koyun and Altunel, 2007; Koyun, 2010, 2012; Soylu, 2013).

Basically, parasitic studies of Barbus lacerta are documented in the Euphrates-Tigris basin in Iran: Pazooki et al. (2006) recorded D. goktschaicus in Zanjan region (Iran) in B. lacerta. D. linstowi and R. denudata, Contracaecum sp. were reported on the same host (Bozorgnia et al., 2012). While D. lankorani, Capoeta umbla observed in our study was also reported by Koyun (2012), D. goktschaicus and Dogielius mokhayeri were the initial records for Turkey. The following observations were made during studies in Turkey: B. acheilognathi by Tekin-Ozan et al. (2008) on C. carpio at Beysehir Lake, C. laticeps at Kovada Lake by Becer and Kara (1998), E. sieboldi and C. laticeps at Dalyan Lagoon by Aydogdu et al. (2001b), C. laticeps and B. acheilognathi at Iznik Lake by Aydogdu et al. (2003); C. laticeps and B. acheilognathi at KaracaAlren Dam Lake by Kir et al. (2004).

Tekin-Ozan and Kir (2005) demonstrated Contracaecum sp. and C. laticeps at Kovada Lake and on C. carassius, at GAllbasi Dam Lake, Aydogdu et al. (2008) showed C. laticeps and Contracaecum sp. on Vimba vimba, Koyun and Altunel (2007) demonstrated at Enne Dam Lake Contracaecum sp. on C. carassius and C. auratus, B. acheilognathi on A. alburnus, A. isoporom and B. acheilognathi on Barbus plebejus escherichi.

Data shows that parasites recorded in the study were also demonstrated in previous study. Our findings demonstrate that parasites mentioned above are widely common for freshwater fish. However, not much is known about parasite on barb fish, except for a few studies (Chubb, 1977; Kennedy, 1974, Molnar and Jalali, 1992; Iyaji and Eyo, 2008). Much less is known about the relationship between biological parameters of the host and the success of the related parasite (Kennedy, 1974; Dence, 1957).

Barbus lacerta is an endemic fish for inland waters of Eastern Anatolia Region in Turkey and it has been recorded in the Euphrates and Tigris basin region (Geldiay and Balik, 2007). The aim of the present study was to describe metazoan parasites fauna of B. lacerta, their prevalence and intensities, as well as the quantitative changes in parasite species. The diversity and the existence of parasites in relation to seasons and size levels of the B. lacerta were investigated and discussed for the first time for Murat River in Eastern Anatolia, Turkey.

MATERIALS AND METHODS

Murat River is a sharp shallow flow, at least 15 km northeast of the city of BingAll and is fed by various tributary sources and small streams (Fig. 1). Fish were caught at monthly intervals during a two-year span, from March 2008 to February 2010, using seine and dip nets and transported back to the laboratory in river water alive. Fish species were identified according to Geldiay and Balik (2007).

Fish were killed with a sharp blow on the head, followed by exsanguinations. Total and fork length were measured (to the nearest mm) and total weight (to the nearest gram) for each individual fish and recorded. The stomach, intestine and gills of each fish were examined for metazoans within 24 h after sampling.

Each gill arch was removed to examine monogeneans. The intestine tract was removed and examined for endoparasites using a stereomicroscope.

Isolated parasites were fixed and preserved in accordance with the methods described in Bylund et al. (1980). The parasites were counted and preserved in 70% ethanol for further examination. Their identification was done according to Pugachev et al. (2010) and Bychowskaya-Pavlovskaya (1962).

Correlation test was applied to define correlations between the values of parasite prevalence, fish length, fish weight and water temperature for each parasite species (Little and Hills, 1978).

RESULTS

Table I shows 92% rate of infection, a total of 11 parasite taxa from 110 barbell fish, whereas Table II shows distribution of parasites in the host fish on monthly basis. Four species of Monogenea (701 Dactylogyrus goktschaicus, 2 Dactylogyrus lankorani, 27 Dogielius mokhayeri and 40 Gyrodactylus sp.), one species of Digenea (72 Allocreadium isoporom), two species of Cestoda (5 Bothriocephalus acheilognathi, 3 Caryophylleous laticeps), two species of Nematoda (46 Rhabdochona denudata, 7 Contracaecum sp.) and two species of Copepoda (121 Lemproglena pulchella and 98 Ergasilus sieboldi) were found on the gills and in the intestinal tract of B. lacerta caught at the Murat river, with their infection levels listed in Table III. The most prevalent and abundant parasite species were the monogenean D. goktschaicus, which were observed in 67.3% of the studied fish and comprised 62.4% of the total parasite specimens recorded.

