Int. J. Aquat. Biol. (2015) 3(6): 414-424 E-ISSN: 2322-5270; P-ISSN: 2383-0956 Journal homepage: www.ij-aquaticbiology.com © 2015 Iranian Society of Ichthyology Original Article Parasitic worms and their histopathological effects in four sturgeon species from the southwest shores of the Caspian Sea Mohammad Reza Noei1, Shaig Ibrahimov1, Masoud Sattari*21 1Institute of Zoology, the Azerbaijan National Academy of Sciences, Baku, Azerbaijan. 2Fisheries Department, Faculty of Natural Resources, University of Guilan, Sowmeh Sara, Iran. Article history: Received 17 August 2015 Accepted 2 N o v e m b e r 2015 Available online 2 5 D e c e m b e r 2015 Keywords: Trematode Cestode Acanthocephalans Huso huso Acipenser stellatus Acipenser nudiventris Acipenser gueldenstaedtii Abstract: This study conducted to provide the status of parasite communities of four sturgeon species viz. Acipenser stellatus, A. gueldenstaedtii, A. nudiventris, and Huso huso in the southwest of the Caspian Sea and their histopathological effects on the examined fishes. For this purpose a total of 93 individuals of four sturgeon species were caught in two fisheries regions from the southwest of the Caspian Sea (Guilan Province, Iran) from March 2010 to May 2011. The histological slides of the infested tissues of the examined fishes were prepared for study of the histopathological effects of the parasites. Classical epidemiological variables, including mean intensity, prevalence, abundance and dominance were calculated for overall samples, grouped by season, geographical region, and sex. Five worm species, including two nematodes (Cucullanus sphaerocephalus and Eustrongylides excisus larvae), one cestode (Bothrimonus fallax), one acanthocephalans (Leptorhynchoide plagicephalus) and one digenean trematode (Skrjabinopsolus semiarmatus) were found in examined sturgeons and their histopathological effects on the fish tissues were assessed. Based on the results, the diversity of the parasites (including freshwater ones) in the southern part of the Caspian Sea have decreased since the time of the first study in 1972. This may be related to unfavorable conditions in freshwater ecosystems. Introduction Sturgeons are evolutionary relicts with a wide distribution in the northern hemisphere (Holcik, 1989). Their status as basal actinopterygian fish, unique benthic specializations, and variation in their basic diadromous life history make sturgeons interesting biological and biogeographical subjects (Holcik, 1989). Extensive studies on Eurasian sturgeons indicate that they are also unique among fishes in possessing a markedly diverse assemblage of host-specific parasites. The parasites of sturgeons have been studied in several works (Dogiel and Bykhovskiy, 1939; Dubinin, 1952; Shulmann, 1954; Nechaeva, 1964; Mokhayer, 1972; Skryabina, 1974; Sattari and Mokhayer, 2006; Sattari et al., 2007, 2008, 2009; Khara et al., 2009: Mousavi Sabet and Sattari, 2013; Daghigh Roohi et al., 2014a, b; Khara * Corresponding author: Masoud Sattari E-mail address: msattari@guilan.ac.ir and Sattari, 2014). However, there are only a few reports about their parasites in the southern part of the Caspian Sea. Mokhayer (1972) studied the parasites of three sturgeon species, namely A. stellatus, A. gueldenstaedtii, and Huso huso from the Caspian Sea, and reported 17 parasite species, including Trichodina reticulata, Polypodium hydriforme, Skrjabinopsolus skrjabini, S. acipenseris, Amphilina foliacea, Bothrimonus fallax, Eubothrium acipenserinum, Ascarophis ovotrichuria, Cyclozone acipenserina, Cucullanus sphaerocephalus, Contracaecum squalii, Anisakis schupakowi, Eustrongylides excisus, Leptorhyn- choides plagicephalus, Pomphorhynchus laevis, Corynosoma capsicum and Pseudotracheliastes stellatus. Gorogi (1996a) studied the parasites of A. persicus and reported three parasite species, 415 Noei et al./Parasitic worms and histopathologic effects in sturgeons including C. sphaerocephalus, S. semiarmatus and L. plagicephalus. In another study, Gorogi (1996b) reported five parasite species viz. C. sphaero- cephalus, Anisakis schupakovi, S. semiarmatus, Corynosoma strumosum and E. acipenserinum from H. huso. There are also other reports regarding the parasites