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Iranian Journal of Fisheries Sciences 15(3) 1067- 1077 2016

Internal parasites of saposhnikovi shad, Alosa saposchnikowii (Grimm, 1887), from the southeastern part of the Caspian Sea, Iran

Mazandarani M. 1*; Hajimoradloo A.M.1; Niazi E.1

Received: March 2015 Accepted: August 2015

Abstract This paper presents the results of a parasitological study on internal parasitic infections in saposhnikovi shad, Alosa saposchnikowii, from the southern part of the Caspian Sea. In this regard 30 fish were studied for abdominal cavity parasites in February 2014. Results showed all of the specimens were infected at least with one kind of parasite and there was no significant difference in parasitic infections between males and females. According to the results three kinds of parasites including one trematode (Pronoprymna ventricosa) and two kinds of ( simplex and Eustrongylides sp) were isolated from the abdominal cavity of the studied fish. 43.33 % of the specimens were infected with A. simplex, 96.66 % were infected with P. ventricosa and 16.66 % of the specimens were infected with Eustrongylides sp. Intensity of infection to A. simplex, P. ventricosa and Eustrongylides sp in saposhnikovi shad was calculated as, 3.46 ± 1.76, 131 ±16.78 and 2 ± 0.71, respectively. According to the results 33.33% intestine, 10% liver and 6.66% mesentery of specimens were infected with A. simplex, 26.66% stomach, 86.66% pyloric caeca and 66.66% intestine of studied fish were infected with P. ventricosa and Eustrongylides sp was isolated in 13.33% mesentery and 3.33% liver of the specimens. It seems this is the first record of A. simplex and Eustrongylides sp infection from saposhnikovi shad in Iran. These parasites are important because of their pathogenicity in fish and zoonotic risk in human health care.

Keywords: Trematode, , Parasites, Alosa saposchnikowii, Caspian Sea

1-Department of Fisheries, Faculty of Fisheries and Environment, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran *Corresponding author’s Email: [email protected]

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Introduction Clupeonella spp and Alosa spp can be Parasites are an important group of found in the Caspian Sea. They are pathogens that cause infection and widely distributed in the southern part diseases in both freshwater and marine of Caspian Sea and Alosa spp is mainly fish. Parasite infestation can be found in seen in the coastal and deltaic areas. most fish in natural environments. This Parasite infections are expected in these fish can not only be host to different fish due to their feeding habit (feeding parasites but also can be the carrier of on crustaceans and small fishes) in many zoonotic parasitic diseases which natural environments. can cause serious problems in many Unfortunately there are few studies vertebrates including human. Parasitic on parasitic infections from clupeidae infections in fish can lead to decrease in family in the Caspian Sea. There are growth rate, weight loss and five records of parasitic infestation emaciation, affect yield of fish from Alosa caspia and three species of products, cause human and animal the Clupeonella in the Caspian Sea diseases, delay in sexual maturity and (Shamsi and Dalimi, 1996; Kornijchuk mortalities (Woo, 2006). and Barzegar, 2005; Varshoie et al., Many studies have been done on 2010; Youssefi et al., 2011; Barzegar et identifying parasitic infestation in some al., 2012 ). There is no record of Caspian Sea fish. It can be noted that a saposhnikovi shad parasites fauna from comprehensive study on the parasites of the Caspian Sea. The aim of this study the southern part in the Caspian Sea is to survey prevalence and intensity of fishes by Mokhayer (1980) reported 29 internal helminthic parasites of A. species of fish parasites. After that saposchnikowii in the southern part of parasite infections have been attributed Caspian Sea. in different fishes of the Caspian Sea by researchers. In this regard studies by Material and methods Malek (1993), Satari and Faramarzi In the present study, parasitic fauna of (1997), Pazooki and Masoumian (1999, the abdominal cavity of A. 2004); Eslami et al. (1972), Mokhayer saposchnikowii in the southeast part of (1974, 1975, 1981), Eslami and the Caspian Sea were studied in Mokhayer (1977), Eslami and February 2014. Fish samples were Kohneshahri (1978), Jalali (1998) etc. caught by purse seine nets by fisherman can be mentioned. Totally, at least more in Behshahr City - Mazandaran than 248 species of parasites were province. Totally 30 fish specimens of recorded from 102 fish species in Iran saposhnikovi shad were studied. After (Pazooki and Masoumian, 2012). biometry, specimens were rinsed and Clupeidae are pelagic fish that play a their abdominal cavities were opened, key role in many food chains. Two and the digestive tract and other organs genera of this family including: (kidney, spleen, liver and mesentery)