The copepodit L. pulchella were observed in 40% of studied fish, and 10.8% of the total parasite specimens recorded and E. sieboldi were observed in 21.8% of studied fish and 8.7% of the total parasitic specimens recorded, R. denudata were observed in 15.4% of studied fish and 4.1% of the total parasite specimens recorded; A. isoporum were observed in 7.2% of studied fish and 6.4% of the total parasite specimens. The remaining parasite species comprised less than 5% each.

DISCUSSION

Metazoan parasites are generally found in all freshwater fishes. The parasite prevalence and intensity depend on many factors like parasite and its life cycle, host and its feeding habits and the physical factors of water body where the fish lives (Zaidi and Khan, 1976). Parasites are very sensitive to changes in environmental factors as a part of the natural environment and these factors affect the distribution and abundance of the parasite population. Seasonal variation factors; especially temperature is one of the important abiotic factors that affects the parasite populations (Hanzelova and Zitnan, 1985). Determination of seasonal parasite dynamics is important in terms of understanding of parasite biology, determination of fishes which are delicate against disease in which periods and regulation of aquaculture activities with control strategies (Neary et al., 2012).

In this study the distribution of the parasites shows change according to the seasons. D. goktschaicus, a monogenean parasite, is never seen in January, 109 parasites were recorded on 6 female fishes in August and 108 were recorded on 6 of 7 male fishes in the same month.

D. lenkorani is mostly specific for Capoeta species but its occurrence on male and female fishes shows that parasite was stumbled across. Dogielus makhoyeri is also not specific for this fish. Out of total of 27 parasites, 20 were found only on one female fish in August whereas in males 3 were detected in July and 4 in August.

Gyrodactylus species were encountered more likely in spring and autumn, and numbers showed inverse relationship with temperature. Twenty three parasites were recorded on 5 female fishes in spring, 2 on 2 fishes in autumn, and ten were recorded on one fish in December. Similar results are also seen in male fishes. Neary et al. (2012) have also reported similar type of data. Gyrodactylus sp. was reported 25% in summer, 22% in autumn and 100% in spring.

E. sieboldi shows distribution on wide range of freshwater fishes but sometimes cosmopolitan distribution is seen as a free form. We encountered, Copepodit parasites (L. pulchella and E. sieboldi), in our studies. E. sieboldi was first described by Nordmann in 1832 infecting various freshwater fish in Europe and is the type species of the genus Ergasilus. Tildesley (2008), Mokhayer (1985), Mirhashemi Nasab and Pazooki (2003), reported E. sieboldi, respectively, on Barbus brachycephalus in Persia Caspian Sea Region, in Mahabad Reservoir and Uromia and Zanjan (Persia) Region. Jalali (1998) reported L. pulchella on Barbus luteus and E. sieboldi on Barbus sharpeyi in Karoon Lake (Persia). From these parasites, L. pulchella prevails in especially cyprinid fish gills (Saglam, 1998; Soylu, 2012; Oktener et al., 2008). In this study, E. sieboldi and L. pulchella were recorded first time in Turkey on Barbus sp.

Table I.-Prevalence and mean intensity of infestation with metazoan parasites of Kura barbell during different seasons.

Parasites recorded###Fish###Infected###Infected###Prevalence###Mean No.###Mean###Min.-Max.###Total

###examined###fish###fish###(%)###of parasites###intensity###Parasite###parasites