of the sturgeons from the Caspian Sea (Sattari and Mokhayer, 2006). Therefore, this study attempts to provide the status of parasite communities (prevalence, mean intensity of infection, abundance and dominance) of four sturgeon species viz. stellate sturgeon, Acipenser stellatus Pallas, 1771, Russian sturgeon, A. gueldenstaedtii Brandt, 1833, Ship sturgeon, A. nudiventris Lovetsky, 1828, and great sturgeon, Huso huso in the southwestern of the Caspian Sea and their histopathological effects on the examined fishes. Materials and Methods A total of 93 individuals of four sturgeon species, namely A. stellatus (n=60), A. gueldenstaedtii (n=12), A. nudiventris (n=9), and Huso huso (n=12) were collected from March 2010 to May 2011. The samples includes sturgeons caught in fisheries regions 1 (region 1: western coast of Guilan Province) and 2 (region 1: eastern coast of Guilan Province) along a shore line of more than 200 km. The stellate sturgeons (60 fish) had a mean weight of 8.725 kg (±2.735 kg, range=4-15 kg) and fork length of 129.57 cm (±18.11 cm, range=83-170 cm). The Russian sturgeons (12 fish) had a mean weight of 19.417 kg (±6.007 kg, range=12-32 kg) and fork length of 135.33 cm (±15.20 cm, range=110-155 cm). The Ship sturgeons (9 fish) had a mean weight of 28.444 kg (±11.304 kg, range=11-41 kg) and fork length of 156.78 cm (±29.28 cm, range=112-190 cm). Great sturgeons (12 fish) had a mean weight of 119.500 kg (±71.008 kg, range=22-271 kg) and fork length of 207.5 cm (±41.097 cm, range=144-274 cm). Since the samplings of this study were restricted by the governmental fishing program (i.e. for artificial propagation and then exporting their flesh), therefore, age determination was not possible. After recording biometric characteristics of fishes, common necropsy and parasitology methods (Bykhovskaya-Pavlovskaya, 1985; Stoskopf, 1993) were used for finding parasites. Live trematodes and acanthocephalans were relaxed in distilled water at 4ºC for 1 hrs and fixed in 10% hot buffered formalin. Live nematodes were fixed in hot 70% ethanol and cleared in hot lactophenol. Frozen specimens were thawed in water, and then fixed with 10% formalin (trematodes and acanthocephalans) or 70% ethanol (nematodes). All fixed specimens in 10% formalin were stained with aqueous acetocarmine, dehydrated and mounted in Permount. After fixation of the infested tissues of the examined fishes for 24 hrs, they were processed based on Eagderi et al. (2013), embedded in paraffin and subsequently cut (with a thickness of 5 μm) with a microtome (Model 1130 Rotary Microtome, Reichert-Jung) for preparing histological slides. Then, they were stained with haematoxylin-eosin for study of the histopathological effects of the parasites. The worms were identified using parasite identification keys (Yamaguti, 1961; Bykhovskaya-Pavlovskaya et al., 1962; Avdeyev, 1987; Moravec, 1994) and then were deposited at the Laboratory of Fish Diseases, Faculty of Natural Resources, University of Guilan, Iran. Statistical analysis: Classical epidemiological variables (prevalence, intensity and abundance) were calculated according to Bush et al. (1997). Mean intensity of infection was determined by dividing the total number of recovered parasites by the number of infected fish samples, while calculating abundance was carried out by dividing the total number of recovered parasites by the number of (infected and uninfected) fish samples. Prevalence was also calculated by dividing the number of infected fish samples by the total number of the examined fishes and expressed as a percentage. The dominance of a parasite species was calculated as N/N sum (where N=abundance of a parasite species and N sum=sum of the abundance of all parasite species found) and expressed as a percentage (modified after Leong and Holmes, 1981). Mean 416 Int. J. Aquat. Biol. (2015) 3(6): 414-424 intensity of infection and abundances of parasite species (with prevalences >10%) among seasons, age classes and sexes were tested by the Kruskal- Wallis test (KW, multiple comparisons) and Mann- Whitney U test (MW, pairwise comparisons). The results were considered significant at the 95% level (P<0.05). Data analysis were performed using SPSS software (IBM