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were fully examined for parasites Mean abundance of infection = the total following standard parasitological number of parasites/ the total number of methods. All isolated parasites were surveyed fish counted after washing, and transferred Data were analyzed separately using the to fixative solution and sent to the SPSS software version no.18, and t-test was used to determine the presumptive Iranian National Parasitology Museum, differences between both sexes and Faculty of Veterinary Medicine of the both seasons depending on the Tehran University, for identification. mentioned variables. Data were In this study isolated trematodes presented as mean ± SD and p<0.05 were washed in normal saline (0.6% was considered statistically significant. NaCl), fixed in 70% ethanol, and prepared for microscopic examination Results by staining with iron acetocarmine Totally three helminthes species (Georgiev et al., 1986). Nematodes including , P. were washed in normal saline and fixed ventricosa and Eustrongylides sp were in 4 % formaldehyde, preserved in 70 found in the examined fish. According % ethanol, then the parasites were to the result, all the specimens were cleared in glycerin and stained by lacto contaminated with at least one kind of parasite. The highest prevalence of phenol (Moravec, 1994). Finally, all parasitic infection belonged to P. metazoan parasites were mounted in ventricosa which have been isolated entellan (Merck Co, Germany) after from pyloric caeca, intestine and staining. Drawing of parasites was stomach of 96.66 % of specimens. carried out with the aid of a camera Eustrongylides sp infection showed the lucida fixed on a compound lowest prevalence of parasitic infection microscope. The parasite specimens in this study which was isolated from were deposited in the collection of fish the liver and mesentery of 16.66 % of parasites in the museum. Identification specimens. Infection in A. simplex was was basically those described by Hanek isolated from the liver and intestine of and Fernando (1972) and Roberts infected fish (Tables 2 and 3). 33.33 % of intestine, 10 % of liver and 6.66 % of (2001) mesentery in studied fish were infected Prevalence of infection (%), mean with A. simplex, as well as 26.66 % of intensity and abundance of infection stomach, 86.66% of pyloric caeca and and the limit number of infection were 66.66% of intestine in specimens were calculated according to the following infected with P. ventricosa. In relation formula: to Eustrongylides sp infection, this Prevalence of parasites (%) = the parasite was observed in13.33% of number of infected fish/ the total mesentery and 3.33% of liver in studied number of examined fish×100 fish. Mean intensity of infection = the number of counted parasites/ the total infected fish.

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Table 1: Biometric characters of Alosa saposchnikowii specimens (Mean ± SD). Variables Mean±SD Minimum Maximum Weight (g) 378.06±310 58.00 957.00 Total length (cm) 32.40±7.82 21.00 45.00 Standard length (cm) 27.53±6.83 17.50 38.00

Table 2: Prevalence of parasite infections in Alosa saposchnikowii. Kind of infestation Prevalence Intensity (mean Range Mean (%) ±SD) abundance of infection±SD Total parasite infection 100% 133.2 ± 17.63 1 - 150 133.2 ± 17.63 A. simplex 43.33% 3.46 ± 1.76 1 - 8 1.5 ± 1.12 P. ventricosa 96.66% 131 ±16.78 2 - 150 126.63± 17.33 Eustrongylides sp 16.66% 2 ± 0.71 1- 3 0.33 ± 0.06

Table 3: prevalence, intensity, limit number and abundance of infection in Alosa saposchnikowii. Infected organ Parasites name Prevalence (%) Intensity ± SD Rang Abundance ±SD A. simplex 33.33 2.60±1.45 1-5 0.87±0.45 Intestine P. ventricosa 66.66 34.83±11.83 2-67 33.66±13.25

Pyloric caeca P. ventricosa 86.66 80.83± 28.45 7- 150 78.13±28.44 Stomach P. ventricosa 26.66 15.34±10.06 3 - 35 14.83±10.27

Eustrongylidessp 3.33 2.00±0.36 0-2 0.07±0.36 Liver A. simplex 10.00 4.00±1.54 1-8 0.40±1.54

Mesentery Eustrongylides 13.33 2.00±0.74 1-3 0.27±0.07 sp A. simplex 6.66 3.50±0.97 2-5 0.23±0.08

Based on data analysis, gender had no are presented in Tables 2 and 3. In this significant effects on parasite burden study P. ventricosa had the highest and parasite kinds in A. saposchnikowii intensity of infection in saposhnikovi (Tables 4 and 5). Intensity of infections shad and was mostly isolated from from A. simplex, P. ventricosa and pyloric caeca. Eustrongylides sp in saposhnikovi shad

Table 4: Relationship between sex and parasite burden in Alosa saposchnikowii. Fish Host Sex No. No. Parasitic Significance examined infected load (p=0.05) A. saposchnikowii F 20 20 2643 N M 10 10 1211 F: female, M: male, N: negative (p<0.05).

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Table 5: Relationship between sex and parasite species burden in Alosa saposchnikowii Parasite species Sex No. No. Total Mean Significance examined infected parasitic parasitic (p=0.05) load load A. simplex F 20 9 34 1.70 M 10 4 11 1.70 N P. ventricosa F 20 19 2604 8.97 N M 10 10 1195 1.14 Eustrongylides sp F 20 3 5 0.25 N M 10 2 5 0.50 F: female, M: male, N: negative (p<0.05).

Figure 1: Pronoprymna ventricosa isolated from digestive tract of saposhnikovi shad. Figure 2: Eustrongylides sp isolated from abdominal cavity of saposhnikovi shad.