###number###number

Spring###40###43

Dactylogyrus goktschaicus###25###58###5.16###3###1-17###129

Dactylogyrus lenkorani###-###-###-###-###-###-

Dogielius mokhayeri###-###-###-###-###-###-

Gyrodactylus sp.###8###19###3.25###0.60###1-18###26

Allocreadium isoporum###2###4.7###2.5###0.11###1-4###5

Bothriocephalus acheilognathi###4###9.3###1###0.09###1###4

Caryophylleous laticeps###2###4.7###1.5###0.07###1-2###3

Rhabdochona denudata###10###23###2.7###0.63###1-7###27

Contrcaecum sp.###2###4.7###3.5###0.16###1-6###7

Lemproglena pulchella###13###30###2.46###0.74###1-5###32

Eergasilus sieboldi###3###6.9###2.67###0.19###1-5###8

###241

Summer###42###39

Dactylogyrus goktschaicus###35###83###13.62###11.4###1-94###477

Dactylogyrus lenkorani###2###5###1###0.05###1###2

Dogielius mokhayeri###4###9.5###6.75###0.64###1-20###27

Gyrodactylus sp.###1###2.3###1###0.02###1###1

Allocreadium isoporum###3###7.1###1.66###0.12###1-3###5

Bothriocephalus acheilognathi###-###-###-###-###-###-

Caryophylleous laticeps###-###-###-###-###-###-

Rhabdochona denudata###7###16.7###2.71###0.45###1-7###19

Contrcaecum sp.###-###-###-###-###-###-

Lemproglena pulchella###19###45.2###3.05###1.38###1-11###58

Eergasilus sieboldi###16###38.1###4.93###1.88###1-46###79

###668

Autumn###20###18

Dactylogyrus goktschaicus###13###65###6.92###4.5###1-11###90

Dactylogyrus lenkorani###-###-###-###-###-###-

Dogielius mokhayeri###-###-###-###-###-###-

Gyrodactylus sp.###3###15###1###0.15###1-2###3

Allocreadium isoporum###3###15###20.67###3.10###62

Bothriocephalus acheilognathi###1###5###1###0.05###1###1

Caryophylleous laticeps###-###-###-###-###-###-

Rhabdochona denudata###-###-###-###-###-###-

Contrcaecum sp.###-###-###-###-###-###-

Lemproglena pulchella###9###45###2.78###1.25###1-8###25

Eergasilus sieboldi###5###25###2.20###0.55###1-3###11

###192

Winter###5###3

Dactylogyrus goktschaicus###19###20###21###22###23###24

Dactylogyrus lenkorani###1###20###5###1###5###5

Dogielius mokhayeri###-###-###-###-###-###-

Gyrodactylus sp.###-###-###-###-###-###-

Allocreadium isoporum###1###20###10###2###10###10

Bothriocephalus acheilognathi###-###-###-###-###-###-

Caryophylleous laticeps###-###-###-###-###-###-

Rhabdochona denudata###-###-###-###-###-###-

Contrcaecum sp.###-###-###-###-###-###-

Lemproglena pulchella###-###-###-###-###-###-

Eergasilus sieboldi###3###60###2###1.2###2-4###6

###100###45

Table II.- Recorded parasites of female and male specimens of Kura barbell according to months.

Months###Examined###Found###Mean weight###Main length###Recorded###parasites

###Infected###(g)###(mm)###1###2###3###4###5###6###7###8###9###10###11###12

Female fish

March###7###7###24.97###140###19###-###-###2###-###-###1###5###1###2###7###37

April###12###11###22.75###148###34###-###-###3###-###-###2###6###-###4###-###49

May###5###4###30.34###153###30###-###-###18###-###1###-###2###-###8###-###59

June###9###8###31.55###146###40###1###-###-###-###-###-###2###-###4###5###52

July###7###7###34.42###148###99###-###-###1###-###-###-###1###-###2###58 161

August###6###6###49.00###179###109###-###20###-###2###-###-###6###-###14###5 156

September###6###5###22.95###148###32###-###-###1###8###-###-###-###-###7###5###53

October###5###4###30.02###147###9###-###-###1###-###1###-###-###-###2###-###13

November###1###1###36.10###162###-###-###-###-###4###-###-###-###-###4###-###8

December###3###3###51.80###182###5###-###-###10###-###-###-###-###-###6###-###21

January###1###-###114.20###240###-###-###-###-###-###-###-###-###-###-###-###-

Total###62###56###-###-###377###1###20###36###14###2###3 22###1###53###80 609

Male fish

March###5###5###16.32###137###8###-###-###1###-###-###-###1###-###-###-###10

April###10###9###17.63###126###37###-###-###2###5###3###- 13###6###11###-###77

May###4###4###18.93###131###1###-###-###-###-###-###-###-###-###7###1###9

June###8###7###27.23###140###36###1###-###-###3###-###-###8###-###8###4###60

July###5###5###26.80###143###85###-###3###-###-###-###-###-###-###9###5 102

August###7###6###29.28###148###108###-###4###-###-###-###-###2###-###21###2 137

September###3###3###31.00###149###6###-###-###1###50###-###-###-###-###1###3###60

October###3###3###28.56###147###39###-###-###-###-###-###-###-###-###9###3###52

November###2###2###28.80###164###4###-###-###-###-###-###-###-###-###2###-###6

December###-###-###-###-###-###-###-###-###-###-###-###-###-###-###-###-

January###1###-###22.20###167###-###-###-###-###-###-###-###-###-###-###-###-

Total###48###44###-###-###324###1###7###4###58###3###- 24###6###68###18 513

Table III.- Fish length - parasitic relationship.

###Total 1nfected###M: Male

F1sh length groups (mm)###Exam1ned of number###of number###1###2###3###4###5###6###7###8###9###10###11###12###F: Female

126-137###19###18###46###-###-###3###5###3###-###14###6###18###1###96###M(19), F(-)

140-146###29###27###180###2###3###2###3###-###1###15###1###23###21###251###M(13), F(16)

147-149###43###39###327###-###4###7###58###1###2###9###-###46###71###525###M(13), F(30)

158-167###9###7###34###-###-###18###4###1###-###2###-###14###-###73###M(3), F(6)

179-240###10###9###114###-###20###10###2###-###-###6###-###20###5###177###M(-), F(10)

Total###110###100###701###2###27###40###72###5###3###46###7###121###98###1122 M(48), F(62)

In this study 68 parasites were found in male fishes 38 parasites on 9 hosts in summer, 18 on 6 hosts in spring and 12 parasites on 5 hosts in autumn. Similar results were also recorded for female fishes with 53 parasites. For female fishes, 58 parasites were mostly seen in July and 5 were seen on male fishes. A total of 80 parasites were recorded on female hosts and 18 parasites on male fishes during the study. Tombi and Bilong Bilong (2004) also reported that male fishes get infected less by this parasite especially in reproductive period because of their increased activity.