SPSS Statistics, IBM Corporation). Results A total of 762 parasite belonging to five species, including two nematodes viz. Cucullanus sphaerocephalus Rudolphi, 1809 and Eustrongylides excisus Jagerskiold, 1909, one cestode species, namely Bothrimonus fallax Luhe, 1900, one acanthocephalans, namely Leptorhynchoides plagicephalus Westrumb, 1821, and one digenean trematode, namely Skrjabinopsolus semiarmatus Molin, 1858 were found in the examined sturgeons, including A. stellatus, A. gueldenstaedtii, A. nudi- ventris and H. huso. The prevalence, mean intensity, range, abundance and dominance of the collected parasites are presented in Tables 1 and 5-7. A total of 631 worms belonging to five species were found in A. stellatus. Leptorhynchoides plagi- cephalus had the highest prevalence (45%), abundance (5.22) and dominance (49.6%), while S. semiarmatus had the highest mean intensity of infection (24.45) (Table 1). These two parasites constituted up to 92.23% of parasite communities in A. stellatus. The prevalence of C. sphaerocephalus and S. semiarmatus in A. stellaus was higher in spring (16.22 and 27.02) than that of winter and autumn, respectively, whereas the prevalence of L. plagice- phalus was higher in winter than that of spring and autumn, respectively (Table 2). The mean intensity of infection of these three parasites was higher in spring than winter and autumn, respectively, but the differences between seasons were not significant (KW, χ2=0.778, df=2, P=0.678 for C. sphaero- cephalus; KW, χ2=0.00, df=1, P=1.00 for Parasites Prevalence (%) Mean intensitySD Range AbundanceSD Dominance (%) S. semiarmatus N=269 18.33 24.4562.41 1-212 4.4827.4 42.63 L. plagicephalus N=313 45 11.5917.06 1-71 5.2212.7 49.6 C. sphaerocephalus N=22 17.26 2.442.30 1-8 0.371.22 3.49 B. fallax N=12 1.66 12 0 12 0.21.55 1.9 E. excisus larvae N=15 5 5.03.61 1-8 0.251.28 2.4 Table 1. The prevalence, mean intensity, range, abundance and dominance of some parasites in A. stellatus. Parasite Season C. sphaerocephalus Prevalence (%) MeanSD Range S. semiarmatus Prevalence (%) MeanSD Range L. plagicephalus Prevalence (%) MeanSD Range E.exisus Prevalence (%) MeanSD Range B. fallax Prevalence (%) MeanSD Range Spring N=37 16.22 2.82.7 (1-8) 27.02 26.465.4 (1-212) 45.95 14.2920.58 (1-71) 2.70 1 8 2.70 12 12 Autumn N=16 12.5 21.4 (1-3) 0 37.5 5.57.23 (1-20) 0 0 Winter N=7 14.29 1 1 14.29 5 5 57.14 9.257.27 (2-19) 28.57 3.53.53 (1-6) 0 Table 2. The prevalence, mean intensity and range of some parasites of A. stellatus in various seasons. 417 Noei et al./Parasitic worms and histopathologic effects in sturgeons S. semiarmatus; and KW, χ2=1.606, df=2, P=0.448 for L. plagicephalus). The same results were found regarding the abundance of these three parasites in various seasons (KW, χ2=0.098, df=2, P=0.952 for C. sphaerocephalus; KW, χ2=5.374, df=2, P=0.068 for S. semiarmatus; and KW, χ2=1.524, df=2, P=0.467 for L. plagicephalus). The prevalence of C. sphaerocephalus and S. semiarmatus in A. stellatus in region 1 was higher, but the prevalence of L. plagicephalus in region 2 was higher (Table 3). The mean intensity of infection of C. sphaerocephalus in region 1 was significantly higher (KW, χ2=4.8, df=1, P<0.05, but no significant differences were found between these two regions concerning to S. semiarmatus and L. plagicephalus (KW, χ2=1.457, df=1, P=0.224 for S. semiarmatus; and KW, χ2=0.223, df=1, P=0.637 for L. plagicephalus). Also, no significant differences were found regarding the abundance of these three parasites between regions (KW, χ2=0.685, df=1, P=0.408 for C. sphaerocephalus; KW, χ2=0.031, df=1, P=0.806 for S. semiarmatus; and KW, χ2=0.166, df=1, P=0.684 for L. plagicephalus). The prevalence of C. sphaerocephalus in females of A. stellatus (16.66) was higher than males (12.5), but the prevalence of S. semiarmatus and L. plagicephalus in males (20.83 and 45.83, respectively) was higher (Table 4). The mean intensity of the infection of these three parasites in females was higher than males, although the differences between males and females were not significant (KW, χ2=0.333, df=1, P=0.564 for C. sphaerocephalus; KW, χ2=0.009, df=1, P=0.926 for S. semiarmatus; and KW, χ2=4.054, df=1, P=0.054 for L. plagicephalus). The