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Discussion C.engrauliformis, C. cultriventris and Some Caspian saposhnikovi shad C. grimmi from the Caspian Sea. In remain in the southern part of the another study, Varshoie et al. (2010) Caspian Sea all year round, while recorded this parasite from the three others migrate long distances between mentioned fish too. the southern and northern regions of the (Pseudopentagramma, is synonymous Caspian Sea during spring and winter to Pronoprymna, (Chulkova, 1939). for spawning or nutrition (Naderi Kornijchuk and Barzegar (2005) Jolodar and Abdoli, 2004), and this registered P. ventricosa from Caspian long distance migration may increase shad (Alosa caspia persica) in the parasite exposure. In the present study, southern part of The Caspian Sea. all specimens were infected with at Youssefi et al. (2011) and Barzegar et least one parasite. As shown in Tables 3 al. (2012) in different studies isolated and4, there weren’t any differences in this parasite from Caspian shad. In the parasite infection as well as in intensity present study P. ventricosa was isolated of parasitic infestation between from 96.66% of sampled saposhnikovi genders. This can be because of similar shad. This result is in line with nutritional habits in both genders. Barzegar et al. (2012) who isolated this Despite numerous reports in the parasite from 100 % of sampled occurrences of various parasitic Caspian shad. Varshoie et al. (2010) infections in fish of the Caspian Sea isolated P. ventricosa from 53-58% of and basins, there is little information three species of Clupeidae (C. about infection to P. ventricosa in engrauliformis, C. cultriventris and Caspian Sea fish. This trematode has C.grimmi) from the Iranian coastal been isolated from pyloric caeca and regions of the Caspian Sea. Due to intestine of different marine fishes, and similar migration and eating habits in was largely isolated from Clupeidae the clupeide family, infection to P. too. For example, This parasitic ventricosa in other fish of this family in infection has been reported in Alosa spp the Caspian Sea is expected. in the Norheasten Atlantic Sea and As shown in Table 5, A. simplex and Mediterranean Sea (Bray and Gibson, Eustrongylides sp were isolated from 2008), Azov Sea (Nizova and 43.33% and 16.66 % of specimens, Syrovatka, 2000), and Black Sea respectively. Despite reports of these (Koval, 1962; Gaevskaya et al., 2003; parasitic infections in different bony Popjuk, 2009; Ozer et al., 2013). Fish fish of the Caspian Sea (Pazooki and infection to P. ventricosa has just been Masoumian, 2012), it seems this is the reported from Clupeidae in Iran. first record of A. simplex and Shamsi and Dalimi (1996) reported Eustrongylides sp infection from Pseudopentagramma symmetrica in saposhnikovi shad in Iran. These three species including parasites have pathogenic effects on

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fish and human. Dubinin (1952), Dogiel et al., 1997; Audicana et al., 2002). and Bykhovskiy (1939) showed the This parasite has been isolated from pathogenicity of Eustrongylides spp. in shad in other regions (Bao et al., 2015). Ship sturgeon (A. nudiventris) causing Eustrongylides is another zoonotic heavy infections leading to gonad parasite the accidental infection of destruction. which in human, by eating raw infected Eiras and Rego (1988) reported fish can lead to gastritis and intestinal similar changes in South American perforation with severe pain in fishes (Pygocentrus nattereri) with abdominal cavity; this parasite larva granulomatous inflammation and can result in serious damages to patients exudates accumulation due to parasite and sometimes surgical intervention is penetration in somatic muscles and needed for treatment (Deardorff and inner organs. In similar reports of Overstreet, 1991; Cole, 1999). experimental infections in rainbow trout, third-stage larvae of A. simplex Acknowledgements caused considerable cellular reaction in The authors would like to thank the the body cavity and in the tissue staff of the Department of Parasitology penetrated, especially in the pyloric - Veterinary Medicine - Tehran caeca (Santamarina et al., 1994; Larsen University for providing the necessary et al., 2002). Some studies showed facilities. various severity destruction and necrosis of the liver parenchyma and Reference ruptures of the wall of the blood vessels Ancillo, M., Cabalerro,, M.T., in abdominal cavity organs, in Cabanas, R., Contreras, J., consequence of Anisakis spp larvae Baroso, J.A.M., Barranco, P. and migration through infected tissues Serrano, M.C.L., 1997. Allergic (Hauck and May, 1977; Smith, 1984). reactions to Anisakis simplex On the other hand, Anisikis and parasitizing seafood. Annals Eustrongylides are important because of of Allergy, Asthma & Immunology, their pathogenicity in human too. These 79, 246-250. parasites can make serious problems in Audicana, M.T., Ansotegui, I.J., human (via consuming raw or Corres, L.F. and Kennedy, M.W., uncooked infected fish). Anisakis spp 2002. Anisakis simplex: dangerous- larvae can penetrate digestive tract and dead and alive? migrate along intestinal wall, tongue, Trends in Parasitology, 18, 20-25. lung, lymphatic ganglia or pancreas in Bao, M., Mota, M., Nachón, human (Rosales et al., 1999) and lead D.J., Antunes, C., Cobo, F., Garci, to serious clinical signs such as allergic M.E., Pierce, G.J. and Pascual, S., reaction, stomach pain, vomiting, 2015. Anisakis infection in allis nausea and gingivostomatitis (Ancillo shad, Alosa alosa (Linnaeus, 1758),

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