A. isoporum is not specific endoparasite for host species that commonly seen in more than 16 cyprinid fish, viz., Alburnoides bipunctatus, Alburnus filippi, Aphanius vladykovi, Barbus lacerta, Barbus barbus, Capoeta aculeata. C. capoeta, C. damascina, Cobitis taenia, Leusiscus lepidus, G. gobio, Leusiscus cephalus, L. leusiscus, and A. alburnus (Moravec, 1994; Pazooki, 2012). Tieri et al. (2006) from Italy and Moravec (1994) from Czechoslovakia reported A. isoporum on L. cephalus; and Rantanen et al. (1998) reported it on Pisidium amnicum. In Turkey, Koyun and Altunel (2007) have reported it in B. plebejus escherichi and A. alburnus from Enne dam; Aydogdu et al. (2001a) has been reported it from Doganci dam. The rate of A. isoporum in the study is 7% as against Aydogdu et al. (2001a). Total of 14 parasites were found in the 4 female hosts and 58 individuals in the 4 male hosts. With this inference, distribution of A. isoporum on B. lacerta doesn't have an importance in terms of seasons.

Bothriocephalus acheilognathi (Asian cestode) is spread from Asia to the other varied regions because of wide distribution of Ctenopharyngodon idella (Scholz, and Cave, 1992).

Aydogdu et al. (2003) from Iznik Lake and Ozturk et al. (2001) in from Manyas Lake reported C. carpio, Ozturk et al. (2002) reported it on Gobius fluviatilis from Uluabat Lake. The same species were also recorded on A. alburnus from Enne Dam Lake by Koyun and Altunel (2007). Koyun (2010) and on B. plebejus escherichi (Aydogdu et al., 2001a) and reported it on L. cephalus from Doganci Dam Lake. Although, yearly distribution of B. acheilognathi was 35% according to the Koyun and Altunel (2007) database, in this study, the rate is totally 6%. Two parasites were recorded on 2 female hosts and 3 parasites in 3 male hosts.

There were 54 species reported according to the Moravec (1994) systematic evaluations associated with Rhabdochona genus. He also reported that Rhabdochona sp. is mostly found in Percidae, Solmonidae, Siluridae and Gobitidae family fishes. Rhabdochona has been recorded by Pereira and Pellitero (1979) in Spain and Moravec (1989) in Czechoslovakia on a variety of freshwater fishes. Larval form of R. denudata in Turkey was reported in L. cephalus from Doganci Dam Lake by Aydogdu et al. (2001a), in A. alburnus by Aydogdu and Selver (2006), in A. brama from Durusu Lake by Karatoy and Soylu (2006) and in Gobius fluviatilis from Manyas and Uluabat lakes by Ozturk et al. (2001, 2002). This study is the first record for R. denudate in B. lacerta. In this study Aydogdu et al. (2001b) has recorded 46 individuals of R. denudata during spring and summer months.

Larval form of Contracaecum sp. was found in intestinal cavity of B. lacerta in our study. Koyun and Altunel (2007) found it on A. alburnus, Selver et al, (2009) found it on V. vimba and also on C. carassius, C. auratus, C. tinca, B. plebejus escherichi, and S. erythrophthalmus. In our study, totally 6 parasites were found in only March and April.

Considering the correlation between fish length and parasite numbers, the maximum parasite number (525) was seen on 147-167 cm fish group that consists of 43 fishes (30 female and 13 male). The minimum parasite number (73) was recorded on 158-167 cm fish group that consist 6 female and 3 male fishes. According to the Table III data, there is no significant result between fish length and parasite distribution. The parasite distributions are more heterogeneous in lotic water than lentic that clarifies the accordance of recorded seasonal distributions of parasite species.

Aquatic living organisms have more activity because of continuous flows of river water. During the study, insufficient number of fish samples were obtained in winter due to hypermobility of fish due to sudden change of temperature.

CONCLUSIONS

In this study the prevalence and quantitative changes in 11 endo-and ecto parasites of kura barbell (B. lacerta) from Murat River has been described. Among the recorded parasites Dactylogyrus goktschaicus, and Dogielius mokhayeri are the first records for Kura barbell and in freshwater fish parasite fauna of Turkey.

ACKNOWLEDGEMENT

This work was supported by BingAll University with a BAP Project no: 2010/19.

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