same results were found regarding the abundance of these three parasites in males and females (KW, χ2=0.179, df=1, P=0.673 for C. sphaerocephalus; KW, χ2=0.153, df=1, P=0.695 for S. semiarmatus; and KW, χ2=0.326, df=1, P=0.568 for L. plagicephalus) (Table 4). The prevalence of C. sphaerocephalus, S. semiar- matus and L. plagicephalus in higher length groups of A. stellatus were higher than in lower length groups. The mean intensity of the infection of these three parasites in higher length groups were higher than lower length groups, but the differences were Parasite locality C. sphaerocephalus Prevalence (%) Mean SD Range S. semiarmatus Prevalence (%) MeanSD Range L. plagicephalus Prevalence (%) MeanSD Range E. excisus Prevalence (%) MeanSD Range B. fallax Prevalence (%) MeanSD Range Location 1 N=27 18.52 18.52 40.74 3.70 3.70 3.62.61 8.86.1 10.7315.25 8 - 12 - (1-8) (2-17) (1-54) 8 12 Location 2 N=33 12.12 18.18 48.48 6.06 1.00 - 37.585.5 12.1918.67 3.53.54 0 1 (1-212) (1-71) 1-6 Table 3. The prevalence, mean intensity and range of some parasites of A. stellatus in two sampling regions. Parasite Sex C. sphaerocephalus Prevalence (%) MeanSD Range S. semiarmatus Prevalence (%) MeanSD Range L. plagicephalus Prevalence (%) MeanSD Range E. excisus Prevalence (%) MeanSD Range B. fallax Prevalence (%) MeanSD Range Female N=36 16.66 16.66 44.44 5.56 2.82.7 39.3  84.7 13.818.03 3.53.53 0 (1-8) (1-212) (1 - 71) (1-6) Male N=24 12.5 20.83 45.83 4.17 4.17 1.671.15 6.66.35 8.3615.8 8 12 (1-3) (1-17) (1-54) 8 12 Table 4. The prevalence, mean intensity and range of some parasites of A. stellatus in males and females. 418 Int. J. Aquat. Biol. (2015) 3(6): 414-424 not significant (KW, χ2=6.667, df=7, P=0.464 for C. sphaerocephalus; KW, χ2=9.119, df=8, P=0.332 for S. semiarmatus; and KW, χ2=15.750, df=15, P=0.399 for L. plagicephalus). The same results were found regarding the abundance of these three parasites in various length groups (KW, χ2=18.789, df=27, P=0.878 for C. sphaerocephalus; KW, χ2=25.993, df=27, P=0.519 for S. semiarmatus; and KW, χ2=20.508, df=27, P=0.809 for L. plagicephalus). In addition, the prevalence of C. sphaerocephalus and S. semiarmatus in higher weight groups of A. stellatus was more than lower weight groups. The mean intensity of infection of these two parasites in higher weight groups was also more than lower weight groups, but the differences were not significant ((KW, χ2=6.667, df=5, P=0.247 for C. sphaerocephalus; KW, χ2=6.103, df=5, P=0.296 for S. semiarmatus). The same results were found regarding the mean intensity of infection of this parasite, but the differences were not significant (KW, χ2=4.769, df=5, P=0.782). No significant differences was found concerning to the abundance of these three parasites in various weight groups of A. stellatus (KW, χ2=12.681, df=11, P=0.315 for C. sphaerocephalus; KW, χ2=14.596, df=11, P=0.202 for S. semiarmatus; and KW, χ2=13.111, df=11, P=0.767 for L. plagicephalus). A total of 43 worms belonging to three species were found in A. gueldenstaedtii (Table 5). In this species, C. sphaerocephalus had the highest prevalence (50%), mean intensity of infection (6.17), abundance (3.08), and dominance (86.04%). Eustrongylides excisus larvae had the second highest prevalence (16.66), mean intensity of infection (2.5), abundance (0.41,) and dominance (11.63%). These two parasites were constituted up to 97.67% of parasite communities in the examined specimens of A. gueldenstaedtii (Table 5). A total of 48 worms belonging to four species were found in the specimens of A. nudiventris (Table 6). Based on the results, C. sphaerocephalus had the highest prevalence (55.5%), abundance (3) and parasites Prevalence (%) Mean intensity  SD Range Abundance SD Dominance (%) L. plagicephalus N=37 8.33 1 1 0.080.01 2.32 C. sphaerocephalus N=1 50 6.174.02 1-12 3.080.13 86.04 E. excisus larvae N=5 16.66 2.52.12 1-4 0.410.02 11.63 Table 5. The prevalence, mean intensity, range, abundance and dominance of some parasites in A. gueldenstaedtii. parasites Prevalence (%) Mean intensity  SD Range Abundance SD Dominance (%) L. plagicephalus N=37 8.33 1 1 0.080.01 2.32 C. sphaerocephalus N=1 50 6.174.02 1-12 3.080.13 86.04 E. excisus larvae N=5 16.66 2.52.12 1-4 0.410.02 11.63 Table 6. The prevalence, mean intensity, range, abundance and dominance of some parasites in A. nudiventris. parasites Prevalence (%) Mean intensity  SD Range Abundance SD Dominance (%) S. semiarmatus N=4 8.33 4 4 0.330.11 10 C. sphaerocephalus N=35 41.67 77.65 1-19 2.920.1 87.5 E. excisus larvae N=1 8.33 1 1 0.080.01 2.5 Table 7. The prevalence, mean intensity, range, abundance and dominance of some parasites in Huso huso. 419 Noei et al./Parasitic worms and histopathologic effects in sturgeons dominance (56.25%). Skrjabinopsolus semiarmatus had the second highest prevalence (22.2), abundance (1.56) and dominance (29.17%). The mean intensity of the infection of S. semiarmatus (7) was higher than C. sphaerocephalus (5.4). These two parasites constituted up to 85.42% of the parasite communities in A. nudiventris. A total of 40 worms belonging to three species were found in the samples of H. huso (Table 7). Cucullanus sphaerocephalus had the highest prevalence (41.67%), mean intensity of infection (7) abundance (2.92) and dominance (87.5%). Skrjabinopsolus semiarmatus had the second prevalence (8.33), mean intensity of infection (4), abundance (0.33) and dominance (10%). These two parasites constituted up to 97.5% of parasite communities in H. huso. The histopathological effects of some parasites on the gut of the sturgeons are as follows: Eustrongylides excisus larvae: The parasites were encapsulated in the wall of the intestinal mucosa. There was chronic inflammation around the parasites Figure 1. Histopathologic section of the infested tissues by E. excisus larvae in the gut of H. huso (H&E, 40X). Figure 2. Histopathologic section of the infested tissues by E. excisus in the gut of H. huso (H&E, 400X). Figure 3. Histopathologic section of the infested tissues by L. plagicephalus in the gut of A. nudiventris (H&E, 40X). Figure 4. Histopathologic section of the infested tissues by L. plagicephalus in the gut of A. nudiventris (H&E, 400X). Figure 5. Histopathologic section of the infested tissues by C. sphaerocephalus in the gut of A. gueldenstaedtii (H&E, 40X). 420 Int. J. Aquat. Biol. (2015) 3(6): 414-424 with infiltration of the macrophages, lymphocytes, fibroblasts, and multiple eosinophils (Figs. 1, 2). Leptorhynchoides plagicephalus: The head of the parasite with horny proboscis was attached in a pitted zone of intestinal wall of the sturgeon. The spines of proboscis formed severe necrosis in the epithelium with chronic inflammation. The mononuclear cells with multiple lymphocytes were infiltrated and also some lymphoid follicles were present (Figs. 3, 4) Cucullanus sphaerocephalus: This parasite is caused the focal necrosis and acute to sub-acute inflammation with multiple lymphocytes (Figs. 5, 6). Bothrimonus fallax: Necrosis and destruction of the mucosa were observed in the site of attachment this parasite. Mononuclear cells such as lymphocytes and a few number of eosinophils were also observed (Figs. 7, 8). Discussion There are few reports about the parasites of sturgeons in Iran. Mokhayer (1972) studied the parasites of three sturgeon species, namely A. stellatus, A. gueldenstaedtii and H. huso, and reported 17 parasite species. Gorogi (1996a, b) also studied the parasites of two sturgeon species, including A. persicus and H. huso with reporting 3 and 5 parasite species, respectively. Sattari and Mokhayer (2006) studied the parasites of 206 individuals of A. persicus and reported nine parasite species. However, in the present study, Trichodina reticulata, Polypodium hydriforme, Ascarophis ovotrichuria, Cyclozone acipenserina, Contraca- ecum squalii and Pomphorhynchus laevis were not recovered from the samples. Skryabina (1974) found that A. stellatus is parasitized by more worm species than A. gueldenstaedtii, particularly in the Caspian Sea basin. Skryabina (1974) also found that in the Azov and Caspian Seas, the prevalence of C. sphaerocephalus in A. stellatus is less than other sturgeon species from the same localities. Similarly, in the present study, it was found that the diversity of helminth fauna in A. stellatus was more than other examined sturgeons. It was also found that the prevalence and mean intensity of C. sphaerocephalus in A. stellatus were less than in the other examined Figure 6. Histopathologic section of the infested tissues by C. sphaerocephalus in the gut of A. gueldenstaedtii (H&E, 400X). Figure 7. Histopathologic section of the infested tissues by B. fallax in the gut of A. stellatus (H&E, 40X). Figure 8. Histopathologic section of the infested tissues by B. fallax in the gut of A. stellatus (H&E, 400X). 421 Noei et al./Parasitic worms and histopathologic effects in sturgeons sturgeons. Markov et al. (1967) found that the most important parasites of A. stellatus from the lower course of the Volga River are cestodes and acanthocephalans. They also found that along the coast of Dagestan, the most important species are E. acipenserinum, B. fallax, L. plagicephalus and S. semiarmatus. Similarly, in the present study, the prevalence and mean intensity of L. plagicephalus in A. stellatus were higher than other examined sturgeons. Bothrimonus fallax was only found in A. stellatus. Of all acipenserid species, the Russian sturgeon has the best-known parasite fauna (Holcik, 1989). The complete list of the parasites found in A. gueldenstaedtii includes 46 species; of these, parasitic worms are the largest group (Dogiel and Bykhovskii, 1939; Shulman, 1954; Nechaeva, 1964; Skryabina, 1974). Skryabina (1974) reported that the parasite fauna of A. gueldenstaedtii is similar to that of A. stellatus, while in this study and also in Sattari and Mokhayer (2006), the parasite fauna of A. gueldenstaedtii was similar to that of A. nudiventris and H. huso than A. stellatus. The main parasites of A. nudiventris includes 32 parasites species and most of them are specific to acipenserids (Dogiel and Bykhovskii, 1939; Shulman, 1954; Skryabina, 1974). Shulman (1954) pointed out that the adult ship sturgeons are infested primarily in the sea by helminthes such as S. semiarmatus, E. acipenserinum and C. sphaero- cephalus. In juveniles, the predominant parasites are freshwater species such as T. acipenseri, Amphilina foliacea, Hysterothylacium bidentatum, Piscicapill- aria tuberculata, Chilodonella cyprini, Trichodina domerguei and Argulus foliaceus. Along the Iranian shore of the Caspian Sea, however, the catching of juvenile sturgeons is forbidden by government. Therefore, there is no report about their parasite fauna in this region. Although some researchers have reported Anisakis sp. larvae and Cystoopsis acipenseris from dead juvenile sturgeons (A. Hajimoradloo, personal communications). The parasite fauna of H. huso has been studied by many authors (Dogiel and Bykhovskii, 1939; Shulman, 1954; Nechaeva, 1964; Skryabina, 1974; Bauer et al., 1977) and 33 parasite species have been reported (Holcik, 1989). With great probability, the local populations of the great sturgeon are infested by different aggregations of parasitic worms (Dogiel and Bykhovskii, 1939). Dogiel and Bykhovskii (1939) stated that the stocks inhabiting the northern Caspian region are mostly infested to typical freshwater parasitic worms than those of the southern part of the Caspian Sea. Similarly, in the present study and also in the previous studies (Mokhayer, 1972; Gorogi, 1996b; Sattari and Mokhayer, 2006), more marine typical worms such as E. acipenserinum, Anisakis sp. (L.), E. excisus larvae, C. strumosum and C. sphaerocephalus were found in the great sturgeon. The sample of the sturgeons, particularly A. nudiventris and H. huso, were small in the present study due to decreasing numbers of these species in catching yields. However, with respect to the works of Gorogi (1996a, b) and Sattari and Mokhayer (2006), it seems that expected helminthofauna in the sturgeons of the southern part of the Caspian Sea does not exceed 13-15 species. In this study, C. sphaerocephalus and S. semiarmatus were the most prevalent worms and their mean intensity, abundance and dominance were higher than the others parasites. In addition, E. excisus larvae were mostly found in more carnivorous sturgeons such as H. huso, A. gueldenstaedtii and A. nudiventris. This is likely because E. excisus larvae needs some benthophagous fishes (e.g., Rutilus caspius and Neogobius spp.) as obligatory second intermediate hosts. In the present study, Amphilina foliacea and D. armatum (belonging to freshwater parasite fauna) were not found in the examined sturgeons that have already been reported by Sattari and Mokhayer (2006). This may be because of decreasing spawning migrations of the sturgeons into freshwater, which can be as result of unfavorable conditions of freshwater ecosystems caused by pollution, dam construction, etc. According to the results of this study and the results 422 Int. J. Aquat. Biol. (2015) 3(6): 414-424 of Mokhayer (1972), Gorogi (1996a, b), and Sattari and Mokhayer (2006), the diversity of the sturgeons’ parasites in the southern part of the Caspian Sea is lower than that of the northern part. It should be noted that the maximum depth of the Caspian Sea in the northern part is about 12 m, while in the southern part it is about 980 m. Furthermore, the salinity in the northern part of the Caspian Sea is about 5 ppt, while in the southern part, it is about 13 ppt and may reach to 20 ppt in the southeast region. In addition, the productivity and carbonate ions between the southern and northern parts are different. These factors may have some impacts on the parasite communities of the sturgeons. Based on the results, the diversity of parasites (including freshwater ones) in the southern part of the Caspian Sea have decreased since the time of the first study by Mokhayer (1972). This may be related to unfavorable conditions in freshwater ecosystems, such as pollution and dam construction. In these conditions, it is impossible for the sturgeons to migrate into the rivers for spawning. Acknowledgments We would like to thank Dr. M. Pour Kazemi for providing the laboratory equipment, and the International Research Institute of Sturgeons in Iran and the University of Tehran for their financial supports. References Avdeyev V.V. (1987). Key to parasites of freshwater fishes of the USSR. Vol. 3, Academy of Science of the USSR, 583 p. Bykhovskaya-Pavlovskaya I.E., Gusev A.V., Dubinina M.N., Izyumova N.A., Smirnova T.S., Sokolovskaya A.L., Schtein G.A., Shulman S.S., Epshtein V.M. (1962). Key to parasites of freshwater fishes of the USSR, Academy of Science of the USSR, Zoology Inc. Bauer O.N., Musselius V.A., Nikolaeva V.M., Strelkov Y.A. (1977). Ikhtiopatologiya, Pishchepromizdat, Moskva. (In Russian). Bush A.O., Laferty K.D., Lotz J.M., Shostak A.W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of parasitology, 83: 575-583. Bykhovskaya-Pavlovskaya I.E. (1985). Parasites of fishes. Manual for research. Leningrad, Nauka, 122 p. Daghigh Roohi J., Sattari M., Asgharnia M., Roofchaei, R. (2014a). Occurrence and intensity of parasites in European catfish, Silurus glanis L., 1758 from Anzali wetland, southwest of the Caspian Sea, Iran. Croatian Journal of Fisheries, 72: 25-31. Daghigh Roohi J., Sattari, M., Asgharnia, M., Roofchaei, R., (2014b). Occurrence and intensity of parasites in Prussian carp, Carassius gibelio from Anzali wetland, southwest of the Caspian Sea, Iranian Journal of Fisheries Sciences, 13(2): 276-288. Dogiel V.A., Bykhovskiy B.E. (1939). Parasity ryb Kaspiiskogo morya. Trudy po kompleksnomu izucheniyu Kaspiiskogo morya 7. Izd. Akad. Nauk SSSR, Moskva-Leningrad, 172-173. (In Russian). Dubinin V.B. (1952). Parazitofauna molodi osetrovikh ryb Nizhnei Volgi. Uchen. Zapiski Leningradsk, Gos. Univ., 141, seryia Biologich. Nauk, 28: 238-251. (In Russian) Eagderi S., Mojazi Amiri B., Adriaens D. (2013). Description of the ovarian follicle maturation of the migratory adult female bulatmai barbel (Luciobarbus capito, Güldenstädt 1772) in captivity. Iranian Journal of Fisheries Sciences, 12(3): 550-560. Gorogi A. (1996a). Identification of blood and intestinal parasites of A. persicus in southern part of Caspian Sea. Iranian Journal of Fisheries Science, 1: 35-39. Gorogi A. (1996b). Identification of blood and intestinal parasites of H. huso in southern part of Caspian Sea. Iranian Journal of Fisheries Sciences, 4: 43-47. (In Persian) Holcik J. (1989). The freshwater fishes of Europe, Vol. 1, Part 2, Aula-Verlag, Weisbaden. Khara H., Nezami S., Sattari M., Yousefi R., Saeedi S.E., Goodarzi L. (2009). Parasitic worms of some sturgeons (Acipenseriformes: Acipenseridae) from the southern coast of the Caspian Sea, 14th EAFP International Conference on Diseases of Fish and Shellfish, Prague, Czech Republic, p. 220 Khara H., Sattari M. (2014) Occurrence and intensity of parasites in Wels catfish, Silurus glanis L., 1758 from Amirkelayeh wetland, southwest of the Caspian Sea, Journal of Parasitic Diseases, DOI 10.1007/s 12639- 014-0591-7, online first Leong T.S., Holmes J. (1981). Communities of metazoan 423 Noei et al./Parasitic worms and histopathologic effects in sturgeons parasites in open water fishes of Cold Lake, Alberta, Journal of Fish Biology, 18: 693-713. Mokhayer B. (1972). Recherches sur le parasitisme des esturgoens de La Mer Caspienne Meridionale, PhD Dissertation, Universite de Paris, France. (In France). Moravec F. (1994). Parasitic nematodes of freshwater fishes of Europe, Kluwer Academic publishers. 473 p. Mousavi Sabet H., Sattari M. (2013). First report of Neoechinorhynchus rutili in Cobitis faridpaki (Cobitidae), from the Southern Caspian Sea basin. Ribarstvo Croatian Journal of Fisheries, 97-110. Nechaeva N.L. (1964). Parazitofauna molodi osetrovykh ryb Kaspiisko–Kurinskogo rajona. Trudy Vniro, 54: 223-238. (In Russian) Sattari M., Mokhayer B. (2006). Parasitic worms of Persian sturgeon (Acipenser persicus Borodin, 1897) from the southwest of the Caspian Sea. Bulletin of the European Association of Fish Pathologists, 26(3): 131-136. Sattari M., Mokhayer B., Khara H., Nezami S., Shafii S. (2007). Occurrence and intensity of Parasites in some bony fish species of Anzali wetland from the southwest of the Caspian Sea. Bulletin of European Association of Fish Pathologists, 27(2): 54 - 60 Sattari M., Mokhayer B., Khara H., Roohi J.D., Nezami S. (2008). Parasitic worms of some bony fish species from the southern shore of the Caspian Sea. Bulletin of European Association of Fish pathologists, 28(1): 166-177. Sattari M., Khara H., Nezami S., Ahmadi M.R., Rohii J.D., Balalanfard Z., Faez S., Jafarzadeh A., Taherkhani A., Pourmohammadi R., Mahdaviniya H. (2009). Parasites of some bony fish species in Sourkhankol River from the southwest of the Caspian Sea, 14th EAFP International Conference on Diseases of Fish and Shellfish, Prague, Czech Republic, p. 218 Shulman S.S. (1954). Obzor fauny parasitov osetrovikh ryb SSSR. Trudy Leningradskogo Obshchestva Estetstvoispttatelei, 72: 190-254, (In Russian). Skryabina E.S. (1974): Gel’minty osetrovikh ryb. Izd. Nauka, Moskva (in Russian with English abstract). Stoskopf M.K. (1993). Fish Medicine. W.B. Saunders Co, Philadelphia. Yamaguti S. (1961). The nematodes of vertebrate, Part I, II. Systema helmintum III, Interscience publisher, New York, London, 1261 p. Int. J. Aquat. Biol. (2015) 3(6): 414-424 E-ISSN: 2322-5270; P-ISSN: 2383-0956 Journal homepage: www.ij-aquaticbiology.com © 2015 Iranian Society of Ichthyology چکیده فارسی خزر دریای غربیجنوب سواحل در خاویاری ماهیان از چهارگونه روی بر هاآن شناسیآسیب اثرات و کرمی هایانگل *2ستاری مسعود ،1ابراهیموف شایق ،1نوعی محمدرضا .آذربایجان باکو، آذربایجان، علوم ملی آکادمی جانورشناسی، انستیتو1 .ایران سرا، صومعه گیالن، دانشگاه طبیعی، منابع دانشکده شیالت، گروه2 چکیده: هاآن شناسیآسیب اثرات و ماهیفیل و شیپ چالباش، برون،ازون شامل تاسماهیان از گونه چهار انگلی هایجمعیت وضعیت تعیین برای مطالعه این دریای غربیجنوب شیالتی ناحیه دو در گونه چهار این از ماهی عدد 39 تعداد منظور، این برای. گرفت صورت خزر دریای غربیجنوب سواحل در مطالعه برای آزمایش مورد ماهیان آلوده هایبافت شناسی بافت هایالم. شدند صید 2211 می ماه تا 2212 مارس ماه از( ایران گیالن، استان) خزر شاخص و وانیفرا شیوع، آلودگی، شدت میانگین شامل کالسیک شناختی گیریهمه متغیرهای. گرفتند قرار استفاده مورد هاانگل شناسیآسیب اثرات وسکوکوالن) نماتود دو شامل انگل گونه پنج. شدند محاسبه جنسیت و جغرافیایی ناحیه فصل، اساس بر همچنین و هانمونه تمام برای غالبیت یک و( سفالوسیپالژ لپتورینکوئیدس) آکانتوسفال یک ،(فاالکس بوتریمونوس) سستود یک ،(اکسیسوس یواسترونژیلیدس نوزاد و اسفروسفالوس مورد ماهیان هایبافت روی بر آنها شناسیآسیب اثرات و شدند یافت آزمایش مورد هاینمونه در( آرماتوسسمی اسکریابینوپسولوس) دیژن ترماتود کاهش 1392 سال در مطالعه اولین زمان از خزر دریای غربیجنوب در( شیرین آب هایگونه شامل) هاانگل تنوع نتایج، اساس بر. گرفت قرار ارزیابی . باشد ارتباط در شیرین آب هایاکوسیستم در نامطلوب شرایط با است ممکن امر این. است یافته .چالباش ،شیپ برون،ازونماهی، فیل ،آکانتوسفال ،سستود ،ترماتود :کلمات کلیدی